minimally invasive esophagectomy

ORIGINAL ARTICLES

Minimally Invasive EsophagectomyLessons Learned From 104 Operations

Ninh T. Nguyen, MD, FACS,* Marcelo W. Hinojosa, MD,* Brian R. Smith, MD,*Kenneth J. Chang, MD,† James Gray, BS,* and David Hoyt, MD, FACS*

Objectives: To review the outcomes of 104 consecutive minimallyinvasive esophagectomy (MIE) procedures for the treatment ofbenign and malignant esophageal disease.Summary Background Data: Although minimally invasive surgi-cal approaches to esophagectomy have been reported since 1992,MIE is still considered investigational at most institutions.Methods: This prospective study evaluates 104 MIE proceduresperformed between August 1998 and September 2007. Main out-come measures include operative techniques, operative times, bloodloss, length of stay, conversion rates, morbidities, and mortalities.Results: Indications for surgery were esophageal cancer (n � 80),Barrett esophagus with high-grade dysplasia (n � 6), recalcitrantstricture (n � 8), gastrointestinal stromal tumor (n � 3), and gastriccardia cancer (n � 7). Surgical approaches included thoracoscopic/laparoscopic esophagectomy with a cervical anastomosis (n � 47),minimally invasive Ivor Lewis esophagectomy (n � 51), laparo-scopic hand-assisted blunt transhiatal esophagectomy (n � 5), andlaparoscopic proximal gastrectomy (n � 1). There were 77 males.The mean age was 65 years. Three patients (2.9%) required conver-sion to a laparotomy. The median ICU and hospital stays were 2 and8 days, respectively. Major complications occurred in 12.5% ofpatients and minor complications in 15.4% of patients. The inci-dence of leak was 9.6% and of anastomotic stricture was 26%. The30-day mortality was 1.9% with an in-hospital mortality of 2.9%.The mean number of lymph nodes retrieved was 13.8.Conclusions: Minimally invasive esophagectomy is feasible with alow conversion rate, acceptable morbidity, and low mortality. Ourpreferred operative approach is the laparoscopic\thoracoscopicIvor Lewis resection, which provides a tension-free intrathoracicanastomosis.

(Ann Surg 2008;248: 1081–1091)

The enthusiasm for minimally invasive surgery, whichbegan with the first laparoscopic cholecystectomy, has

since expanded to many other areas of abdominal and tho-racic surgery. The speed by which adoption of a new mini-mally invasive operation evolves is often a reflection of thedegree of technical difficulty of the procedure and the fre-quency of the operation. For example, within only a few yearsof the first clinical report of laparoscopic cholecystectomy,the number of laparoscopic cholecystectomies performed inthe United State exceeded that of open cholecystectomies. Incontrast, it took more than 5 years from the first report oflaparoscopic Roux-en-Y gastric bypass for the treatment ofmorbid obesity before widespread dissemination of this com-plex operation occurred. It was not until 2004 that the numberof laparoscopic gastric bypass operations exceeded that ofopen gastric bypass.1,2 Open esophageal resection for benignor malignant disease is another complex gastrointestinal op-eration, and minimally invasive surgical approaches havebeen reported since 1992.3 However, to date, there has beenonly 1 large study reporting outcomes of minimally invasiveesophagectomy (MIE).4 Although every imaginable tech-nique for MIE has been described in the literature, it isdifficult to determine the best minimally invasive approachfor esophageal resection due to the limited experience withthis complex operation at most centers. We have been per-forming MIEs since 1998 and previously reported on aninitial experience of thoracoscopic and laparoscopic esopha-gectomy performed on 46 consecutive patients with a meanfollow-up of 26 months.5 Since that report, our surgicaltechniques have evolved, and we have made several impor-tant technical and philosophical improvements. The currentreport describes lessons learned in performing MIE on 104consecutive patients over a 9-year period.

PATIENTS AND METHODS

PatientsBetween August 1998 and September 2007, 104 con-

secutive patients underwent MIE at the Universities of Cali-fornia, Irvine and Davis Medical Centers. There were no openesophagectomy performed during this time period. The first43 cases were performed at the University of California,Davis Medical Center and all subsequent cases were per-formed at the University of California, Irvine Medical Center.All operations were performed by a single surgeon. The

From the Departments of *Surgery and †Medicine, University of California,Irvine Medical Center, Orange, California.

Dr. Nguyen received an educational grant from Covidien.Presented at the American College of Surgeons 93rd Annual Clinical

Congress, New Orleans, LA, October 9, 2007.Reprints: Ninh T. Nguyen, MD, Department of Surgery, 333 City Blvd.

West, Suite 850, Orange, CA 92868. E-mail: [email protected] © 2008 by Lippincott Williams & WilkinsISSN: 0003-4932/08/24806-1081DOI: 10.1097/SLA.0b013e31818b72b5

Annals of Surgery • Volume 248, Number 6, December 2008 1081

following data were prospectively collected on a computer-ized data form: demographics, tumor characteristics, indica-tions for surgery, type of resection, performance of a pylo-roplasty, operative times, estimated blood loss, transfusionrequirements, length of intensive care unit (ICU) stay, lengthof hospital stay, histopathologic analysis of the surgicalspecimen, postoperative complications, and mortality. Post-operative complications occurring within the first 30 daysafter surgery were categorized as either major or minor. Latecomplications were defined as any occurring after 30 days.This retrospective review was approved by our InstitutionalReview Board.

