Early experience in minimally invasive esophagectomy for treatment of thoracic esophageal cancer

doi:10.21203/rs.3.rs-2102266/v1

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Early experience in minimally invasive esophagectomy for treatment of thoracic esophageal cancer

https://doi.org/10.21203/rs.3.rs-2102266/v1

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Introduction: Minimally invasive esophagectomy (MIE) has gained popularity in the surgical treatment of esophageal cancer over the past three decades. By introducing minimally invasive techniques, esophageal oncological surgery has advanced in terms of safety, radicality, functional preservation and quality of life post-esophagectomy of the patients.

Material and Method: We present the experience of the Center of Excellence in Esophageal Surgery at Sf. Maria Clinical Hospital regarding total (MIE) through total 3D HD thoraco-laparoscopic modified McKeown triple approach. In between January 2015 - December 2021, 24 patients (M) were treated for thoracic esophageal cancer. The average age of patients was 57 years. Most of the esophageal tumors were midthoracic (62.5%), 83.3% were squamous carcinomas and half were moderately differentiated. Most of the esophageal tumors were locally advanced tumors (cT3N1 – 58.3%), 18 patients were staged III. 70.8% of patients received neoadjuvant chemo radiotherapy.

Results: Thoracoscopic esophageal mobilizations were successful in all 24 patients, no conversion to thoracotomy. Laparoscopic gastric mobilizations were successful in all 24 patients, conversion to open technique was performed in 7 patients for creation extracoporeally of the gastric conduit through an epigastric minilaparotomy. The esophageal substitute was represented by the gastric conduit. The intraoperative blood loss was minimal. The average duration of surgical interventions was 360 minutes. All the surgical interventions were considered with curative intention (R0). The rate of intraoperative complications was 20.8%. The rate of early postoperative complications was 66%. Distribution of postoperative complications according to the Clavien-Dindo Classification (0-33.3%, 1-16.6%, 2-4.1%, 3a-12.5%, 3b-8.3%, 4a-0%, 4b-8.3%, 5-16.6%) highlighted a rate of 33.3% of major complications. The advantages of MIE observed in the studied group in the postoperative period were: reduced postoperative pain, improved comfort and early mobilization of the patients.

Conclusions: The early outcomes of using the minimally invasive approach in the treatment of esophageal cancer in our clinic include the reduction of perioperative morbidity, the duration of hospitalization and a faster recovery.

3D HD minimally invasive esophagectomy

thoracic esophageal cancer

McKeown modified triple approach

total thoraco-laparoscopic approach

Esophageal cancer is nowadays the eight-leading cause of cancer-related deaths [1]. Esophagectomy combined with chemoradiotherapy is the principal strategy in multimodality treatment of resectable esophageal cancer. Esophagectomy with esophageal reconstruction is considered one of the most complex interventions for the treatment of digestive tract neoplasms. Reducing the invasiveness of esophageal resections and achieving better outcomes of patients' quality of life in the postoperative period with an uncompromising oncological result, given the relatively reduced overall survival, have become a priority of the multidisciplinary approach in the treatment of esophageal cancer [2].

Over recent decades, minimally invasive esophagectomy has gained popularity and is increasingly performed worldwide. Minimally invasive esophagectomy (MIE) via thoracoscopy and laparoscopy have reduced the morbidity and mortality of esophagectomy in experienced centers [3].

This study reports an early, single-institution experience of the Center of Excellence in Esophageal Surgery at Sf. Maria Clinical Hospital Bucharest, Romania regarding MIE through thoraco-laparoscopic modified McKeown triple approach for treatment of thoracic esophageal cancer. A retrospective review of a institutional database was performed including patients operated for thoracic esophageal cancer in our centre between January 2015 and December 2021. The study was conducted according to the guidelines of the Declaration of Helsinki. Informed consent is waived by Carol Davila University Ethics and Deontology Commission(CEDU) for this retrospective study.

Institutional Review Board Statement. Ethical review and approval were waived for this retrospective study, according article 6 and article 8 of Code of Ethics and Professional Ethics of Carol Davila University of Medicine and Pharmacy Bucharest adopted in the meeting of the Carol Davila University Senate from 05.07.2011 and endorsed by Ministry of Education with no. 47594/07.10.2011.

Also, we present the technique of minimally invasive esophagectomy through the modified McKeown approach thoracoscopic, laparoscopic and cervical with gastric pull-up through the posterior mediastinum and end-to-side cervical esophago-gastric anastomosis.

Patient selection criteria. Patients who received surgical treatment for thoracic esophageal cancer were included in the study. Patients with cervical or distal esophageal tumors invading the esophagogastric junction and patients with distant metastases in which the esophagectomy was performed for palliative purposes were excluded. Patients with incomplete information in the observation sheets or in the results of paraclinical investigations were also excluded from the study.

Patients were staged and evaluated preoperatively with upper gastrointestinal endoscopy and biopsy, endoscopic ultrasound, abdominal ultrasound, CT TAP and CT-PET when there was a suspicion of disease substadialization. In order to assess the degree of stenosis of the esophageal lumen, in order to palliate the dysphagia (percutaneous endoscopic gastrostomy -PEG), barium swallow was performed in all patients in the studied group.

Clinical staging (cTNM) and pTNM of the esophageal cancer was established according the 7th (2010) and 8th edition (2018) of the American Joint Committee on Cancer (AJCC) cancer staging manual.

After the multidisciplinary consultation, patients with early esophageal cancer received an indication for first-line surgery, while most patients with locally advanced tumors received preoperative radiochemotherapy or neoadjuvant chemotherapy. In addition, all patients underwent ventilatory tests and bronchoscopy was recommended based on the location of the tumor. After neoadjuvant treatment, patients were operated on at approximately 4–6 weeks later. All the risks of minimally invasive esophagectomy were explained to the patients.

