Initial Results of Minimally Invasive Ivor Lewis Esophagectomy After Induction Chemoradiation (50.4 Gy) for Esophageal Cancer

Thomay, Alan A. MD*; Snyder, Justin A. DO; Edmondson, Donna M. MSN, CRNP; Scott, Walter J. MD

Innovations: Technology & Techniques in Cardiothoracic & Vascular Surgery:
doi: 10.1097/IMI.0b013e31828130b7
Original Articles

Objective: Esophageal cancer patients receiving induction chemoradiation to 41 Gy randomized to minimally invasive (MIS) esophagectomy have fewer postoperative pulmonary complications compared with those who underwent open procedures. We evaluated the feasibility of MIS Ivor Lewis esophagectomy in patients treated with induction chemoradiation to 50.4 Gy.

Methods: We retrospectively analyzed clinical data from 30 consecutive patients undergoing MIS Ivor Lewis esophagectomy after induction chemoradiation to a mean dose of 50.4 Gy by a single surgeon at a tertiary institution since 2010. Data collected included patient demographics, preoperative risk factors, neoadjuvant treatment modalities, histology, staging, operative factors, and perioperative complications.

Results: The mean age of the patients was 61 ± 9.5 years, and 87% were men. The dominant histology was adenocarcinoma (90%), with most tumors (70%) located at the gastroesophageal junction. A total of 22 patients (73%) presented with dysphagia, but only 15 (50%) had associated weight loss (mean 12.2% total body mass). All patients had R0 resections; mean number of resected lymph nodes was 27.1 ± 11.4. Mean operating room time was 535 ± 120 minutes, with the last 10 operations 2 hours shorter than the preceding 20. Four patients (13.3%) had major complications. including 2 (6.7%) anastomotic leaks. There was no operative mortality.

Conclusions: Minimally invasive Ivor Lewis esophagectomy after chemoradiation to 50.4 Gy can be performed with decreased morbidity and mortality compared with historical series of open Ivor Lewis esophagectomy. Oncologic outcomes were acceptable as demonstrated by lymph node retrieval and complete resection rates. Operative time decreased significantly after 20 cases.

Author Information

From the *Department of Surgical Oncology and †Division of Thoracic Surgery, Fox Chase Cancer Center, Philadelphia, PA USA.

Accepted for publication November 26, 2012.

A.A. Thomay and J.A. Snyder contributed equally to this work.

Presented at the Annual Scientific Meeting of the International Society for Minimally Invasive Cardiothoracic Surgery, May 30 – June 2, 2012, Los Angeles, CA USA.

Disclosures: Walter J. Scott, MD, is a shareholder in Johnson & Johnson, Cincinnati, OH USA, Celgene Corp, Summit, NJ USA, and Biogen, Weston, MA USA, and has been a consultant for Covidien, Mansfield, MA USA. Alan A. Thomay, MD, Justin A. Snyder, DO, and Donna M. Edmondson, MSN, CRNP, declare no conflict of interest.

Address correspondence and reprint requests to Walter J. Scott, MD, Division of Thoracic Surgery, Fox Chase Cancer Center, 333 Cottman Avenue, C312, Philadelphia, PA 19111-2497 USA. E-mail:

Article Outline

In 2012, the American Cancer Society estimated the number of new esophageal cancers at 17,460, with the estimated number of deaths being 15,070.1 A meta-analysis by Sjoquist et al2 and a recent randomized controlled trial by the Chemoradiotherapy for Oesophageal Cancer followed by Surgery Study (CROSS) Group have demonstrated a significant survival benefit from neoadjuvant chemoradiation. Surgery is the preferred treatment for localized, resectable disease and can be safely performed after chemoradiation, with a proven survival benefit and increase in R0 resections.4,5 Esophagectomy has traditionally been performed using open three-hole (McKeown), transhiatal, or transthoracic (Ivor Lewis) approaches.

Complications after open esophageal surgery have been well documented. Thoracotomy contributes significantly to an increase in pulmonary morbidity secondary to pain and splinting.4 Beginning in the early 1990s, surgeons began pursuing minimally invasive (MIS) techniques of combined laparoscopy and thoracoscopy to reduce the high morbidity associated with surgery of the esophagus.5,6 Initially, MIS esophagectomy techniques included a cervical anastomosis, which has been associated with a higher anastomotic stricture and leak rate, as well as injury to the recurrent laryngeal nerve.7,8 This led to the development of the MIS Ivor Lewis esophagectomy.

