Minimally Invasive Esophagectomy

ORIGINAL ARTICLES

Minimally Invasive Esophagectomy
Lessons 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 minimally
invasive esophagectomy (MIE) procedures for the treatment of
T he enthusiasm for minimally invasive surgery, which
began with the first laparoscopic cholecystectomy, has
since expanded to many other areas of abdominal and tho-
benign and malignant esophageal disease. racic surgery. The speed by which adoption of a new mini-
Summary Background Data: Although minimally invasive surgi- mally invasive operation evolves is often a reflection of the
cal approaches to esophagectomy have been reported since 1992, degree of technical difficulty of the procedure and the fre-
MIE is still considered investigational at most institutions. quency of the operation. For example, within only a few years
Methods: This prospective study evaluates 104 MIE procedures of the first clinical report of laparoscopic cholecystectomy,
performed between August 1998 and September 2007. Main out- the number of laparoscopic cholecystectomies performed in
come measures include operative techniques, operative times, blood the United State exceeded that of open cholecystectomies. In
loss, length of stay, conversion rates, morbidities, and mortalities. contrast, it took more than 5 years from the first report of
Results: Indications for surgery were esophageal cancer (n 80), laparoscopic Roux-en-Y gastric bypass for the treatment of
Barrett esophagus with high-grade dysplasia (n 6), recalcitrant morbid obesity before widespread dissemination of this com-
stricture (n 8), gastrointestinal stromal tumor (n 3), and gastric plex operation occurred. It was not until 2004 that the number
cardia cancer (n 7). Surgical approaches included thoracoscopic/ of laparoscopic gastric bypass operations exceeded that of
laparoscopic esophagectomy with a cervical anastomosis (n 47), open gastric bypass.1,2 Open esophageal resection for benign
minimally invasive Ivor Lewis esophagectomy (n 51), laparo- or malignant disease is another complex gastrointestinal op-
scopic hand-assisted blunt transhiatal esophagectomy (n 5), and eration, and minimally invasive surgical approaches have
laparoscopic proximal gastrectomy (n 1). There were 77 males. been reported since 1992.3 However, to date, there has been
The mean age was 65 years. Three patients (2.9%) required conver- only 1 large study reporting outcomes of minimally invasive
sion to a laparotomy. The median ICU and hospital stays were 2 and esophagectomy (MIE).4 Although every imaginable tech-
8 days, respectively. Major complications occurred in 12.5% of
nique for MIE has been described in the literature, it is
difficult to determine the best minimally invasive approach
patients and minor complications in 15.4% of patients. The inci-
for esophageal resection due to the limited experience with
dence of leak was 9.6% and of anastomotic stricture was 26%. The
this complex operation at most centers. We have been per-
30-day mortality was 1.9% with an in-hospital mortality of 2.9%.
forming MIEs since 1998 and previously reported on an
The mean number of lymph nodes retrieved was 13.8. initial experience of thoracoscopic and laparoscopic esopha-
Conclusions: Minimally invasive esophagectomy is feasible with a gectomy performed on 46 consecutive patients with a mean
low conversion rate, acceptable morbidity, and low mortality. Our follow-up of 26 months.5 Since that report, our surgical
preferred operative approach is the laparoscopicthoracoscopic techniques have evolved, and we have made several impor-
Ivor Lewis resection, which provides a tension-free intrathoracic tant technical and philosophical improvements. The current
anastomosis. report describes lessons learned in performing MIE on 104
(Ann Surg 2008;248: 1081–1091)
consecutive patients over a 9-year period.

PATIENTS AND METHODS
Patients
From the Departments of *Surgery and †Medicine, University of California, Between August 1998 and September 2007, 104 con-
Irvine Medical Center, Orange, California.
Dr. Nguyen received an educational grant from Covidien. secutive patients underwent MIE at the Universities of Cali-
Presented at the American College of Surgeons 93rd Annual Clinical fornia, Irvine and Davis Medical Centers. There were no open
Congress, New Orleans, LA, October 9, 2007. esophagectomy performed during this time period. The first
Reprints: Ninh T. Nguyen, MD, Department of Surgery, 333 City Blvd. 43 cases were performed at the University of California,
West, Suite 850, Orange, CA 92868. E-mail: ninhn@uci.edu.
Copyright © 2008 by Lippincott Williams & Wilkins Davis Medical Center and all subsequent cases were per-
ISSN: 0003-4932/08/24806-1081 formed at the University of California, Irvine Medical Center.
DOI: 10.1097/SLA.0b013e31818b72b5 All operations were performed by a single surgeon. The