We analyzed general patient identification data, age and sex, risk factors, personal pathological history, symptomatology at diagnosis, paraclinical investigations, histological type, operative indication and pre-therapeutic staging, preoperative evaluation, surgical technique, intraoperative incidents, postoperative complications early and late, hospitalization in the intensive care unit, histopathological analysis reports, length of hospital stay and remote oncology results. The postoperative results were evaluated according to the most recent classification of postesophagectomy complications stated by the Consensus Group for Postesophagectomy Complications (ECCG) as well as the Clavien-Dindo classification. Multiple clinical and paraclinical parameters were selected for analysis that were associated with the occurrence of early postoperative complications. Perioperative, clinicopathologic and oncological outcomes were examined. Primary outcome measures were length of hospital stay, morbidity, mortality, lymph node harvest and margin involvement. Secondary outcome measures were overall and disease-free survival from diagnosis.

Methods of statistical analysis. For statistical analysis we used Microsoft Office Excel and IBM SPSS software 20.0. The statistical significance threshold was set at (p < 0.05).

Instrumentation and equipment (Table 1)

Table 1

Instrumentation and equipment.
3D HD laparoscopic surgery kit (3D camera)
Equipment for thoracoscopic stage
Five thoracoport trocars 5-10-12 mm thoracoport trocars
45 mm EndoGIA vascular stapler grey or white cartridge (for the arch of azygos vein)
10mm Hem-o-lok clips
Ultrasonic dissector
EndoFan retractor
Equipment for laparoscopic stage
5-10-12mm trocars
45 mm EndoGIA vascular stapler (for left gastric artery)
linear GIA and EndoGIA staplers of a 60 mm blue or green cartridge
5 mm endoscopic Ligasure instrument
Penrose drain (for isolation of esophagus)
Catheter for jejunostomy

The operating device consisted of selective AG-IOT with Carlens probe. The position of the patient on the table for the thoracoscopic time was for left lateral decubitus, and for the laparoscopic and cervical time for dorsal decubitus (French or American position depending on the operator's preference.

In order to reduce the duration of surgery, we use linear GIA and EndoGIA staplers of a 60 mm blue or green cartridge depending on the thickness of the gastric wall for extracorporeal preparation of the gastric graft when performing the lesser curvature resection with the creation of the gastric tube. For the thoracoscopic approach, we used the left lateral decubitus position and the supine position for the laparoscopic and cervical approach.

Minimally invasive fully esophagectomy surgical technique by modified thoracoscopic, laparoscopic and cervical McKeown approach with gastric pull up through the posterior mediastinum and termino-lateral eso-gastric anastomosis consisted of the following operatives tages: chest stage performed by right thoracoscopic approach in which esophageal mobilization thoracic and mediastinal lymphadenectomy; laparoscopic approach in which the mobilization of the stomach was performed with the sectioning of the left gastric pedicle and perigastric lymphadenectomy and the preparation of the gastric graft and mounting of the feeding jejunostomy. Cervical stage consisted of left lateral cervicotomy with isolation and sectioning of the cervical esophagus and extraction of the subtotal esophagectomy piece and termino-lateral eso-gastric cervical anastomosis. The ascent of the gastric graft was performed by the gastric pull-up technique.

Thoracoscopic stage. For proper intraoperative monitoring, a central venous line and an arterial line are used. We use a high thoracic epidural catheter for additional analgesia. General anesthesia uses a selective oro-tracheal intubation with the Carlens probe, a thick Faucher probe is inserted intraesophageally. The patient is placed in the left lateral decubitus position and the operating table is angled to extend the intercostal spaces. The operating surgeon is located on the right side, and the assistant and the cameraman on the left side of the patient. With the right lung colapsed after selective intubation, the optic trocar is inserted using a 12mm Optiview® trocar in the 8th anterior intercostal space of the midline axillary line that allows a direct view of the anatomical layers and avoids damage to the lung parenchyma in the presence of pleural adhesions. The working trocars are inserted into the right hemithorax so that the distance between them is sufficient to avoid as much as possible the conflicts between the surgical instruments during the operation (Fig. 1).

After the right lung is collapsed and all the trocars are inserted the right hemithorax is explored. CO2 insufflation may be used for further lung collapse up to a pressure of 8 mmHg. After the collapse of the right lung, the anatomical elements are identified: azygos vein, thoracic esophagus, main right bronchi, trachea and pulmonary pedicles.

The first step is the section of the pulmonary triangular ligament at the level of the inferior pulmonary vein with the Ligasure forceps. This is followed by an incision of the lower and upper mediastinal pleura. Carefully any adhesions of the right lung can be cut to avoid damage to the visceral sheet of the pleura which can cause an air leak. A 10 mm “fan” type endoscopic fan is used to retract the lung forward. Dissection of the esophagus and isolation of the azygos vein is facilitated by the presence of the Faucher probe in the esophagus, but for using the vascular stapler it is necessary to remove it in the upper esophagus. The azygos vein arch is sectioned after applying Hem-o-lock clips or after stapling with a 45mm EndoGIA Ultra vascular stappler with white (2.5mm) or gray (2mm) cartridge depending on its size (Fig. 2).

The esophagus is dissected circumferentially along its entire length from the superior thoracic opening to the hiatus, in block with the periesophageal tissue using the ultrasonic dissector or the Ligasure (Fig. 3). The posterior aorto-esophageal vessels are ligated using EndoClips for to prevent postoperative bleeding. If the thoracic duct is highlighted during mediastinal dissection, it is clipped using metal clips to prevent postoperative chylothorax (Fig. 4). The dissection of the subcarinary lymphnodes, is performed carefully around the main bronchi (Fig. 5).

After the complete mobilization of the esophagus, pleural drainage is installed, two tubes connected to Béclaire type drainage, one in the costophrenic sinus and another towards the pulmonary apex. The extraction of the working trocars and the expansion of the lung were performed under visual control (Fig. 6).

Laparoscopic stage. The patient was placed in the French or American laparoscopic supine position. The selective Carlens orotracheal intubation probe is replaced with a single lumen. The position of the trocars for laparoscopic stage is described in the Fig. 7.