A recent randomized trial from the Netherlands demonstrated a reduction in postoperative pulmonary complications in patients who underwent induction chemoradiation and MIS esophagectomy compared with those who underwent the same induction regimen and open esophagectomy.9 This study used the CROSS trial regimen of carboplatin (area under the curve = 2) and paclitaxel (50 mg/m2) with concurrent radiation to 41 Gy.3 In the United States, results from the RTOG 85-01 trial10 and the INT 0123 trial11 supported the combination of radiotherapy (RT) to 50.4 Gy given concurrently with 5-fluorouracil and cisplatin for the treatment of localized esophageal carcinoma.

In this report, we present our initial experience with MIS Ivor Lewis esophagectomy after induction chemoradiation for esophageal cancer. Most of the patients in this series underwent concurrent chemotherapy and RT to 50.4 Gy. We hypothesized that MIS Ivor Lewis esophagectomy would minimize morbidity while achieving standard oncologic outcomes in terms of lymph node dissection and negative margin status in these patients following an induction regimen that uses a higher dose of RT than that used in the CROSS trial.

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Study Design

The records of 30 consecutive patients undergoing MIS Ivor Lewis esophagectomy after induction therapy for esophageal cancer by a single surgeon from October 2010 to August 2012 were retrospectively reviewed. Patient data were maintained in a prospective database, which had been approved by the institutional review board at Fox Chase Cancer Center. Data collected included preoperative factors (baseline patient demographics, preoperative risk factors such as Barrett esophagus, medical comorbidities, and symptoms such as dysphagia and/or weight loss), treatment factors (type of chemotherapy, dose of RT, nutritional status, and treatment interruptions), tumor factors (histology, clinical and pathologic stage, and response to treatment), operative factors (technique, blood loss, and operative time), and perioperative complications. Comparable variables were analyzed via Student t test, with a P value < 0.05 considered significant.

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Staging and Complications

All patients received both clinical and pathologic staging according to the TNM classification of the American Joint Committee for Cancer Staging, 7th Edition.12 Preinduction clinical staging consisted of dedicated computed tomography (CT) of the chest and abdomen, whole-body positron emission tomography/CT scan, and endoscopic ultrasound. Suspicious mediastinal lymph nodes were routinely biopsied if doing so did not violate the plane of the primary tumor. Peritoneal washings were performed in those patients receiving preoperative laparoscopic jejunostomy tubes. Patients selected for this treatment algorithm were those presenting with dysphagia, weight loss, or bulky tumors when there was concern for treatment delays secondary to inadequate oral nutrition during the course of induction chemoradiation. Patients underwent restaging imaging studies (positron emission tomography/CT and/or dedicated chest and abdomen CT) and pulmonary function testing 2 to 3 weeks after completion of induction therapy. In fit patients without disease progression, resection was scheduled at 4 to 8 weeks after the conclusion of induction therapy.

Operative mortality was defined as death within the first 30 days postoperatively or during the initial hospitalization. Complications were recorded based on The Society of Thoracic Surgeons National Database initiative13 and were graded via the Clavien-Dindo classification of surgical complications.14 Any complication classified as Clavien Class III or above was recorded as major morbidity. Individual results were grouped into pulmonary, cardiovascular, gastrointestinal, and infectious types.

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Surgical Technique

With several modifications, our technique for MIS Ivor Lewis esophagectomy is similar to those previously described6 and the critical steps nearly identical to the open variant performed at our institution. Of note, unlike previously published experiences, hybrid techniques are not presented in this study. All patients underwent entirely MIS Ivor Lewis esophagectomy consisting of both laparoscopic and thoracoscopic phases. Most of the patients had undergone a diagnostic laparoscopy with jejunostomy feeding tube placement before neoadjuvant chemoradiation.

With the patient in lithotomy or the supine position, the laparoscopic phase begins with the placement of six trocars: four working ports, one camera port, and one port for liver retraction (Fig. 1A). After inspection for metastatic disease, the gastrocolic omentum is opened and short gastric vessels are divided, preserving the gastroepiploic artery and enough omentum to wrap the future esophagogastric anastomosis (Fig. 2A). Next, the gastrohepatic ligament is entered and the hiatus is dissected until the esophagus is mobilized circumferentially; a Penrose drain is then stapled around the gastroesophageal junction and placed into the mediastinum (Fig. 2B). The left gastric artery and vein are identified and divided with a vascular stapler (Fig. 2C). A lymphadenectomy of the left gastric and celiac axis nodes is performed en bloc with the specimen at this time.