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

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

following data were prospectively collected on a computer- curvature of the stomach was mobilized, preserving the right
ized data form: demographics, tumor characteristics, indica- gastroepiploic vessels. If not divided at the time of laparo-
tions for surgery, type of resection, performance of a pylo- scopic staging, the left gastric vessels were then isolated and
roplasty, operative times, estimated blood loss, transfusion divided with a linear stapler. Lymph nodes along the celiac
requirements, length of intensive care unit (ICU) stay, length axis were resected to remain en bloc with the surgical
of hospital stay, histopathologic analysis of the surgical specimen. Laparoscopic pyloroplasty was performed with
specimen, postoperative complications, and mortality. Post- interrupted sutures in the first 31 patients. A pyloroplasty was
operative complications occurring within the first 30 days not performed in the latter cases as we changed our technique
after surgery were categorized as either major or minor. Late to construction of a tubular gastric conduit. A gastric conduit
complications were defined as any occurring after 30 days. was constructed by dividing the stomach, starting on the
This retrospective review was approved by our Institutional lesser curvature and finishing at the angle of His. The tip of
Review Board. the gastric conduit was then temporarily sutured to the esoph-
ageal specimen.
Preoperative Evaluation In the third stage, a horizontal neck incision was per-
Preoperative workup for patients with esophageal or formed in the left neck, 1 fingerbreadth above the supraster-
gastric cardia cancer included upper endoscopy with biopsy, nal notch. The cervical esophagus was mobilized to commu-
barium swallow, endoscopic ultrasound, computed tomogra- nicate with the dissection plane achieved in the right chest.
phy of the chest and abdomen, and positron emission tomog- The entire esophageal specimen with the attached gastric
raphy. Cardiopulmonary evaluation included pulmonary conduit was then delivered up through the cervical incision.
function testing and a 2-D echocardiogram. If patients were An esophagogastric anastomosis was constructed either with
considered to be surgical candidates after these evaluations, a 21-mm circular stapler or a 2-layer hand-sewn technique.
they would undergo laparoscopic staging and placement of a
jejunostomy feeding catheter approximately 7 to 10 days Laparoscopic and Thoracoscopic Ivor Lewis
before resection. At the time of laparoscopic staging, all Resection
patients underwent placement of a 10F jejunostomy catheter An entirely laparoscopic and thoracoscopic Ivor Lewis
and some patients in the latter part of this series (n 40) also resection was performed in 51 patients and consisted of 2
underwent gastric ischemic conditioning with division of the stages. In the first stage, the patient was placed in a supine
left gastric pedicle using a linear stapler.6 Since implemen- position. Five abdominal ports were used. The greater curva-
tation of gastric ischemic conditioning, preoperative laparo- ture of the stomach was mobilized by dividing the short
scopic ligation of the left gastric vessels is even performed for gastric vessels. The left gastric vessels were then divided with
patients with high-grade dysplasia and benign disease. In this a linear stapler. During construction of the gastric conduit, the
series, a minimally invasive approach to esophagectomy was green stapler load is often used for the first application along
not attempted in patients with T4 disease or morbid obesity. the lesser curvature of the stomach then blue stapler loads are
used as the stomach thins out toward the angle of His (Fig. 1).
Surgical Approach
Thoracoscopic and Laparoscopic Esophagectomy
With Cervical Anastomosis
The entirely laparoscopic and thoracoscopic esopha-
gectomy with cervical anastomosis was performed on 47
patients. Routine upper endoscopy was performed in the
operating room immediately before surgical resection to de-
termine the upper and lower extents of the cancer. The
operation was conducted in 3 stages. In the first stage, the
patient was placed in the left lateral decubitus position. Four
thoracic trocars were introduced into the right chest. Carbon
dioxide insufflation was not used during thoracoscopy. The
lung was retracted anteriorly. The mediastinal pleura overly-
ing the esophagus was divided to expose the intrathoracic
esophagus, and the azygous vein was divided with a linear
stapler. A Penrose drain was placed around the esophagus to
facilitate retraction. The esophagus was then circumferen-
tially mobilized from the esophageal hiatus up to the thoracic
inlet. Paraesophageal lymph nodes were dissected and main-
tained en bloc with the surgical specimen. A subcarinal
lymph node dissection was performed. A 28-French chest
tube was inserted at the 12-mm trocar site for postoperative
drainage.
In the second stage, the patient was rotated to a supine
position. Five abdominal ports were inserted. The greater FIGURE 1. Laparoscopic construction of a gastric conduit.