The patient was placed in the Fowler position. If the patient had a feeding gastrostomy, it was removed preoperatively and the gastrostomy was closed with Silk 3 − 0 threads. The stomach was mobilized on the large and small curvature, by sectioning of small omentum and gastrocolic ligament with the protection of the marginal vascular arches (Fig. 8, Fig. 9). The abdominal esophagus is isolated, joining the dissection plane with the thoracic one, the hiatus is widened through the section of the right and left pillars using Ligasure forceps.

Laparoscopic gastric mobilization is continued by sectioning the coronary pedicle using a vascular stapler or Hem-o-lok clips at the origin of the left gastric artery in the celiac trunk and performing perigastric lymphadenectomy with the graft of the right gastroepiploic pedicle as the arterial source of the graft (Fig. 10, Fig. 11). Kocher duodeno-pancreatic manoeuvre is performed for further mobilization of the future gastric conduit.

Neck stage. An incision of 5–6 cm was made at the anterior edge of the left sterno-cleidomastoid muscle. Through the incision of the platysma, it enters the retrothyroid at the median edge of the left vascular-nervous pedicle of the neck to the level of the prevertebral fascia. The esophagotracheal angle is highlighted and the esophagus is carefully dissected from the tracheal membrane. The cervical esophagus was dissected and the left laryngeal recurrent nerve was identified. For the middle and upper tumor sites, the stomach is fully mobilized according to the Nakayama technique (Fig. 12, Fig. 13). For the lower esophageal cancers, according to the Akiyama technique, the stomach is tubulated on the great curvature using two linear GIA-type staplers with partial excision of the small curvature.

For total minimally invasive technique, after closing the cardia with a linear stapler, a single-layer end-to-side esophago-gastric cervical anastomosis is performed between the cervical esophagus and the gastric conduit with separate threads of PDO 3 − 0 or thread surjet of Maxon 4 − 0. After the end of the posterior layer, a nasogastric tube is inserted into the ascending intrathoracic conduit. The anterior anastomotic layer is performed in the same manner (Fig. 14).

For extracorporeal preparation of the gastric conduit, an epigastric minilaparotomy is performed by prolonging the incision of the optic trocar. The esophagus is cut at the cervical level 3–4 cm above the upper thoracic opening, the distal stump is ligated with silk 2.0, then the esophagectomy piece is anchored to a Levine tube and then it is extracted with the stomach at the level of the epigastric laparotomy.

Sectioning of cardia or creation of gastric conduit is performed (depending on the chosen reconstruction technique) using a stapler with a green or blue cartridge depending on the thickness of the gastric wall. The resection area is reinforced with a 3 − 0 PDO thread. The gastric conduit is anchored to a Levine probe at the proximal point of the fornix and is ascended by the transmediastinal gastric pull-up technique in the former esophageal bed. A gastrotomy is then performed at the level of the fornix and a wide anastomosis is performed in the total eso-gastric layer in the manner already presented. Feeding jejunostomy is inserted on the Foley 20 Ch catheter (Fig. 15). Juxtaanastomotic cervical drainage of cervical anastomoses is optional (Fig. 16).

Postoperative period. Most patients were extubated in the operating room. Early mobilization and respiratory physiotherapy were used to reduce respiratory complications following an integrated post-esophagectomy care protocol. Assessment of recurrent nerve damage was performed on the first postoperative day. Pleural drainage was removed when the daily amount drained was minimal and no air fistula was found, however mediastinal drainage may wait until confirmation of anastomotic integrity. The high epidural anesthesia catheter was generally used in the first three day postoperatively. Feeding through the jejunostomy tube was initiated in the first 24 hours postoperatively (Fig. 17). Anastomosis contrast control was usually performed on the fifth postoperative day and, if normal, patients were gradually initiated an oral diet depending on their ability to have normal swallowing. At discharge, the patient wase fed with solid food, and the feeding jejunostomy was maintained until the first check-up at one month postoperatively, when it was suppressed after a new check-up with barium swallowing (Fig. 18).

Follow up

Patients were re-evaluated every 3 months in the first year, every 6 months in the second year and every year thereafter, or whenever necessary, if postoperative complications occur at a distance.

4.1. Patients

Between January 2015 and December 2021, 24 patients (male) were treated for thoracic esophageal cancer by the modified thoracoscopic, laparoscopic and cervical modified triple McKeown approach. The mean of age at the time of surgery was 57.6 (range 44–75) years, and the mean body mass index was 23.31 (range 17-29.76).

Five (20.8%) patients were exposed to occupational hazards and 91.6% of patients were smokers. The average value of the Brinkman index was 505.6 (range 100–800). 62.5% of patients were alcohol consumers. At the time of diagnosis, 54.1% of the total number of patients had dysphagia for solids (Takita score 2), 79.1% of patients reported weight loss, 37.5% of patients reported gastroesophageal reflux, and symptoms began on average with an average interval of 75 days before diagnosis. In the patient’s group, 25% of patients had a history of hypertension, 12.5% of patients had been diagnosed with ischemic disease, 16.6% had chronic obstructive pulmonary disease, 8.3% had hiatal hernia, 20.8% had documented reflux esophagitis, 25% had chronic gastritis or history of gastric ulcer, 12.5% had dyslipidemia, 16.6% had hepatic steatosis. The mean Charlson index of comorbidities was 3.6.

Most esophageal tumors were midthoracic (62.5%), 83.3% were squamous cell carcinomas 33.3% were non-keratinizing and 20.8% were keratinizing, and half were moderately differentiated G3 tumors (50%). Most esophageal tumors were locally advanced tumors -cT3N1(58.3%). The average length of the tumors was 3.2 cm (range 1-5cm). All patients included in the study were diagnosed with localized esophageal cancer (cM0), 18 patients were in stage III (75.5%). 41.6% of patients benefited from palliation of dysphagia (percutaneous endoscopic gastrostomy) preoperatively. 70.8% of patients received neoadjuvant chemoradiotherapy (Table 2).