Preoperative EvaluationPreoperative workup for patients with esophageal or

gastric cardia cancer included upper endoscopy with biopsy,barium swallow, endoscopic ultrasound, computed tomogra-phy of the chest and abdomen, and positron emission tomog-raphy. Cardiopulmonary evaluation included pulmonaryfunction testing and a 2-D echocardiogram. If patients wereconsidered to be surgical candidates after these evaluations,they would undergo laparoscopic staging and placement of ajejunostomy feeding catheter approximately 7 to 10 daysbefore resection. At the time of laparoscopic staging, allpatients underwent placement of a 10F jejunostomy catheterand some patients in the latter part of this series (n � 40) alsounderwent gastric ischemic conditioning with division of theleft gastric pedicle using a linear stapler.6 Since implemen-tation of gastric ischemic conditioning, preoperative laparo-scopic ligation of the left gastric vessels is even performed forpatients with high-grade dysplasia and benign disease. In thisseries, a minimally invasive approach to esophagectomy wasnot attempted in patients with T4 disease or morbid obesity.

Surgical ApproachThoracoscopic and Laparoscopic EsophagectomyWith Cervical Anastomosis

The entirely laparoscopic and thoracoscopic esopha-gectomy with cervical anastomosis was performed on 47patients. Routine upper endoscopy was performed in theoperating room immediately before surgical resection to de-termine the upper and lower extents of the cancer. Theoperation was conducted in 3 stages. In the first stage, thepatient was placed in the left lateral decubitus position. Fourthoracic trocars were introduced into the right chest. Carbondioxide insufflation was not used during thoracoscopy. Thelung was retracted anteriorly. The mediastinal pleura overly-ing the esophagus was divided to expose the intrathoracicesophagus, and the azygous vein was divided with a linearstapler. A Penrose drain was placed around the esophagus tofacilitate retraction. The esophagus was then circumferen-tially mobilized from the esophageal hiatus up to the thoracicinlet. Paraesophageal lymph nodes were dissected and main-tained en bloc with the surgical specimen. A subcarinallymph node dissection was performed. A 28-French chesttube was inserted at the 12-mm trocar site for postoperativedrainage.

In the second stage, the patient was rotated to a supineposition. Five abdominal ports were inserted. The greater

curvature of the stomach was mobilized, preserving the rightgastroepiploic vessels. If not divided at the time of laparo-scopic staging, the left gastric vessels were then isolated anddivided with a linear stapler. Lymph nodes along the celiacaxis were resected to remain en bloc with the surgicalspecimen. Laparoscopic pyloroplasty was performed withinterrupted sutures in the first 31 patients. A pyloroplasty wasnot performed in the latter cases as we changed our techniqueto construction of a tubular gastric conduit. A gastric conduitwas constructed by dividing the stomach, starting on thelesser curvature and finishing at the angle of His. The tip ofthe gastric conduit was then temporarily sutured to the esoph-ageal specimen.

In the third stage, a horizontal neck incision was per-formed in the left neck, 1 fingerbreadth above the supraster-nal notch. The cervical esophagus was mobilized to commu-nicate with the dissection plane achieved in the right chest.The entire esophageal specimen with the attached gastricconduit was then delivered up through the cervical incision.An esophagogastric anastomosis was constructed either witha 21-mm circular stapler or a 2-layer hand-sewn technique.

Laparoscopic and Thoracoscopic Ivor LewisResection

An entirely laparoscopic and thoracoscopic Ivor Lewisresection was performed in 51 patients and consisted of 2stages. In the first stage, the patient was placed in a supineposition. Five abdominal ports were used. The greater curva-ture of the stomach was mobilized by dividing the shortgastric vessels. The left gastric vessels were then divided witha linear stapler. During construction of the gastric conduit, thegreen stapler load is often used for the first application alongthe lesser curvature of the stomach then blue stapler loads areused as the stomach thins out toward the angle of His (Fig. 1).

FIGURE 1. Laparoscopic construction of a gastric conduit.

Nguyen et al Annals of Surgery • Volume 248, Number 6, December 2008

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The tip of the gastric conduit was temporarily attached to thesurgical specimen with interrupted sutures. The esophaguswas then circumferentially mobilized for a segment of 5 to 6cm into the mediastinum. Finally, a Penrose drain was placedaround the distal esophagus for retrieval during the thoracicportion of the operation (Fig. 2).

In the second stage of the procedure, the patient wasrepositioned to the left lateral decubitus position. Four tho-racic trocars were introduced in the right chest (Fig. 3). Theright lung was retracted anteriorly for exposure of the medi-astinal esophagus. The mediastinal pleura overlying theesophagus was divided. The Penrose drain was identified andused for retraction and mobilization of the esophagus fromthe esophageal hiatus up to the level of the azygous vein (Fig.4). The azygous vein was isolated and divided with a linearstapler (Fig. 5). The esophageal specimen and the attachedgastric conduit were then pulled into the right thoracic cavity.The esophagus was divided at the level of the azygous vein(Fig. 6). The specimen was placed into a protective bag andremoved through a 4-cm thoracic incision without rib resec-tion. The esophagogastric anastomoses were performed withthe linear stapler, hand-sewn, or circular stapler techniquewith the circular stapler being the preferred technique. In the

first 45 cases, the 25-mm anvil was placed transthoracicallyinto the esophageal stump and secured with a purse-stringsuture (Fig. 7). In the most recent several cases, the anvil wasplaced transorally using a pretilted anvil (Orvil; Autosuture,Norwalk, CT) that was developed specifically for the purposeof transoral delivery. A gastrotomy is made at the tip of thegastric conduit. The 25-mm circular stapler was placed trans-thoracically into the gastric conduit and construction of astapled esophagogastric anastomosis ensued (Fig. 8). The25-mm circular stapler was used for construction of thethoracic esophagogastric anastomosis as the thoracic esoph-agus seems to accommodate this larger size stapler in com-parison to the cervical esophagogastric anastomosis, whichoften can only accommodate a 21-mm circular stapler. Thegastrotomy was then stapled closed with a linear stapler (Fig.9). A 28-French chest tube and a Jackson Pratt drain wereplaced for postoperative chest drainage (Fig. 10).