1082 © 2008 Lippincott Williams & Wilkins

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

FIGURE 2. The tip of the gastric conduit is temporarily sutured
to the surgical specimen in preparation for gastric pull-up. A
Penrose drain is positioned around the esophagus in the medi- FIGURE 3. Trocar position for thoracoscopic esophagectomy.
astinum for retrieval in the thorax.

first 45 cases, the 25-mm anvil was placed transthoracically
The tip of the gastric conduit was temporarily attached to the into the esophageal stump and secured with a purse-string
surgical specimen with interrupted sutures. The esophagus suture (Fig. 7). In the most recent several cases, the anvil was
was then circumferentially mobilized for a segment of 5 to 6 placed transorally using a pretilted anvil (Orvil; Autosuture,
cm into the mediastinum. Finally, a Penrose drain was placed Norwalk, CT) that was developed specifically for the purpose
around the distal esophagus for retrieval during the thoracic of transoral delivery. A gastrotomy is made at the tip of the
portion of the operation (Fig. 2). gastric conduit. The 25-mm circular stapler was placed trans-
In the second stage of the procedure, the patient was thoracically into the gastric conduit and construction of a
repositioned to the left lateral decubitus position. Four tho- stapled esophagogastric anastomosis ensued (Fig. 8). The
racic trocars were introduced in the right chest (Fig. 3). The 25-mm circular stapler was used for construction of the
right lung was retracted anteriorly for exposure of the medi- thoracic esophagogastric anastomosis as the thoracic esoph-
astinal esophagus. The mediastinal pleura overlying the agus seems to accommodate this larger size stapler in com-
esophagus was divided. The Penrose drain was identified and parison to the cervical esophagogastric anastomosis, which
used for retraction and mobilization of the esophagus from often can only accommodate a 21-mm circular stapler. The
the esophageal hiatus up to the level of the azygous vein (Fig. gastrotomy was then stapled closed with a linear stapler (Fig.
4). The azygous vein was isolated and divided with a linear 9). A 28-French chest tube and a Jackson Pratt drain were
stapler (Fig. 5). The esophageal specimen and the attached placed for postoperative chest drainage (Fig. 10).
gastric conduit were then pulled into the right thoracic cavity.
The esophagus was divided at the level of the azygous vein Laparoscopic Proximal Esophagogastrectomy
(Fig. 6). The specimen was placed into a protective bag and The laparoscopic proximal esophagogastrectomy was
removed through a 4-cm thoracic incision without rib resec- performed in 1 patient with a gastric cardia cancer. The
tion. The esophagogastric anastomoses were performed with patient was placed in a supine position. Pneumoperitoneum
the linear stapler, hand-sewn, or circular stapler technique was established, and 5 abdominal ports were placed. The
with the circular stapler being the preferred technique. In the greater curvature of the stomach was mobilized with preser-

© 2008 Lippincott Williams & Wilkins 1083


FIGURE 5. Thoracoscopic division of the azygous vein.