The gastric conduit is then fashioned just proximal to the right gastric artery “crow’s feet” using laparoscopic linear stapler loads, keeping the conduit 4 to 5 cm in diameter at its narrowest portion. After dividing the conduit from the cardia, the tip is reattached to the future resected portion with 3 interrupted sutures to prevent torsion and aid in the gastric pull-up. At this time, 100 units of onabotulinum toxin A dissolved in 5 mL of normal saline is injected in four locations along the pylorus with a long endoscopic needle, replacing traditional pyloromyotomy (Fig. 2D). If a jejunostomy tube was not inserted before induction therapy, a needle jejunostomy catheter is placed at this time, adding no more than half an hour to the overall procedure (Fig. 2E).

For the thoracoscopic portion, the patient is placed in the left lateral decubitus position and a utility access port with a wound protector is placed in the seventh intercostal space anterolaterally, with two additional ports placed at similar levels in the seventh or eighth intercostal space (Fig. 1B). The esophageal dissection is performed in the standard fashion; periesophageal tissue and lymph nodes are taken while avoiding injury to the thoracic duct (Fig. 2F). Identification of the Penrose drain placed during the abdominal part of the procedure facilitates the initial esophageal dissection. Lymphadenectomy of thoracic nodal stations 4R, 7, 8, 9, and 10R is routinely performed. The esophagus is divided above the level of the azygous vein (Fig. 2G). The distal esophagus and proximal stomach are then pulled up into the chest along with the gastric conduit, while maintaining proper orientation. The sutures attaching the conduit to the specimen are then cut and the specimen is placed in an endoscopic retrieval bag and sent for frozen section of the proximal and distal margins.

Two techniques have been used for the remaining portion of the thoracoscopic phase. The first 20 patients in this seriesunderwent circular end-to-end anastomosis with a 28-mm end-to-end anastomotic (EEA) stapler (Covidien, Mansfield, MA USA). For the technique, a purse-string suture is placed around the open end of the esophagus and cinched down around the anvil of a 28-mm EEA circular stapler (Covidien).

The remaining patients underwent a circular end-to-end anastomosis using a transoral EEA stapling technique (OrVil; Covidien). This technique uses a nasogastric (NG) tube attached to a 25-mm anvil with the NG tube end passed transorally.15 For this anastomotic technique, the esophagus is divided with a linear stapler. The NG tube end is passed transorally into the proximal end of the esophagus and through a small opening made along the midportion of the staple line at the end of the proximal esophagus. The NG tube is advanced through the opening in the esophagus until the stem of the anvil is visible and the anvil portion of the device is positioned in the end of the proximal esophagus (Fig. 2H). The NG tube portion that was used as a guide is discarded. After a gastrostomy is made at the tip of the gastric conduit, the corresponding EEA stapler is inserted via the utility anterolateral port and into the stomach through the gastrostomy. The spike is extended through the wall of the gastric conduit at the desired location (a well-perfused area along the greater curve), inserted into the stem of the anvil, and after approximation, the stapler is fired to create the circular anastomosis (Fig. 2I). After a standard NG tube is passed from the nose across the anastomosis into the conduit, the gastrostomy is closed and excess stomach is removed via linear stapling. Omentum is then wrapped around the conduit and the anastomosis.

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Patient Demographics and Preoperative Treatment

Minimally invasive Ivor Lewis esophagectomy was performed on 30 consecutive patients after induction chemoradiation given for cancer of the lower third of the esophagus. Patient demographics and perioperative risk factors are described in Table 1. The mean patient age was 61 ± 9.5 years, with 26 (87%) of the patients being men. There were 29 (97%) whites and 1 (3.3%) African American. In total, 21 (70%) patients had a significant smoking history, whereas only 5 (17%) had an alcohol abuse history. Obesity (body mass index >30 kg/m2) was noted in four patients (13%). Further perioperative risk factors were reviewed using the Charlson comorbidity index16 (median, 3; range, 2–8) and a combined age-comorbidity index17 (median, 5; range, 2–8).

Twenty-two patients (73%) initially presented with dysphagia, but only 15 (50%) had associated weight loss (mean 12.2% total body mass). Twenty patients (67%) had a jejunal feeding tube placed without complication before their esophagectomy, with routine inspection for carcinomatosis and peritoneal washings (all of which were negative). Of these 20 patients, mean preoperative serum albumin level was 3.8 (vs 3.6, P < 0.05). No patients receiving a preoperative jejunal feeding tube required interruptions or delays in neoadjuvant therapy. It is our protocol to place jejunostomy feeding tubes in these patients as opposed to performing esophageal dilation or stenting.

The gastroesophageal junction (70%) was the most common tumor location, with lower thoracic tumors comprising the rest. Adenocarcinoma (90%) was the most common histological diagnosis. Two (7%) patients had squamous cell carcinoma and one (3%) had a gastrointestinal stromal tumor. Seventeen (57%) patients were clinical stage III or above (Table 2).