Table 2

Patients characteristics.
	No. of patients All (n = 24)	%
Age(mean)	57
Male	24
Body mass index – BMI (mean)	23.3
Co-morbidities
Charlson index	3.6
Tumor location
Upper thoracic	2	8.3%
Midthoracic	15	62.5%
Lower toracic	7	29.1%
Histopathological result preoperative
Squamous cell carcinoma	20	83.3%
Adenocarcinoma	4	16.6%
Clinical T stage
T1	3	12.5%
T2	4	16.6%
T3	16	66.6%
T4	1	4.16%
Clinical N stage
N0	4	16.6%
N1	18	75%
N2	2	8.3%
Clinical stage
Stage I	3	12.5%
Stage II	3	12.5%
Stage III	18	75%
Stage IV	0
Neoajuvant chemoradiotherapy	17	70.8%
Preoperative risk assement
ASA 2	4	16.6%
ASA 3	20	83.3%
ECOG
0	11	45.8%
1	9	37.5%
2	4	16.6%

After performing neoadjuvant radiochemotherapy (RCT), patients were re-evaluated endoscopically and imaging. Applying RECIST criteria, a complete response was obtained in 29.1% of patients. The mean hemoglobin value was 13.41 g/ dL (range 11-16.6), 41.6% of patients had preoperative anemia. The mean total serum protein was 7.16 g / dl (range 6.17–7.87). 83.3% of patients were in the 3rd class of ASA. The mean Karnofsky index was 82.5, the ECOG performance score was 0 in 45,83% of patients. 19(79.1%) patients had normal ventilatory tests preoperatively.

4.2. Operative results

Thoracoscopic esophageal mobilizations were successful in all 24 patients, no conversion to thoracotomy. Laparoscopic gastric mobilizations were successful in all 24 patients, 7 (29.1%) patients required extracorporeal preparation of the gastric graft by epigastric mini-laparotomy (Akiyama technique). All surgeries were considered curative, all esophagectomies were R0. The median operative time was 360 minutes (range 300–420 minutes), the median average time of thoracoscopic stage was 120 minutes (range 100–150 minutes) and the median average time of laparoscopic stage was 180 minutes (range 120–200 minutes). The esophageal substitute was represented by the gastric conduit in all the patients. Intraoperative blood loss was minimal. 29.1% of patients in the group received blood transfusions intraoperatively. We used the Nakayama technique for esophageal reconstruction with the whole stomach in 17 (70.8%) of the patients, and we used the stomach tubing according to the Akiyama technique in 7 (29.1%) of the patients. Pyloroplasty was performed in 4 patients (16.6%) and the gastric graft was ascended through the posterior mediastinum in all patients. Restoration of digestive continuity was done after ascending the gastric conduit to the cervical level by a hand-sewn end-to-side monolayer esophago-gastric anastomosis with separate threads in 95.8% of the patients.

Intraoperative complications. The rate of intraoperative complications was 20.8%. Intraoperative complications consist in damage of thoracic duct, pulmonary parenchima and spleen. The intraoperative complications were managed without conversion to open surgery.

4.3. Perioperative Outcomes

Postoperative complications. The rate of early postoperative complications was 66%. One patient (4.1%) required emergency reoperation in the first 24 hours for air leak when a pericardial patch was applied on thrachea. Clavien-Dindo classification highlighted a rate of 33% (8 patients) of major complications (Table 3).

Table 3

Clavien-Dindo classification.
Clavien Dindo grade 0 1 2 3a 3b 4a 4b 5 in-hospital mortality	No. of patients (%) 8 (33.3%) 4 (16.6%) 1 (4.1%) 3 (12.5%) 2 (8.3%) 0 2 (8.3%) 4 (16.6%)
Minor complications	8 (33.3%)
Major complications	8 (33.3%)

The rate of fistular complications was 41.6%. Most fistulas were grade III (50%) acordind Consensus Classification of Esophagectomy Complications (ECCG) and required reoperation. The rate of pulmonary complications was 54.1%. 3 patients with anastomotic leakage and cervical abscesses developed esophago-gastro-tracheal fistula. One patient had Covid-19 pneumonia. Excluding patients with anastomotic leak, a post-operative pulmonary complication rate of 25% was found.

The rate of postoperative cardiac complications was 12.5%. Thromboembolic complications were diagnosed in a patient (4.1%) with Covid-19 infection. Postoperative intrathoracic bleeding was managed conservatively in one patient. Postoperative bleeding from inferior thyroidian artery in a patient with anastomotic fistula required multiple reoperations. There was no recurrent laryngeal nerve injury intraoperative or postoperative in the study group.

The rate of gastrointestinal complications, other than fistular (Clostridium difficile colitis) was 4.1%. Gastric conduit necrosis was found in 2 patients (8.3%). The thoracic duct injury grade III was discovered postoperatively in a patient (4.1%), when a large amount of pleural drainage with a lactescent appearance was found. The rate of postoperative sepsis was 29.1% and they appeared in the evolution of fistular complications in 6 patients. The rate of wound infections was 33.3%, most of which were associated with cervical anastomotic leakage (Table 4).

Table 4

Early postoperative major complications.
Morbidity	No of patients (%)
Early postoperative complications	16 (66.6%)
Anastomotic fistula	10 (41.6%)
ECCG grade of anastomotic fistula 1 2 3	1 (10%) 4 (40%) 5 (50%)
Gastric conduit necrosis	2 (8.3%)
Chylothorax	1 (4.1%)
Pulmonary complications	13 (54.1%)
ARDS	9(37.5%)
Pleural effusion	9(37.5%)
Pleural empyema	4(16.6%)
Pneumothorax	9(37.5%)
Tracheal membrane injury	1(4.1%)
Esophago-gastro-tracheal fistula	3(12.5%)
Covid-19 pneumonia	1(4.1%)
Cardiac complications	3(12.5%)
Thrombotic complications	1 (4.1%)
Postoperative hemorrhage	2 (8.3%)
Sepsis	7 (29.1%)
Wound infections	8 (33.3%)

Treatment of postoperative complications. Treatment of early postoperative complications was required in 14 (58.3%) patients. Two thoracoscopic reinterventions were performed in the same patient to clip the injured thoracic duct. Reoperation rate for anastomotic leakage was 29.16%. Reoperations included drainage of cervical abscess, right thoracoscopy with drainage and lavage of the pleural cavity, endosponge vacuum and endoscopic stenting. Returning to operating room was required for the treatment of gastric conduit necrosis in two patients when resection of stomach and cervical esophagostomy were performed. In patients without piloric drainage in postoperative period the air distension of the intrathoracic stomach was managed with aspiration of intragastric air every 4 hours through nasogastric tube.