Laparoscopic Proximal EsophagogastrectomyThe laparoscopic proximal esophagogastrectomy was

performed in 1 patient with a gastric cardia cancer. Thepatient was placed in a supine position. Pneumoperitoneumwas established, and 5 abdominal ports were placed. Thegreater curvature of the stomach was mobilized with preser-

FIGURE 2. The tip of the gastric conduit is temporarily suturedto the surgical specimen in preparation for gastric pull-up. APenrose drain is positioned around the esophagus in the medi-astinum for retrieval in the thorax.

FIGURE 3. Trocar position for thoracoscopic esophagectomy.

Annals of Surgery • Volume 248, Number 6, December 2008 Minimally Invasive Esophagectomy

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vation of the right gastroepiploic vessels. The left gastricvessels were then divided. The gastric conduit was created bydividing the stomach, starting on the lesser curvature, andending at the midaspect on the greater curvature. The distalesophagus was circumferentially mobilized through theesophageal hiatus. The esophagus was divided 3 to 4 cmabove the gastroesophageal junction with a linear stapler. Theesophagus was sutured to the left and right cruses of thediaphragm to prevent cephalad retraction. A 2-layer hand-sewn esophagogastric anastomosis was performed. A naso-gastric tube was guided into position in the gastric conduit.The surgical specimen was placed into a protective bag andremoved through an enlarged trocar incision.

Hand-Assisted Laparoscopic TranshiatalEsophagectomy

The hand-assisted laparoscopic transhiatal esophagec-tomy was performed in 5 patients. Each patient was placed ina supine position and pneumoperitoneum was established.The gastric conduit was constructed, and the distal esophaguswas circumferentially mobilized through the esophageal hia-tus. At this point, an 8-cm subxiphoid midline incision was

performed and the mid- and proximal-esophagus was bluntlymobilized transhiatally. The esophageal specimen was re-moved through a cervical incision, and a hand-sewn cervicalesophagogastric anastomosis was constructed. Although atotal laparoscopic transhiatal esophagectomy is feasible, thelimiting aspect of this operation is laparoscopic transhiatalmobilization of the middle-third and proximal-third esopha-gus. The hand-assisted approach was used in this series tofacilitate mobilization of the mediastinal esophagus.

Postoperative Care and Follow-upMost patients were extubated in the operating room

before transfer to the ICU for cardiorespiratory monitoring.Postoperative analgesia was provided by patient-controlledanalgesia. A Gastrograffin contrast study was performed onpostoperative days 3 to 6. The chest tube and nasogastric tubewere removed when the contrast study demonstrated an intactanastomosis. The patient was discharged home with theJackson Pratt drain in place for removal at the first clinic visit.Supplemental jejunostomy tube feeding was given for 2 to 3weeks and the tube was removed thereafter. Patients wereseen for follow-up at 3-month intervals for a year and yearlythereafter. Computed tomography scans of the chest andabdomen were performed yearly after surgery for patientswith cancer. Pathologic staging was based on histologicexamination of the resected specimen and categorized ac-cording to the TNM staging system of the American Joint

FIGURE 4. Thoracoscopic esophageal mobilization using thePenrose drain to retract the esophagus.

FIGURE 5. Thoracoscopic division of the azygous vein.



Commission on Cancer. Anastomotic stricture was defined aspatient’s symptoms of dysphagia and/or postprandial vomit-ing in combination with an endoscopy showing a narrowedesophagogastric anastomosis, which impedes the passage of a9.8-mm endoscope.

Statistical AnalysisData are expressed as mean � SD. Differences in blood

loss and operative time in the first 50 cases compared withlatter cases were determined using 2-sample t-tests. Forcategorical data, differences were analyzed using �2 tests.Statistical analysis was performed using Statistix software,version 8 (Tallahassee, FL). A P value of less than or equalto 0.05 was considered statistically significant.

RESULTS

Patient DemographicsOf the 104 patients, there were 77 males and 27 females

with a mean age of 65 years. The indications for an esopha-gectomy are listed in Table 1. Esophageal resections wereperformed for esophageal cancer (n � 78), Barrett esophaguswith high-grade dysplasia (n � 8), gastric cardia cancer (n � 7),gastrointestinal stromal tumor (n � 3), and benign stricture

FIGURE 8. The 25-mm circular stapler is placed transthoraci-cally into the gastric conduit in preparation for constructionof the esophagogastric anastomosis.

FIGURE 6. Thoracoscopic division of the proximal esophagusat the level of the azygous vein using a linear stapler.

FIGURE 7. The anvil is placed within the esophageal stumpand a gastrotomy is performed at the tip of the gastric conduit.



(n � 8). Of the 78 patients with esophageal cancer, 11patients (14%) had squamous cell carcinoma, 1 patient hadadenosquamous cancer, and 66 patients (85%) had adenocar-cinoma. The location of esophageal cancer was predomi-nately in the lower-third esophagus (58 patients). Fourteenpatients had middle-third esophageal cancer and 6 patientshad proximal-third esophageal cancer. Seven patients hadgastric cardia cancer. Thirty-five (40%) of 87 patients withesophageal or gastric cardia cancer had preoperative chemo-radiation therapy. Eight patients underwent esophagectomyfor benign recalcitrant stricture; 3 of these patients developeda severe stricture from lye ingestion; and the other 5 patientsdeveloped grade 4 strictures as a complication of gastro-esophageal reflux. All patients with benign recalcitrant stric-tures underwent multiple unsuccessful attempts at endoscopicdilatation before surgical therapy. Forty (38%) of 104 pa-tients had prior abdominal surgery, 5 patients had priorgastric or esophageal surgery, and 1 patient had a priorRoux-en-Y gastric bypass for the treatment of morbidobesity.