Neoadjuvant treatment was given to all 30 patients, with 26 (87%) getting chemoradiation and 4 (13.3%) receiving chemotherapy alone; 85% of patients received their treatment at our institution. Administered chemotherapy was most often platinum-doublet based, with cisplatin and 5-fluorouracil (40%) the most common regimen. Of the 26 patients receiving neoadjuvant radiation, the most common dose was 50.4 Gy (range, 45–57.6 Gy). The mean and median interval to operation after completion of neoadjuvant treatment was 7.2 ± 1.2 and 7.6 weeks, respectively.

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Operative Data

All anastomoses were performed with an end-to-end circular stapler. The first 20 (66.7%) were performed using a 28-mm EEA circular stapler with a hand-sewn purse string. The last 10 (33.3%) used the transoral EEA technique and a 25-mm stapler. Mean operating room (OR) time was 535 ± 120 minutes, with the first 20 procedures (569 ± 114 minutes) taking significantly longer than the final 10 (469 ± 96 minutes; P = 0.025). Mean intraoperative estimated blood loss was 278 mL, with only one (3.3%) patient requiring transfusion. The mean number of lymph nodes dissected was 27.1 ± 11.4. Pathological analysis confirmed that an R0 resection (negative proximal, distal, and circumferential margins) was achieved on all 30 (100%) patients.

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Postoperative Outcomes and Complications

Thirty-day morbidity and mortality are summarized in Table 3. Seventeen (56.7%) patients had postoperative complications, with only 4 (13.3%) having a major complication according to the Clavien-Dindo classification of surgical complications.14 Median hospital length of stay after MIS Ivor Lewis esophagectomy was 10 days (mean, 10.7 ± 4 days; range, 8–30 days). There were four readmissions within the 30-day period, two for emesis without evidence of gastric outlet obstruction or delayed gastric emptying, one for wound infection, and one for treatment of deep venous thrombosis. No perioperative mortality was seen in this series.

Three (10%) patients were taken back to the OR postoperatively. One patient had a pericardial effusion requiring a pericardial window, whereas the other two (6.7%) were treated for anastomotic leaks. Both anastomotic leaks occurred in the first four patients of the series, requiring a limited posterior thoracotomy with primary repair covered by an intercostal muscle flap. Each of these patients subsequently recovered uneventfully and was able to be advanced to a regular diet.

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Histopathologic Staging and Outcomes

Histopathologic analysis of the resected specimens revealed a complete pathologic response in 10 (33%) patients. Only 4 (13.3%) remained a pathologic stage III or greater in contrast to the 17 (56.7%) who were clinical stage III or greater preoperatively. Three patients (10%) had pN2 disease, and four (13.3%) had pN1 disease. Refer to Table 4 for a summary of pathologic staging.

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This report describes a series of 30 consecutive MIS Ivor Lewis esophagectomies performed for esophageal cancer after the administration of neoadjuvant chemoradiation to 50.4 Gy. Although these therapies have been shown to downstage esophageal tumors, they also increase operative technical difficulty via radiation-induced adhesions and scar.18

The initial series of two-stage esophagectomy was first reported in 1946 by the Welsh surgeon Ivor Lewis19 and has since become the standard resection for esophageal cancer in many centers. The advantages of this operation include thoracic exposure for mediastinal lymphadenectomy and ability to resect larger portions of the gastric cardia to ensure adequate margins as the conduit need not reach the neck. However, others argue that undue morbidity arises from an open thoracotomy and the intrathoracic anastomosis. Indeed, when comparing Ivor Lewis esophagectomy with transhiatal approaches, patients receiving an open thoracotomy had a higher incidence of postoperative pulmonary complications.20 With the widespread success of MIS techniques in other aspects of abdominal and thoracic surgery, it was only a matter of time until these principles were applied to esophagectomy.

Laparoscopic gastric mobilization with an intrathoracic anastomosis was first described in animal models during the early 1990s.21,22 Thoracoscopic stapled anastomoses were described around the same time.23 However, the combination was not successfully used in patients until 1999.24 Since then, additional studies have demonstrated the safety and efficacy of MIS esophagectomy, thus increasing its use.6,8,25–29 A recent meta-analysis of 16 studies containing 1212 patients demonstrated equivalent oncologic outcomes of MIS to open esophagectomy as to the extent of lymph node clearance, number of lymph nodes retrieved, staging, and mortality.30

In this series, mean OR time was at the higher end of the range of five recently published series.27 However, several points are worth noting. First, the OR time in this series includes flexible esophagoscopy, midpoint patient positioning with double lumen endotracheal tube placement, as well as toilet bronchoscopy at the end of the procedure, which is routinely performed for these cases at our institution. Second, a complete thoracoscopic mediastinal lymph node dissection was performed in every patient. In previously reported cohorts, fewer than 50% of patients received induction chemoradiation, which could account for the shorter overall operative time in those reports compared with our series.