Hospitalization. The mean length of hospital stay in the intensive care unit (ICU) was 8.5 days (range 2–33). The mean period of days ventilation of patients in ICU was 2.4 days (range 1–23). The mean duration of postoperative hospitalization was 20 (range 2–61) days. The mean value of total hospitalization was 25.9 days (range 4–64). In patients without major postoperative complications the mean length of hospital stay in the ICU was 5.5 days (range 3–7), the mean duration of postoperative hospitalization was 12.8 days (range 10–18), and the mean duration of total hospitalization was 17.7 days (range 14–26). Hospital readmission rate was 16.6%. Patients were readmitted for management of complications of anastomotic fistula or replacement of feeding jejunostomy.

Postoperative mortality. The in-hospital postoperative mortality rate in the first 30 days was 8.33% (2 patients died). The postoperative mortality rate in the first 90 days was 16.6% (4 patients died). In hospital mortality has been associated with complex cervical anastomotic fistula, damage of trachea and septic shock with multiple organs failure.

4.4. Long-term outcomes

The rate of delayed postoperative complications was 54.1%(13 patients). The rate of delayed surgical postoperative complications (incisional hernia, diaphragmatic hernia, small bowel obstruction) was 37.5%. The incidence of late pulmonary complications (aspiration pneumonia, pleural effusion, Covid-19 infection) was 25%, and the incidence of late cardiac complications was 8.3%. The incidence of secondary anemia in the first 6 weeks postoperatively was 12.5%. In his new anatomical localisation, the gastric reservoir was exposed to several complications. The incidence of erosive gastritis was 12.5%, and 4.1% of patients reported postoperative reflux. Delayed gastric conduit emptying was diagnosed in 7 patients (29.1%)(Table 5).

Table 5

Delayed postoperative major complications.
Morbidity	No of patients (%)
Delayed postoperative complications	13 (54.1%)
Incisional hernia	3 (12.5%)
Diaphragmatic hernia	2 (8.3%)
Small bowel obstruction	1 (4.16%)
Erosive gastritis	3 (12.5%)
Delayed gastric emptying	7 (29.1%)
Swallowing disorders	4 (16.6%)
Dysphagia	10 (41.6%)
Postoperative reflux	1 (4.1%)
Stenosis of anastomosis	8 (33.3%)
benign	7 (29.1%)
malignant	1 (4.1%)
Pulmonary complications	6 (25%)
Covid-19 infection	2 (8.3%)
Cardiac complications	2 (8.3%)
Anaemia	3 (12.5%)

The rate of swallowing disorders was 16.6%. The healing process of the eso-gastric anastomosis led to the appearance of stenosis in 33.3% of the total number of patients. Regarding the etiology of anastomotic stenosis, it was benign in 7 patients (29.1%) and it was of malignant in one patient (4.1%). The resumption of oral feeding was difficult for some patients who complained of dysphagia after surgery. Late postoperative dysphagia affected 41.6% of patients.

Treatment of long-term complications. Pneumatic and boujie dilations and esophageal stenting were performed for management of postoperative dysphagia. Bowel obstruction by transdiaphragmatic hernias of the intestinal loops required emergency laparotomy.

4.5. Pathological results

The distribution of final anatomopathological results was as follows: 62.5% of the results were squamous cell carcinoma, 12.5% were adenocarcinomas, and in 20.8% of patients the presence of residual tumor was not determined on the main specimen. In one patient (4,1%) tumor cell were found only in the lymhpnodes. The distribution of the type of keratinized / non-keratinized squamous cell carcinoma highlighted the preponderance of keratinized squamous cell carcinoma (33.3%). A reduction in tumor size was observed in 66.6% of patients. All esophagectomy specimens had resection limits without tumor infiltration (R0). The distribution of residual tumors according to the Mandard tumor regression classification (TRG) showed that 25% of the esophagectomy specimens had tumor cells (grade 2) and 25% of the resection specimens did not contain residual tumor cells. 29.1% had venous invasion, 37.5% had perineural invasion, 33% had lymphatic invasion.

The distribution of cases according to the anatomopathological results of pT and ypT revealed the preponderance of pT3 (21.4%), followed by ypT0, ypT1b, pT1B, ypT2, ypT3 with 14.3%. The pN distribution revealed the preponderance of pN0 (71.4%)(Table 6).

Table 6

Pathological results.
	No of patients (%)
Pathological stage
Complete response	5 (20.8%)
Stage IB	6 (25%)
Stage IIA	1 (4.1%)
Stage IIB	8 (33.3%)
Stage IIIA	4 (16.6%)

A large number (298) of lymph nodes resected by minimally invasive approach was found, the average value of the number of lymph nodes analyzed was 12.41 (range 2–45). The mean value of the invaded lymph nodes was 0.45 (range 0–4). The ratio of invaded / analyzed lymph nodes was 0.036. The mean value of the lymph nodes identified on the esophagectomy specimen was 3.2 (range 2–15). The mean number of lymph nodes identified in the periesophageal and perigastric tissues was 9.1 (range 1–43). The distribution of cases according to the degree of differentiation revealed the preponderance of poorly differentiated G2 tumors 37.5%. The distribution of patients according to the final anatomopathological staging highlighted the preponderance of stage IIB (33.3%). 37.5% of patients received adjuvant chemotherapy.