The 4 types of MIEs performed in this series are listedin Table 2. The preferred MIE operation changed in thisseries. In the first 50 cases, 41 of the 50 operations were thethoracoscopic and laparoscopic esophagectomy with a cervi-cal anastomosis. After the 50th case, the approach in 46 of 54operations was the entirely laparoscopic and thoracoscopicIvor Lewis esophagectomy. The first 31 patients had a pylo-roplasty, whereas a pyloroplasty was not performed in thelatter cases. The stomach was used as the esophageal substi-

FIGURE 10. Final intraoperative view showing a reinforcedgastric conduit staple line. A nasogastric tube is positionedwithin the gastric conduit, and a chest tube is placed in thepleural space for postoperative drainage.

FIGURE 9. The tip of the gastric conduit is closed with a lin-ear stapler.

TABLE 1. Indications for Minimally InvasiveEsophagectomy

Indications for Esophagectomy n

Carcinoma or premalignant lesion

Lower-third esophagus cancer 58

Middle-third esophagus cancer 14

Upper-third esophagus cancer 6

Gastric cardia cancer 7

Barrett esophagus with high-grade dysplasia 8

Gastrointestinal stromal tumor 3

Total 96

Benign recalcitrant stricture

End-stage gastroesophageal reflux disease 5

Corrosive injury from lye ingestion 3

Total 8

TABLE 2. Types of Minimally Invasive Esophagectomy

Procedures n � 104

Laparoscopic and thoracoscopic Ivor Lewisresection

51

Thoracoscopic and laparoscopic esophagectomywith a cervical anastomosis

47

Hand-assisted laparoscopic blunt transhiatalesophagectomy

5

Laparoscopic proximal gastrectomy 1



tute in 102 (98%) of 104 patients. The remaining 2 patientshad colonic interposition.

Operative DataThe mean overall operative time was 291 � 88 minutes

(range, 150–520). The mean operative time for thoracoscopicand laparoscopic esophagectomy with a cervical anastomosiswas 333 � 75 minutes, and the mean operative time forlaparoscopic and thoracoscopic Ivor Lewis resection was249 � 72 minutes (Table 3). The mean estimated blood losswas 220 � 224 mL (range, 50–1000 mL). Thoracoscopy wasunsuccessful as a result of dense pulmonary adhesions in 1patient and that patient underwent a laparoscopic hand-as-sisted blunt transhiatal esophagectomy. Three (2.9%) of 104patients underwent conversion from laparoscopy to laparot-omy; 1 patient had bleeding during division of the left gastricvessels, 1 patient required a colonic interposition, and the lastpatient had bleeding at the splenic hilum requiring iatrogenicsplenectomy. There were no conversions from thoracoscopyto thoracotomy. Thirteen (12.5%) of 104 patients required

blood transfusions during or after operation. The most com-mon reason for perioperative transfusion was a low preoper-ative blood count. The median length of ICU stay was 2 days(range, 1–43), and the median length of hospital stay was 8days (range, 4–60). Compared with the initial 50 cases,operative experience in the latter cases was associated with ashorter operative time (242 vs. 350 minutes, respectively) andlower blood loss (142 vs. 300 mL, respectively); however,there are no significant differences between groups withregard to length of stay, morbidity, and mortality.

MorbidityMajor complications are shown in Table 4. Major

complications occurred in 13 (12.5%) of 104 patients (includ-ing the 3 surgical deaths). Six patients had a gastrointestinalleak requiring reoperation; 4 patients had an anastomoticintrathoracic leak requiring thoracoscopic or thoracotomydrainage; 1 patient had a leak at the body of the gastricconduit from a nasogastric tube perforation; and the lastpatient developed a leak at the gastric conduit staple-line.Prolonged respiratory failure occurred in 1 patient. Pulmo-nary embolism occurred in 2 patients. One patient developedintraabdominal hemorrhage on postoperative day 6, whenheparin was started for rate-controlled atrial fibrillation.There was no significant difference in the leak rate betweenpatients who underwent gastric ischemic conditioning com-pared with patients who did not undergo gastric ischemicconditioning (5% vs. 9.4%, respectively, P � .7). There wasalso no significant difference in the leak rate between patientswho had a pyloroplasty compared with patients who did notundergo pyloroplasty (9.7% vs. 6.8%, respectively; P � 0.7).

Minor complications occurred in 15.4% of patients(Table 5). Four patients with cervical leak were controlledwith neck wound drainage without the need for reoperation.One patient with a colonic interposition developed a loculatedintrathoracic abscess not communicating with the anastomo-sis. The abscess was drained percutaneously and resolvedwith antibiotics. Late complications occurred in 32.7% ofpatients. The most frequent late complication was anasto-motic stricture (26.0%). There were no significant differencesin the stricture rate between patients who underwent cervical

TABLE 3. Outcomes According to Type of MinimallyInvasive Esophagectomy (MIE)

Demographics andOutcomes

MIE With CervicalAnastomosis*

MIE With ThoracicAnastomosis

No. operations 47 51

Gender: males (%) 83 65

Age (yrs) 65 � 10 64 � 12

Operative time (min) 333 � 75† 249 � 72

Estimated blood loss (mL) 263 � 179† 146 � 117

Length of hospital stay (d) 12.1 � 12.2 9.7 � 8.1

Length of ICU stay (d) 4.8 � 9.1 2.9 � 4.4

Major complications (%) 12.8 11.8

Patients requiringtransfusion (%)

12.8 9.8

Anastomotic stricture (%) 23.4 27.5

Leaks (%) 6.4 9.8

*Hand-assisted procedures were excluded from this group.†P � 0.05 compared to MIE Ivor Lewis, 2-sample t tests.