performed and the mid- and proximal-esophagus was bluntly
FIGURE 4. Thoracoscopic esophageal mobilization using the mobilized transhiatally. The esophageal specimen was re-
Penrose drain to retract the esophagus. moved through a cervical incision, and a hand-sewn cervical
esophagogastric anastomosis was constructed. Although a
total laparoscopic transhiatal esophagectomy is feasible, the
vation of the right gastroepiploic vessels. The left gastric limiting aspect of this operation is laparoscopic transhiatal
vessels were then divided. The gastric conduit was created by mobilization of the middle-third and proximal-third esopha-
dividing the stomach, starting on the lesser curvature, and gus. The hand-assisted approach was used in this series to
ending at the midaspect on the greater curvature. The distal facilitate mobilization of the mediastinal esophagus.
esophagus was circumferentially mobilized through the
esophageal hiatus. The esophagus was divided 3 to 4 cm Postoperative Care and Follow-up
above the gastroesophageal junction with a linear stapler. The Most patients were extubated in the operating room
esophagus was sutured to the left and right cruses of the before transfer to the ICU for cardiorespiratory monitoring.
diaphragm to prevent cephalad retraction. A 2-layer hand- Postoperative analgesia was provided by patient-controlled
sewn esophagogastric anastomosis was performed. A naso- analgesia. A Gastrografﬁn contrast study was performed on
gastric tube was guided into position in the gastric conduit. postoperative days 3 to 6. The chest tube and nasogastric tube
The surgical specimen was placed into a protective bag and were removed when the contrast study demonstrated an intact
removed through an enlarged trocar incision. anastomosis. The patient was discharged home with the
Jackson Pratt drain in place for removal at the ﬁrst clinic visit.
Hand-Assisted Laparoscopic Transhiatal Supplemental jejunostomy tube feeding was given for 2 to 3
Esophagectomy weeks and the tube was removed thereafter. Patients were
The hand-assisted laparoscopic transhiatal esophagec- seen for follow-up at 3-month intervals for a year and yearly
tomy was performed in 5 patients. Each patient was placed in thereafter. Computed tomography scans of the chest and
a supine position and pneumoperitoneum was established. abdomen were performed yearly after surgery for patients
The gastric conduit was constructed, and the distal esophagus with cancer. Pathologic staging was based on histologic
was circumferentially mobilized through the esophageal hia- examination of the resected specimen and categorized ac-
tus. At this point, an 8-cm subxiphoid midline incision was cording to the TNM staging system of the American Joint



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

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

Commission on Cancer. Anastomotic stricture was defined as
patient’s symptoms of dysphagia and/or postprandial vomit-
ing in combination with an endoscopy showing a narrowed
esophagogastric anastomosis, which impedes the passage of a
9.8-mm endoscope.
Statistical Analysis
Data are expressed as mean SD. Differences in blood
loss and operative time in the first 50 cases compared with
latter cases were determined using 2-sample t-tests. For
categorical 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 equal
to 0.05 was considered statistically significant.

RESULTS
Patient Demographics
Of 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 were
performed for esophageal cancer (n 78), Barrett esophagus FIGURE 8. The 25-mm circular stapler is placed transthoraci-
with high-grade dysplasia (n 8), gastric cardia cancer (n 7), cally into the gastric conduit in preparation for construction
gastrointestinal stromal tumor (n 3), and benign stricture of the esophagogastric anastomosis.



TABLE 1. Indications for Minimally Invasive
Esophagectomy
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

(n 8). Of the 78 patients with esophageal cancer, 11
patients (14%) had squamous cell carcinoma, 1 patient had
adenosquamous cancer, and 66 patients (85%) had adenocar-
cinoma. The location of esophageal cancer was predomi-
nately in the lower-third esophagus (58 patients). Fourteen
patients had middle-third esophageal cancer and 6 patients
had proximal-third esophageal cancer. Seven patients had
FIGURE 9. The tip of the gastric conduit is closed with a lin- gastric cardia cancer. Thirty-five (40%) of 87 patients with
ear stapler.
esophageal or gastric cardia cancer had preoperative chemo-
radiation therapy. Eight patients underwent esophagectomy
for benign recalcitrant stricture; 3 of these patients developed
a severe stricture from lye ingestion; and the other 5 patients
developed grade 4 strictures as a complication of gastro-
esophageal reflux. All patients with benign recalcitrant stric-
tures underwent multiple unsuccessful attempts at endoscopic
dilatation before surgical therapy. Forty (38%) of 104 pa-
tients had prior abdominal surgery, 5 patients had prior
gastric or esophageal surgery, and 1 patient had a prior
Roux-en-Y gastric bypass for the treatment of morbid
obesity.
The 4 types of MIEs performed in this series are listed
in Table 2. The preferred MIE operation changed in this
series. In the first 50 cases, 41 of the 50 operations were the
thoracoscopic and laparoscopic esophagectomy with a cervi-
cal anastomosis. After the 50th case, the approach in 46 of 54
operations was the entirely laparoscopic and thoracoscopic
Ivor Lewis esophagectomy. The first 31 patients had a pylo-
roplasty, whereas a pyloroplasty was not performed in the
latter cases. The stomach was used as the esophageal substi-