4.6. Survival

20 (83.3%) patients (2 deaths in the first 30 days, 2 deaths due to postoperative major complications in the first 90 days postoperatively) survived surgery for the treatment of thoracic esophageal cancer. The overall rate of medically documented recurrence was 12.5% (3 patients). Local recurrence was diagnosed in 2 (8.3%) patients (604 days after surgery). The overall rate of medically documented systemic recurrence was 4.1% (1 patient) (1289 days after surgery).

As of December 31, 2021, 12 (50%) patients who survived esophagectomy by minimally invasive approach were alive.

The mean disease-free survival time was 33.3 months. The median patient’s disease-free survival time was 21.3 months (Fig. 19.). The average survival of patients after recurrence was 164 days (range 108–180 days). The mean survival time to death was 34.1 months. The median patient’s survival time was 21.3 months. The overall survival rates at 1, 3 and 5 years were 68%, 50% and 28% (Fig. 20).

Esophageal cancer is frequently diagnosed in elderly patients with multiple comorbidities, in which the rate of occurrence of post-esophagectomy complications is very high [4].

Current treatment of esophageal cancer involves multidisciplinary cooperation for the preoperative setting or for the management of postoperative complications. Transthoracic esophagectomy remains the current therapeutic standard for thoracic esophageal carcinoma. Esophagectomy with esophageal reconstruction is a complex procedure associated with considerable morbidity and mortality.

Multiple strategies have been proposed for optimal patient management, including patient selection, nutrition optimization, identification of risk factors involved in early postoperative complications, treatment in experienced centers, minimally invasive techniques, specific intraoperative anesthetic and surgical measures, direct start of oral feeding after surgery and the use of standardized postoperative recovery protocols in order to achieve a textbook outcome [5].

In the studied group the localization of mediotoracic predilection of esophageal cancer overlaps with the eastern model of distribution of cases depending on the location. The average size of esophageal tumors of 3.2 cm reflects the evolution of longitudinal intraluminal invasion before the onset of the first symptoms of dysphagia.

Although the use of barium swallow in the initial assessment of esophageal cancer is less and less reported in the literature, it is very useful in assessing the extent of esophageal tumor. The histological diagnosis also confirms the inclusion in the Eastern pattern of incidence of esophageal squamous cancer. Pre-therapeutic staging of cTNM shows in more than two-thirds of cases the presence of locally advanced tumors with invasion in the muscular tunics of the esophagus. These are obviously associated with periesophageal lymph node metastatic deposits.

A very high percentage of patients received neoadjuvant radiochemotherapy. Esophageal squamous cell carcinoma is associated with a good clinical response to neoadjuvant treatment. In the preoperative evaluation, the stratification of the surgical risk is essential for choosing the optimal approach to obtain a low postoperative morbidity and mortality. The Charlson comorbidity index and the biological performance status assessment can guide us in the optimal choice of treatment [6].

Minimally invasive surgery has been proposed as an alternative to open surgery and has been shown to be at least equivalent in terms of early and long-term outcomes. Advanced technology and optics of endoscopic surgery allow better assessment of anatomical plans, a very good access to narrow spaces, and therefore a more precise dissection with lower trauma in esophageal cancer surgery. The long learning curve of minimally invasive approach is much easier to overcome in the presence of an experience in open esophagectomy. Also, advanced technical skills in minimally invasive surgery and the supervision of a mentor are mandatory for the first operations. MIE allows the simplification of postoperative healthcare, the reduction of the incidence of postoperative complications, especially pulmonary, the reduction of hospitalization time and a faster social reintegration. In large series and randomized clinical trials, the results of minimally invasive esophagectomy showed lower postoperative morbidity compared to open esophagectomy [7]. Minimally invasive esophagectomy is an advanced technical surgical procedure with a prolonged learning curve and it requires extensive experience in open esophageal surgery [8]. Minimally invasive esophagectomy can be performed safely after neoadjuvant treatment which may include immunotherapy and chemoradiotherapy [9]. Taking into account the results from the immediate postoperative period but also the long-term oncological ones, MIE has become the standard surgical treatment in some countries given the low availability and high cost of using robotic technology [10].

Minimally invasive esophagectomy by the modified McKeown triple approach was introduced in the Center of Excellence in Esophageal Surgery, Clinical Hospital “Sf. Maria” Bucharest in 2015 in order to reduce the rate of pulmonary complications. Although technically complex, combined laparoscopic and thoracoscopic esophageal resection is feasible. MIE offers excellent visual field for mediastinal lymphadenectomy including around the recurrent laryngeal nerve [11].

Image augmentation in the operative field and the use of a 3D High Definition video camera provides an excellent visual field for accurate aproximation of the dissection plans and overcome difficult moments by reducing the risk of intraoperative accidents and also enables an extensive periesophageal and perigastric lymphadenectomy facilitating a better staging [12].

Minimally invasive esophagectomy is associated with high costs of endoscopic surgical instruments, however the choice of a type of approach for the benefit of patients should not be conditioned by the costs of surgery. The use of appropriate instruments adapted to both thoracoscopic and laparoscopic time is essential to perform this procedure safely and to reduce the duration of surgery [13].

Intraoperative management of patients undergoing esophageal surgery can be difficult due to a variety of surgical and anesthetic problems (bleeding, hypotension, hypoxemia, bronchial or trachial tear). Communication between the surgical and anesthetic team is very important to prevent any incidents. Thoracoscopic mediastinal dissection can be technically difficult due to anatomical, clinicopathological factors (tumor stage) or post-radiochemotherapy adhesions. Thus, hemorrhagic incidents may occur that can be resolved by minimally invasive approach or cause conversion to open surgery (the average conversion rate reported in the literature is 5–7%) [14]. The need for intraoperative blood transfusions is low in patients who received a minimally invasive approach.

We are still in the learning curve of this type of minimally invasive approach, and we used the left lateral decubitus to be able to convert to open surgery via emergency thoracotomy in case of an accident during surgery.