TABLE 4. Major Complications

Patient No. Complications Cause Management Outcome

6 Pulmonary embolism Venous thrombosis Anticoagulation Resolved

9 Respiratory failure Pneumonia Mechanical ventilation Improved

13 Cervical anastomotic leak Ischemia/tension Thoracotomy drainage Improved

21 Intrathoracic anastomotic leak Ischemia Thoracotomy drainage Resolved

22 Intra-abdominal sepsis Bowel obstruction Bowel resection Expired

34 Leak at body of gastric conduit Nasogastric tube Diversion Improved

41 Myocardial infarction Myocardial ischemia Medical support Expired

44 Intra-abdominal bleeding Heparin induced Laparotomy drainage Resolved

64 Gastric conduit staple-line leak Ischemia/tension Diversion Improved

73 Respiratory insufficiency Pneumonia Respiratory support Resolved

74 Intrathoracic anastomotic leak Ischemia/tension Thoracotomy drainage Resolved

98 Intrathoracic anastomotic leak Nasogastric tube Esophageal stent Resolved

102 Pulmonary embolism Venous thrombosis Anticoagulation Expired



esophagogastrostomy using hand-sewn versus circular staplertechnique. Twenty-five (92.6%) of 27 patients with stricturehad good relief with endoscopic balloon dilatation. Twopatients required endoscopic placement of a temporary cov-ered stent. Another frequent late complication was delayedgastric emptying. One (3.2%) of 31 patients who had apyloroplasty developed delayed gastric emptying, whereas 5(6.8%) of 73 patients without a pyloroplasty developed de-layed gastric emptying symptoms. All patients with delayedgastric emptying were successfully treated with endoscopicballoon dilatation with or without Botulinum toxin injection.One patient who maintained the jejunostomy tube for aprolonged period of time for nutritional support while obtain-ing postoperative chemotherapy developed a jejunal-cutane-ous fistula at the jejunostomy site.

MortalityThe 30-day morality rate was 1.9%, and the in-hospital

mortality rate was 2.9%. One patient who underwent athoracoscopic and laparoscopic esophagectomy with a cervi-cal anastomosis died on postoperative day 7 from a myocar-dial infarction. Another patient who underwent a thoraco-scopic and laparoscopic esophagectomy with a cervicalanastomosis developed a bowel obstruction from a Richterhernia at the 12 mm, bladed trocar site requiring a smallbowel resection; this patient later developed an intraabdomi-nal leak at the small bowel anastomosis with intraabdominalsepsis and died of multiorgan failure on postoperative day 41.We attributed this complication to the use of bladed trocars aswe do not routinely close 12 mm, nonbladed trocar sites at thecurrent time. The last patient underwent laparoscopic andthoracoscopic Ivor Lewis esophagogastrectomy developedbilateral adrenal hemorrhage on postoperative day 5 and wastreated conservatively with discontinuation of prophylacticanticoagulation. Upon discharge on postoperative day 11, thispatient developed hypoxemia, respiratory insufficiency, andhemodynamic instability. A CT angiogram of the chest

showed a large saddle pulmonary embolus. Attempts atpercutaneous embolectomy were unsuccessful, and the pa-tient ultimately expired.

Pathology and Follow-upThe mean number of lymph nodes harvested in malig-

nant cases was 13.8 � 8.6. There were no significant differ-ences in the number of lymph node retrieved between oper-ative approaches with cervical or thoracic anastomosis. Thenumber of harvested lymph nodes was also similar betweenmalignant and benign cases (13.8 � 8.6 vs. 10.1 � 10.9,respectively; P � 0.2). Of the 96 patients with carcinoma orBarrett esophagus with high-grade dysplasia, 1 patient had apositive distal surgical margin for cancer. This patient had alarge distal esophagus cancer with involvement of gastriccardia along the lesser curvature and underwent a laparo-scopic and thoracoscopic Ivor Lewis resection.

Nine (25.7%) of 35 patients who underwent neoadju-vant therapy had a complete response with no viable tumorremaining in the surgical specimen. Two additional patientshad complete response in the esophageal specimen but hadmetastatic residual disease present in the surrounding lymphnodes. According to the postsurgical pathology, there were 11patients with stage 0 disease (including patients with Barrettesophagus and high-grade dysplasia or carcinoma in situ), 14patients with stage I, 32 patients with stage II, 31 patientswith stage III, and 5 patients with stage IV disease. At a meanfollow-up of 54 months (range, 8–114 months), the 5-yearsurvival for stages 0 and I, II, III, and IV were 96%, 69%,20%, and 0%, respectively, as shown in the Kaplan-Meiersurvival curve (Fig. 11). At follow-up, there had been notumor recurrence at the thoracic or cervical surgical incisions.One patient developed an abdominal wound cancer recur-rence in conjunction with distant disease.