TABLE 2. Types of Minimally Invasive Esophagectomy
Procedures n 104
Laparoscopic and thoracoscopic Ivor Lewis 51
resection
Thoracoscopic and laparoscopic esophagectomy 47
with a cervical anastomosis
FIGURE 10. Final intraoperative view showing a reinforced Hand-assisted laparoscopic blunt transhiatal 5
gastric conduit staple line. A nasogastric tube is positioned esophagectomy
within the gastric conduit, and a chest tube is placed in the Laparoscopic proximal gastrectomy 1
pleural space for postoperative drainage.



tute in 102 (98%) of 104 patients. The remaining 2 patients blood transfusions during or after operation. The most com-
had colonic interposition. mon reason for perioperative transfusion was a low preoper-
ative blood count. The median length of ICU stay was 2 days
Operative Data (range, 1– 43), and the median length of hospital stay was 8
The mean overall operative time was 291 88 minutes days (range, 4 – 60). Compared with the initial 50 cases,
(range, 150 –520). The mean operative time for thoracoscopic operative experience in the latter cases was associated with a
and laparoscopic esophagectomy with a cervical anastomosis shorter operative time (242 vs. 350 minutes, respectively) and
was 333 75 minutes, and the mean operative time for lower blood loss (142 vs. 300 mL, respectively); however,
laparoscopic and thoracoscopic Ivor Lewis resection was there are no significant differences between groups with
249 72 minutes (Table 3). The mean estimated blood loss regard to length of stay, morbidity, and mortality.
was 220 224 mL (range, 50 –1000 mL). Thoracoscopy was
unsuccessful as a result of dense pulmonary adhesions in 1 Morbidity
patient and that patient underwent a laparoscopic hand-as- Major complications are shown in Table 4. Major
sisted blunt transhiatal esophagectomy. Three (2.9%) of 104 complications occurred in 13 (12.5%) of 104 patients (includ-
patients underwent conversion from laparoscopy to laparot- ing the 3 surgical deaths). Six patients had a gastrointestinal
omy; 1 patient had bleeding during division of the left gastric leak requiring reoperation; 4 patients had an anastomotic
vessels, 1 patient required a colonic interposition, and the last intrathoracic leak requiring thoracoscopic or thoracotomy
patient had bleeding at the splenic hilum requiring iatrogenic drainage; 1 patient had a leak at the body of the gastric
splenectomy. There were no conversions from thoracoscopy conduit from a nasogastric tube perforation; and the last
to thoracotomy. Thirteen (12.5%) of 104 patients required patient 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 developed
TABLE 3. Outcomes According to Type of Minimally intraabdominal hemorrhage on postoperative day 6, when
Invasive Esophagectomy (MIE) heparin was started for rate-controlled atrial fibrillation.
There was no significant difference in the leak rate between
Demographics and MIE With Cervical MIE With Thoracic patients who underwent gastric ischemic conditioning com-
Outcomes Anastomosis* Anastomosis
pared with patients who did not undergo gastric ischemic
No. operations 47 51 conditioning (5% vs. 9.4%, respectively, P .7). There was
Gender: males (%) 83 65 also no significant difference in the leak rate between patients
Age (yrs) 65 10 64 12 who had a pyloroplasty compared with patients who did not
Operative time (min) 333 75† 249 72 undergo pyloroplasty (9.7% vs. 6.8%, respectively; P 0.7).
Estimated blood loss (mL) 263 179† 146 117 Minor complications occurred in 15.4% of patients
Length of hospital stay (d) 12.1 12.2 9.7 8.1 (Table 5). Four patients with cervical leak were controlled
Length of ICU stay (d) 4.8 9.1 2.9 4.4 with neck wound drainage without the need for reoperation.
Major complications (%) 12.8 11.8 One patient with a colonic interposition developed a loculated
Patients requiring 12.8 9.8 intrathoracic abscess not communicating with the anastomo-
transfusion (%)
sis. The abscess was drained percutaneously and resolved
Anastomotic stricture (%) 23.4 27.5
with antibiotics. Late complications occurred in 32.7% of
Leaks (%) 6.4 9.8
patients. The most frequent late complication was anasto-
*Hand-assisted procedures were excluded from this group.
†
motic stricture (26.0%). There were no significant differences
P 0.05 compared to MIE Ivor Lewis, 2-sample t tests.
in the stricture rate between patients who underwent cervical