The consequences of unrecognized intraoperative accidents intraoperatively become evident in the postoperative period (chylothorax after thoracic duct damage, air fistula) [15].

Laparoscopic mobilization of the stomach is associated with a risk of bleeding or injury to the left gastroepiploic pedicle, especially during the learning curve. Evaluation of venous drainage, optimal sizing of the hiatus, avoidance of tension in the graft by proper mobilization including duodeno-pancreatic detachment or extracorporeal preparation are important factors in preventing its ischemia.

Esophageal reconstruction is as important as esophagectomy itself because its success is reflected in postoperative morbidity. The stomach was the preferred organ in esophageal reconstruction in our department due to its good vascular supply, it is long enough to avoid tension in the anastomosis and is easy to prepare by laparoscopic approach, and to restore digestive continuity it is necessary to perform a single anastomosis. In the analyzed group, the stomach represented the esophageal substitute in all patients, both as an integrated gastric reservoir and in the tubular version. There were no difficulties in preparing the gastric graft in patients who benefited from palliative dysphagia by mounting a feeding gastrostomy.

In order to avoid the complications related to the viability of the graft in the first cases, its preparation was done extracorporeal by externalization through an epigastric mini-laparotomy, being recommended in the period of the learning curve [16]. In order to reduce complications related to viabily of the gastric conduit use of indocyanine green is recommended to asses intraoperatively the perfusion of the stomach [17].

Performing the pyloroplasty on vagotomised stomach is not absolutely necessary and we do not recommend it routinely, usually, the emptying of the gastric conduit is improving in the first few weeks postoperatively. Endoscopic pyloromyotomy was proposed as an alterantive for pyloric drainage [18]. Feeding jejunostomy is used routinely in our department to facilitate enteral nutrition in the postoperative period [19].

The use of standardized postoperative perioperative clinical protocols facilitate the reduction of postoperative complications in esophageal cancer surgery [20].

Esophageal surgery involves extensive mediastinal dissection that can cause trauma to the lung parenchyma and some peribronchial nerve elements. Esophagectomy is associated with an increased risk of inoculation of a sterile area with germs from the digestive tract, conditions that can lead to a generalized inflammatory syndrome (SIRS).

We use high epidural anesthesia to control pain in the immediate post-operative period, that facilitates early extubation and mobilization of the patient which reduces the rate of respiratory complications, duration of hospitalization and improves quality of life. We support active respiratory physiotherapy and start of early feeding on the jejunostomy on the first day after surgery which, in our experience, is well tolerated by the patient. The changes in consciousness and infectious risk are carefully assessed by repeating laboratory tests and pulmonary x-rays to identify possible postoperative medical or surgical complications.

Complications in the immediate postoperative period specific to esophagectomy (airway fistula, volvulus or necrosis of the gastric graft, thoracic duct injury, recurrent bilateral paralysis of the nerve) may in some cases require emergency reoperation [21].

When there is a suspicion of gastric graft viability, it can be assessed endoscopically from the first postoperative day if all other non-invasive diagnostic methods have been exhausted. Reintervention may include thoracoscopic / right thoracotomy, as appropriate, for graft excision, thoracic duct ligation in the hiatus, airway fistula sealing, or other additional surgical procedures (cervical esophagostomy, tracheostomy). Use of near infra-red fluorescence may help identification of thoracic duct and reduce the risk of chyle leak postoperatively [22].

Respiratory, cardiac and anastomotic fistula complications may affect the prognosis of patients requiring readmission to the intensive care unit. Pulmonary complications are common after esophagectomy (30–60%), about 80% are early and occur in the first 5 days postoperatively (atelectasis, bacterial pneumonia and adult respiratory distress syndrome - ARDS) [23]. The use of the minimally invasive approach reduced the incidence of lung complications by reducing the manipulation of the lung parenchyma and the use of atraumatic instruments in mediastinal dissection. Intraoperative and postoperative fluid administration may be a contributing factor to the development of respiratory complications after esophagectomy [24]. Esophago-gastric neck anastomosis is associated with significant swallowing and tracheobronchial aspiration problems, which may increase the risk of postoperative pulmonary complications. Neoadjuvant treatments have not been associated with a significant increase in the risk of pulmonary complications if the minimally invasive approach is used [25]. Coronavirus pandemic (COVID-19) has had an impact on the treatment of cancer patients globally by limiting access to healthcare [26]. The increased risk of in-hospital infection in a category of patients such as those receiving esophagectomy and requiring long-term care in the intensive care unit added the additional risk of spectrum of thromboembolic lung damage specific to Sars-Cov-2 virus infection. In the studied group, the infection with Sars-Cov-2 caused in a patient the appearance of a formidable complication, that of gastric conduit necrosis at 6 days postoperatively, which required emergency reintervention and excision of the graft at 11 days postoperatively.

Anastomotic fistula after esophagectomy is a major postoperative complication, has an incidence of 5–20% of cases and can cause a 30-day mortality rate of 2.1–35.7% [27]. The causes that amplify the severity of this complication are both the anatomy of the esophagus and the location of the anastomosis and is not influenced by the minimally invasive approach. Cervical eso-gastric anastomosis has an increased risk of fistular complications [28, 29]. When the presence of anastomotic fistula was combined with general signs and symptoms, the appearance of mediastinitis, systemic inflammatory response or sepsis, it required endoscopic interventions - type II (endoscopic stenting) or reoperation (type III) [30]. In order to reduce the incidence of anastomotic leakage several performing techniques of esophagogastric anastomosis have been proposed by various authors with a reported anastomotic leakage rate of 2.0% [31]. In order to reduce the risk of anastomotic stenosis triangular stapling technique has been proposed for cervical anastomosis [32]. Some authors considered to reconstruct the upper mediastinal pleura or to cover the anastomosis with great omentum in order to reduce the postoperative complications related to anastomic leakage in mediastinum which was used by us for some cases when omentum was available [33]. Our experience using the Endo-vacuum technique with EndoSponge is limited to a few cases and is being evaluated for feasibility in our department [34].