The optimal management of the pylorus during esophagectomy remains controversial. Traditional procedures include pyloromyotomy and pyloroplasty, both of which may cause early edema and long-term bile reflux into the gastric conduit. Given these concerns, our standard practice for management of the pylorus includes the administration of 100 units of onabotulinum toxin A. A recent retrospective analysis of 221 patients demonstrated that this method reduced delayed gastric emptying by 30% over other procedures,31 reducing overall and respiratory morbidity. In addition, that study reported that patients injected with botulinum toxin had shorter operative times by at least 30 minutes and reduced overall hospital stay.

In our series, total operative time was reduced by almost 2 full hours after the first 20 procedures. This may be related to a learning curve and also to adoption of the transoral EEA anastomotic technique. However, in our experience, total operative time varies as a function of the degree of scarring from RT, tumor size, and location, all of which increase the overall complexity of the case.

Length of hospital stay and overall complication rates in our patients were comparable with previously reported series (Table 5).18 Our results add to growing evidence demonstrating the safety of MIS esophagectomy after neoadjuvant chemoradiation up to a mean dose of 50.4 Gy. Several retrospective analyses have shown improved early outcomes of MIS procedures when compared with open cohorts at the same institution.32–34 Patients in these series undergoing MIS esophagectomy had shorter intensive care unit length of stay, shorter overall hospital length of stay, and decreased perioperative mortality without sacrificing lymph node clearance. A recently published prospective randomized trial comparing open with MIS esophagectomy from the Netherlands confirmed the finding of decreased pulmonary complications in patients undergoing MIS esophagectomy.9

These data reflect our initial experience with completely MIS techniques; however, this study does have limitations. This was a retrospective analysis of a prospectively maintained database and is prone to selection bias, which we sought to overcome by presenting 30 consecutive cases. We do not have the data on the other esophageal cancer patients treated with different modalities for comparison. Finally, because the technique is relatively new, long-term oncologic outcomes are lacking.

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This series of 30 consecutive patients shows that MIS Ivor Lewis esophagectomy after neoadjuvant chemoradiation to 50.4 Gy is safe and effective. In addition, these data demonstrate that operative time and complication rates improve after a short learning curve of 20 cases. The procedure is associated with decreased mortality and comparable morbidity with open esophageal operations from historical controls, along with desirable immediate oncologic outcomes demonstrated by completeness of resection and adequate lymphadenectomy.

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Minimally invasive esophagectomy (MIE) is a solution to a potentially debilitating procedure, the esophagectomy. Compared with the transhiatal procedure, another version of a minimally invasive procedure, the MIE allows greater visibility and a potentially wider and more oncologic approach. For locally advanced esophageal cancer, does the combination of chemoradiotherapy and minimally invasive resection achieve oncologic goals with acceptable short-term outcomes?

In this article, the authors attempt to answer that question. The Fox Chase group presents one of the very few series in which all of the patients underwent induction therapy, nearly 90% underwent chemoradiotherapy with radiation dose of 50.4 Gy. Unlike many previous reports, where there were a mixture of different anastomotic locations (intrathoracic vs cervical) and a mixture of patients (those who had undergone no preoperative therapy vs those who underwent chemotherapy, radiation, or the combination of the chemoradiotherapy), all of these patients underwent an Ivor Lewis approach after induction therapy, thus providing us with a better assessment of the impact of induction therapy on MIE outcomes. To achieve a sufficiently negative proximal margin, the Ivor Lewis approach was selected for patients with a GE junction or lower third esophageal cancer. The mean operative time was approximately 10 hours, having achieved an R0 resection and an average of 27 resected lymph nodes in all patients, with only one patient requiring transfusion with no mortality; operative times were significantly improved with greater experience. As with other MIE series, the greatest impact was on the significant reduction in pulmonary complications, resulting in an 11-day mean length of stay and a 13% 30-day readmission rate. In this group of patients and in the hands of the Fox Chase surgeons, the Ivor Lewis MIE postinduction therapy appears to achieve the cancer-related outcomes necessary for optimal short- and long-term outcomes.


Esophageal cancer; Minimally invasive surgery (MIS); Ivor Lewis esophagectomy; Neoadjuvant chemoradiation

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