DISCUSSIONIn this series of 104 consecutive patients, MIE is

demonstrated to be technically feasible, safe, associated witha low conversion rate (2.9%), short length of hospital stay(median 8 days), and acceptable morbidity and mortality(2.9%). The most important lesson learned in this series wasthe detail of the operative technique for this complex, mini-mally invasive operation. For esophageal and gastric cardiacancer, the choice of a particular minimally invasive ap-proach to esophagectomy in this series was based on thelocation of the tumor and its extension. Our primary goal wasto achieve a negative macroscopic and microscopic resectionmargin. For patients with distal-third esophageal cancer, weinitially preferred the combined thoracoscopic and laparo-scopic approach with construction of a cervical anastomosis.5

This technique was chosen due to the inherent advantagessuch as the ability to detect and treat an anastomotic leak inthe postoperative period. Additionally, a chest anastomosiswas avoided due to the technical challenges of performing athoracoscopic esophagogastrostomy. However, constructionof a neck anastomosis is not necessary a safer alternative.Disadvantages of a neck esophagogastrostomy include exces-sive tension on the anastomosis, an ischemic tip of the gastricconduit resulting in a higher leak rate, risk for recurrent

TABLE 5. Minor and Late Complications

Complications n

Minor complications

Cervical anastomotic leak 4

Hoarseness 2

Pleural effusion requiring thoracentesis 2

Pneumonia 2

Wound infection 2

Urinary tract infection 1

Intrathoracic abscess 1

Dislodged jejunostomy tube 1

Bilateral adrenal hemorrhage 1

Total 16 (15.4%)

Late complications

Anastomotic stricture 27

Delayed gastric emptying 6

Esophageal diaphragmatic herniation 1

Jejunostomy site enterocutaneous fistula 1

Total 35 (33.7%)



laryngeal nerve injury, and development of postoperativeoropharyngeal dysfunction. In 2000, we performed the firsttotally laparoscopic and thoracoscopic Ivor Lewis resectionin a patient with gastric cardia cancer, requiring resection ofthe gastric cardia and fundus whereby a cervical anastomosisis not a feasible option.7 Although feasible, the thoracoscopicconstruction of an intrathoracic anastomosis was technicallychallenging. By 2003, our technique evolved to predomi-nately the laparoscopic and thoracoscopic Ivor Lewis ap-proach. This technique continues to be the current preferredoperation for distal esophageal and gastric cardia cancer evenif construction of a cervical anastomosis is feasible. However,the debate between transhiatal and transthoracic esophagec-tomy continues in the literature. Even esophagectomy forbenign disease, we favor the laparoscopic and thoracoscopicIvor Lewis resection with an intrathoracic anastomosis ratherthan a transhiatal approach with a cervical anastomosis.Important advantages in construction of a chest anastomosisinclude the ability to resect the tip of the gastric conduit,which is the most ischemic portion, and that the anastomosisis not under excessive tension.8 The Ivor Lewis approach isalso less invasive as it avoids the need for exposure andresection of the cervical esophagus while avoiding a thora-cotomy. In this series, the entirely laparoscopic and thoraco-scopic Ivor Lewis resection was associated with a shorteroperative time and less blood loss compared with the thora-coscopic and laparoscopic esophagectomy with cervical anas-tomosis. For long segment Barrett esophagus and proximalesophageal cancer, the thoracoscopic and laparoscopicesophagectomy with a cervical anastomosis is the ap-proach of choice.

To date, the largest published study of MIE was re-ported by Luketich et al.4 In that study, they reported theoutcomes in 222 patients who underwent primarily the tho-racoscopic and laparoscopic esophagectomy with a cervicalanastomosis. A cervical anastomosis was chosen, again, dueto the ability to detect postoperative anastomotic leak and thetechnical challenges in performing a thoracoscopic anasto-mosis. They reported a conversion rate of 7.2% (5.4% tothoracotomy and 1.8% to laparotomy). The median ICU staywas 1 day, and the median hospital stay was 7 days. The leakrate was 11.7% with a 30-day mortality of 1.4%. The in-hospital mortality was not reported. Luketich and coworkers9

subsequently published their results on 50 patients who un-derwent a minimally invasive Ivor Lewis esophagectomy.Construction of the esophagogastric anastomosis was per-formed through a mini-thoracotomy in most cases with only15 (30%) of 50 patients having a thoracoscopic constructionof the esophagogastric anastomosis. The leak rate in thatseries was 6% with an operative mortality of 6%. In thecurrent study, all of the 51 patients who underwent laparo-scopic and thoracoscopic Ivor Lewis esophagectomy hadconstruction of a thoracoscopic esophagogastric anastomosiswithout the need for conversion to a thoracotomy.

Other lessons learned with regard to the technical detailof the operation include the use of preoperative gastricischemic conditioning, omission of a pyloroplasty, technicaldetail for construction of the thoracoscopic esophagogastricanastomosis, and suture inversion of the gastric conduitstaple-lines. There is a risk of gastric stasis and gastric outletobstruction after vagotomy associated with esophagectomy.10

Pyloroplasty is commonly performed during an open esoph-

FIGURE 11. Kaplan-Meier survivalplot, according to stage of disease, for93 patients treated with minimallyinvasive esophagectomy for esopha-geal or gastric cardia cancer, or Bar-rett esophagus with high-grade dys-plasia. Survival plot includes surgicaldeaths.