Anastomotic fistula prolonged the duration of postoperative hospitalization and the duration of total hospitalization in the study group. Also, anastomotic fistular complications have influenced intraoperative postoperative mortality. Postoperative pulmonary complications increased the duration of postoperative hospitalization. In the study group, patients without fistular complications did not have postoperative wound infections.

Inadequate calibration of the hiatal orifice and the absence of peritoneal adhesions following minimally invasive surgery predisposes to hernia complications in the postoperative period that may require emergency surgery for intestinal obstruction. The recommendation of several authors is that the repair to be performed if possible in a center specializing in esophageal surgery [35].

The number of lymph nodes in the excision piece after minimally invasive surgery is appropriate, obviously due to the higher exposure of the operating field [36].

Given the disappointing long-term outcomes of esophagectomy, achieving good post-operative quality of life outcomes should become an important goal for the surgical treatment of esophageal cancer [37, 38].

The objective of this study was to report the initial experience of introducing the minimally invasive esophagectomy for surgical treatment of esophageal cancer in a Romanian tertiary health service. Patient safety was the priority of implementing the technique and not the achievement of superior results of minimally invasive esophagectomy. The accumulated experience of the cases allowed us to perform the minimally invasive integral esophagectomy and the successful use of 3D HD video optical technology. The advantages of MIE observed in the studied group were also related to collaboration with patients in the postoperative period: reduced postoperative pain, improved comfort and early mobilization of the patients. The accumulation of a larger number of cases would allow us a more consistent and accurate assessment of the benefits of minimally invasive techniques in the postoperative period as well as long-term oncological results. Performing a thoracoscopic esophagectomy in the prone or semi-prone position for thoracoscopic stage, as well as introducing robotic technique, could be solutions to the unresolved issues.

Although the postoperative surgical results did not live up to expectations and a small number of patients were analyzed, one of the most important objectives of implementing minimally invasive techniques in the surgical treatment of thoracic esophageal cancer is the Center of Excellence in Esophageal Surgery at the Clinical Hospital. "St. Mary" was successfully reached.

There has been an international trend to replace open esophagectomy with minimally invasive esophagectomy in centers with experience in esophageal surgery which is an important step for MIE to become gold standard of surgical treatment of thoracic esophageal cancer [39]. This study has some limitations the number of patients included in this study is small. Also, long-term results are still being evaluated for some patients.

The surgical approach of the esophagus is difficult and reserved for centers specializing in esophageal pathology, because it is associated with considerable morbidity and mortality and a long postoperative recovery. Minimally invasive esophagectomy is a less traumatic surgical procedure with easier postoperative recovery. MIE allows the simplification of postoperative healthcare, the reduction of the incidence of postoperative complications, especially pulmonary, the reduction of hospitalization time and a faster social reintegration.

By introducing minimally invasive techniques, esophageal oncology surgery has progressed in terms of safety, radicality and functional preservation, which has led to an improvement in patients' quality of life after surgery. The early outcomes of using of the minimally invasive approach in treatment of esophageal cancer in our clinic include the reduction of perioperative morbidity, the duration of hospitalization and a faster recovery. Even though minimally invasive surgical techniques are used, esophagectomy is associated with an increased rate of postoperative complications related to the onset of anastomotic fistula.

This preliminary experience suggests that minimally invasive esophagectomy is safe and feasible in centers with experience in advanced minimally invasive surgical procedures. The learning curve of the minimally invasive esophageal surgical technique can only be completed after the learning curve of open esophageal surgery and advanced minimally invasive surgery techniques.

Ethics approval and consent to participate

Ethical statement

The study was conducted according to the guidelines of the Declaration of Helsinki. Informed consent is waived by Carol Davila University Ethics and Deontology Commission(CEDU) for this retrospective study.

Institutional Review Board Statement: Ethical review and approval were waived for this retro-spective study, according article 6 and article 8 of Code of Ethics and Professional Ethics of Carol Davila University of Medicine and Pharmacy Bucharest adopted in the meeting of the Carol Davila University Senate from 05.07.2011 and endorsed by Min-istry of Education with no. 47594/07.10.2011.

Consent for publication

Each patient has given informed consent to publish identifying information/ images relevant to them in an online open access publication prior to surgery.

Availability of data and materials

The datasets generated and/or analysed during the current study are not publicly available due to privacy and ethical concerns but are available from the corresponding author on reasonable request.

Competing interests

The authors report no conflicts of interest in this work.

Funding

This research received no external funding.

Financial disclosure: There are no financial conflicts of interest to disclose. Drs. Florin Achim, Adrian Constantin, Ahmed Mossen, Cristian Rosianu, Silviu Constantinoiu, Dragos Predescu have no financial interest in this article.

Authors' contributions

Conceptualization: F.A.; Investigation: F.A., A.C., A.M. C.R., S.C., D.P.; Writing—original draft preparation: F.A.. Writing—review and editing: F.A., A.C., A.M., C.R., D.P.; Supervision: S.C., D.P.

Acknowledgements

The authors sincerely appreciate all participants involved in implementation of minimally invasive esophagectomy in Center of Excellence in Esophageal Surgery, Clinical Hospital “Sf. Maria” Bucharest.

All authors gave final approval of the version to be published, and agree to be accountable for all aspects of the work. All authors read and approved the final manuscript.

Author details

General and Esophageal Surgery Clinic, Center of Excellence in Esophageal Surgery, Sf. Maria Clinical Hospital, 37-39 Ion Mihalache street, Bucharest, Romania

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No competing interests reported.

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Early experience in minimally invasive esophagectomy for treatment of thoracic esophageal cancer

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Abstract

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1. Introduction

2. Materials And Methods

3. Surgical Technique

4. Results

4.1. Patients

4.2. Operative results

4.3. Perioperative Outcomes

4.4. Long-term outcomes

4.5. Pathological results

4.6. Survival

5. Discussions

6. Conclusions

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