agectomy to prevent the risk of delayed gastric emptying inthe postoperative period. We performed a pyloroplasty in ourinitial 31 MIE cases with 1 patient (3.2%) developing delayedgastric emptying. Our technique has since evolved to con-struct a tubular gastric conduit rather than leaving a largegastric reservoir. Construction of the gastric conduit into atube improves gastric emptying. Bemelman et al11 reportedthat patients with a tubulized stomach without pyloroplastyhave the lowest incidence of delayed gastric emptying com-pared with patients with whole stomach as the conduit (3%vs. 38%, respectively). In our series of 73 cases without apyloroplasty, there was a 6.8% rate of delayed gastric emp-tying. However, treatment consisting of endoscopic balloondilatation, with or without Botulinum toxin injection, wassuccessful in all cases. Hence, pyloroplasty during MIE is nolonger routinely performed as its benefits (improves gastricemptying) does not outweigh its risks (leak at surgical site)and increase in operating time. We have also adopted thepractice of preoperative ischemic gastric conditioning.6 Thispractice arose from the work of Akiyama et al,12 who per-formed preoperative embolization of the left gastric andsplenic vessels and found a significant improvement in gastricblood flow within the conduit at the time of esophagectomy.Additionally, Holscher et al13 reported that laparoscopic isch-emic conditioning of the gastric conduit is feasible and safeand may contribute to the reduction of postoperative morbid-ity and mortality after 83 esophagogastrectomy with gastricpull-up. In this study, some patients in the latter part of ourseries underwent laparoscopic staging with interruption of theleft gastric vessels. With regard to the technical detail ofconstruction of a thoracic anastomosis, the thoracoscopicesophagogastric anastomosis had been constructed usinghand-sewn, linear stapler, and circular stapler techniques.However, the current preferred anastomotic technique is theuse of a circular stapler with the anvil placed transorally toposition in the esophageal stump.8 The circular stapler isplaced transthoracically between the ribs, through the tip ofthe opened gastric conduit, for construction of an end-to-sideesophagogastric anastomosis. A gastrotomy is performed atthe tip of the gastric conduit, the most ischemic portion of theconduit, and is then resected with a linear stapler. Thistechnique was developed from our experience with laparo-scopic construction of an end-to-side gastrojejunostomy us-ing the 25-mm circular stapler during laparoscopic gastricbypass for the treatment of morbid obesity. We routinelyoversew the circular anastomosis with several interrupted,tension, relieving sutures. Finally, although uncommon, an-other reason for postoperative leaks is breakdown of thegastric conduit staple-lines. In this series, 1 patient developeda large dehiscence of the gastric conduit staple-line. Routinesuture inversion of the gastric conduit staple-line is now astandard practice at our institution.

There are few relative contraindications for MIE, whichinclude morbid obesity and T4 cancers. Thoracoscopy istechnically challenging to perform in morbidly obese patients(body mass index greater than 40). In the obese and inpatients with a previous right thoracotomy, we favor thehybrid approach using the laparoscopic hand-assisted blunt

transhiatal esophagectomy to avoid the chest, where thora-coscopy with adhesiolysis is a difficult and time-consumingtask. If a surgical option is proposed for a patient with T4disease, a thoracotomy is still the procedure of choice. Pre-vious gastric surgery is not a contraindication to MIE. In thisseries, 1 patient had a prior Roux-en-Y gastric bypass for thetreatment of morbid obesity and another patient had a priorlaparoscopic Nissen fundoplication. Both of these patientsunderwent successful laparoscopic and thoracoscopic IvorLewis resections without the need for conversion to opensurgery. In the patient with a history of Roux-en-Y gastricbypass, the esophagus, the gastrojejunostomy, and the entireRoux limb were resected. The gastric remnant was then usedto reestablish intestinal continuity.14 During the period of thisstudy, only 1 patient was advised to undergo definitivechemoradiation therapy or an open esophagectomy becauseof liver cirrhosis with portal hypertension.

The outcomes of MIE in this series seem to be compa-rable to those of transthoracic and transhiatal series.15–22

Operative times in this series have improved from 350 min-utes in the first 50 cases to 242 minutes in the latter cases,which is now shorter than most reports for open esophagec-tomy (256–331 minutes). The improvement in operative timein this series is attributed to standardization of the steps of theoperation and the surgeon’s improvement in laparoscopic andthoracoscopic skills. The rate of major complications inthis series was 12.5% with an anastomotic leak rate of9.6%. These leak rates are comparable to the leak rates foropen transthoracic and transhiatal esophagectomies (4.6%-16%).15–22 The types of major complications observed in ourseries are also similar to those following open esophagec-tomy. Therefore, we do not believe that major complicationsare necessarily related to the laparoscopic or thoracoscopictechniques. There were 2 emergent intraoperative conver-sions to laparotomy due to bleeding during division of the leftgastric vessels in 1 patient and the short gastric vessels inanother patient with a history of Child’s C liver cirrhosis. Inthis series, anastomotic strictures occurred in 26% of patients.The rate of anastomotic stricture after open esophagectomyhas been reported to be 10% to 36%.16–18,22 Finally, thein-hospital mortality in this series was 2.9%, which is com-parable to that of open esophagectomy (2.1%-6% from largepublished series).22,23 A major determinant of outcome afteresophagectomy is the annual hospital’s volume. Patti et al24

reported that hospital performing more than 6 esophagecto-mies per year have a 4.8% mortality compared with a mor-tality rate of 16% in hospital performing less than 6 opera-tions per year. Although this study did not compare theoutcome of minimally invasive to that of open surgery, ourgroup previously compared the outcomes of MIE to that ofopen transhiatal and transthoracic esophagectomy and foundthat patients who underwent MIE had shorter operative times,less blood loss, fewer transfusions, and shortened intensivecare unit and hospital courses than patients who underwenttransthoracic or blunt transhiatal esophagectomy.25 However,additional studies including a prospective, multicenter, ran-domized trial comparing the outcomes of minimally inva-



sive esophagectomy to that of open esophagectomy areneeded.

CONCLUSIONMinimally invasive esophagectomy is safe and effec-

tive and offers a reasonable alternative to the conventionalopen esophagectomy. The low morbidity and mortality in thisseries compares favorably with that observed for an openesophagectomy. Although controversy continues as to thebest operative approach for open esophagectomy (transhiatalvs. transthoracic), lessons learned from this large experienceof minimally invasive esophagectomy favor the entirely lapa-roscopic and thoracoscopic Ivor Lewis resection with con-struction of a tension-free, intrathoracic esophagogastricanastomosis using a circular stapler. The stomach is the pre-ferred conduit and a pyloroplasty can be safely omitted. Becauseof the technical complexity of this challenging gastrointestinaloperation, minimally invasive esophagectomy has not beenwidely adopted. Surgeons interested in learning this complexoperation should attend a mini-fellowship with an appropriatebalance of lectures, laboratory, and clinical experience. Mini-mally invasive esophagectomy should continue to be performedat centers with a high volume of open and laparoscopic esoph-ageal surgery and by surgeons with experience in advancedlaparoscopic and thoracoscopic techniques. Lastly, similar to thedevelopment of other minimally invasive surgical operations,there certainly will be scrutiny by the surgical community,particularly during the developmental stage. The evolution ofminimally invasive esophagectomy will surely follow a similarpath and only time will ensure that the most logical and leastinvasive approach to esophagectomy will prevail.

REFERENCES1. Nguyen NT, Root J, Zainabadi K, et al. Accelerated growth of bariatric

surgery with the introduction of minimally invasive surgery. Arch Surg.2005;140:1198–1202.

2. Nguyen NT, Silver M, Robinson M, et al. Result of a national audit ofbariatric surgery performed at academic centers: a 2004 university healthsystem consortium benchmarking project. Arch Surg. 2006;141:445–449.

3. Kawahara K, Maekawa T, Okabayashi K, et al. Video-assisted thoraco-scopic esophagectomy for esophageal cancer. Surg Endosc. 1999;13:218–223.

4. Luketich JD, Alvelo-Rivera M, Buenaventura PO, et al. Minimallyinvasive esophagectomy: outcomes in 222 patients. Ann Surg. 2003;238:486–495.

5. Nguyen NT, Roberts P, Follette DM, et al. Thoracoscopic and laparo-scopic esophagectomy for benign and malignant disease: lessons learnedfrom 46 consecutive procedures. J Am Coll Surg. 2003;197:902–913.

6. Nguyen NT, Longoria M, Sabio A, et al. Preoperative laparoscopicligation of the left gastric vessels in preparation for esophagectomy. AnnThorac Surg. 2006;81:2318–2320.

7. Nguyen NT, Follette DM, Lemoine PH, et al. Minimally invasive IvorLewis esophagectomy. Ann Thorac Surg. 2001;72:593–596.

8. Nguyen NT, Longoria M, Chang K, et al. Thoracolaparoscopic modifi-cation of the Ivor Lewis esophagogastrectomy. J Gastrointest Surg.2006;10:450–454.

9. Bizekis C, Kent MS, Luketich JD, et al. Initial experience with mini-mally invasive Ivor Lewis esophagectomy. Ann Thorac Surg. 2006;82:402–407.

10. Fok M, Cheng SW, Wong J. Pyloroplasty versus no drainage in gastricreplacement of the esophagus. Am J Surg. 1991;162:447–452.

11. Bemelman WA, Taat CW, Slors JF, et al. Delayed postoperative emp-tying after esophageal resection is dependent on the size of the gastricsubstitute. J Am Coll Surg. 1995;180:461–464.

12. Akiyama S, Kodera Y, Sekiguchi H, et al. Preoperative embolizationtherapy for esophageal operation. J Surg Oncol. 1998;69:219–223.

13. Holscher AH, Schneider PM, Gutschow C, et al. Laparoscopic ischemicconditioning of the stomach for esophageal replacement. Ann Surg.2007;245:241–246.

14. Nguyen NT, Tran CL, Gelfand DV, et al. Laparoscopic and thoraco-scopic Ivor Lewis esophagectomy after Roux-en-Y gastric bypass.J Gastrointest Surg. 2006;82:1910–1913.

15. Swanson SJ, Batirel H, Bueno R, et al. Transthoracic esophagectomywith radical mediastinal and abdominal lymph node dissection andcervical esophagogastrostomy for esophageal carcinoma. Ann ThoracSurg. 2001;72:1918–1925.

16. Millikan KW, Silverstein J, Hart V, et al. A 15-year review of esopha-gectomy for carcinoma of the esophagus and cardia. Arch Surg. 1995;130:617–624.

17. Graham AJ, Finley RJ, Clifton JC, et al. Surgical management ofadenocarcinoma of the cardia. Am J Surg. 1998;175:418–421.

18. Gluch L, Smith RC, Bambach CP, et al. Comparison of outcomesfollowing transhiatal or Ivor Lewis esophagectomy for esophagealcarcinoma. World J Surg. 1999;23:271–275.

19. Orringer MB, Marshall B, Iannettoni MD. Transhiatal esophagectomy:clinical experience and refinements. Ann Surg. 1999;230:392–400.

20. Anikin VA, McManus KG, Graham AN, et al. Total thoracic esopha-gectomy for esophageal cancer. J Am Coll Surg. 1997;185:525–529.

21. Lozac’h P, Topart P, Perramant M. Ivor Lewis procedure for epidermoidcarcinoma of the esophagus. A series of 264 patients. Semin Surg Oncol.1997;13:238–244.

22. Karl RC, Schreiber R, Boulware D, et al. Factors affecting morbidity,mortality, and survival in patients undergoing Ivor Lewis esophagogas-trectomy. Ann Surg. 2000;231:635–643.

23. Hagen JA, DeMeester SR, Peters JH, et al. Curative resection foresophageal adenocarcinoma: analysis of 100 en bloc esophagectomies.Ann Surg. 2001;234:520–531.

24. Patti MG, Corvera CU, Glasgow RE, et al. A hospital’s annual rate ofesophagectomy influences the operative mortality rate. J GastrointestSurg. 1998;2:186–192.

25. Nguyen NT, Follette DM, Wolfe BM, et al. Comparison of minimallyinvasive esophagectomy with transthoracic and transhiatal esophagec-tomy. Arch Surg. 2000;135:920–925.



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