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



TABLE 5. Minor and Late Complications
showed a large saddle pulmonary embolus. Attempts at
percutaneous embolectomy were unsuccessful, and the pa-
Complications n tient ultimately expired.
Minor complications
Cervical anastomotic leak 4
Pathology and Follow-up
Hoarseness 2 The mean number of lymph nodes harvested in malig-
Pleural effusion requiring thoracentesis 2 nant cases was 13.8 8.6. There were no significant differ-
Pneumonia 2 ences in the number of lymph node retrieved between oper-
Wound infection 2 ative approaches with cervical or thoracic anastomosis. The
Urinary tract infection 1 number of harvested lymph nodes was also similar between
Intrathoracic abscess 1 malignant and benign cases (13.8 8.6 vs. 10.1 10.9,
Dislodged jejunostomy tube 1 respectively; P 0.2). Of the 96 patients with carcinoma or
Bilateral adrenal hemorrhage 1 Barrett esophagus with high-grade dysplasia, 1 patient had a
Total 16 (15.4%) positive distal surgical margin for cancer. This patient had a
Late complications large distal esophagus cancer with involvement of gastric
Anastomotic stricture 27 cardia along the lesser curvature and underwent a laparo-
Delayed gastric emptying 6 scopic and thoracoscopic Ivor Lewis resection.
Esophageal diaphragmatic herniation 1 Nine (25.7%) of 35 patients who underwent neoadju-
Jejunostomy site enterocutaneous fistula 1 vant therapy had a complete response with no viable tumor
Total 35 (33.7%) remaining in the surgical specimen. Two additional patients
had complete response in the esophageal specimen but had
metastatic residual disease present in the surrounding lymph
nodes. According to the postsurgical pathology, there were 11
esophagogastrostomy using hand-sewn versus circular stapler
patients with stage 0 disease (including patients with Barrett
technique. Twenty-five (92.6%) of 27 patients with stricture
esophagus and high-grade dysplasia or carcinoma in situ), 14
had good relief with endoscopic balloon dilatation. Two
patients with stage I, 32 patients with stage II, 31 patients
patients required endoscopic placement of a temporary cov-
ered stent. Another frequent late complication was delayed with stage III, and 5 patients with stage IV disease. At a mean
gastric emptying. One (3.2%) of 31 patients who had a follow-up of 54 months (range, 8 –114 months), the 5-year
pyloroplasty developed delayed gastric emptying, whereas 5 survival for stages 0 and I, II, III, and IV were 96%, 69%,
(6.8%) of 73 patients without a pyloroplasty developed de- 20%, and 0%, respectively, as shown in the Kaplan-Meier
layed gastric emptying symptoms. All patients with delayed survival curve (Fig. 11). At follow-up, there had been no
gastric emptying were successfully treated with endoscopic tumor recurrence at the thoracic or cervical surgical incisions.
balloon dilatation with or without Botulinum toxin injection. One patient developed an abdominal wound cancer recur-
One patient who maintained the jejunostomy tube for a rence in conjunction with distant disease.
prolonged period of time for nutritional support while obtain-
ing postoperative chemotherapy developed a jejunal-cutane- DISCUSSION
ous fistula at the jejunostomy site. In this series of 104 consecutive patients, MIE is
demonstrated to be technically feasible, safe, associated with
Mortality a low conversion rate (2.9%), short length of hospital stay
The 30-day morality rate was 1.9%, and the in-hospital (median 8 days), and acceptable morbidity and mortality
mortality rate was 2.9%. One patient who underwent a (2.9%). The most important lesson learned in this series was
thoracoscopic and laparoscopic esophagectomy with a cervi- the detail of the operative technique for this complex, mini-
cal anastomosis died on postoperative day 7 from a myocar- mally invasive operation. For esophageal and gastric cardia
dial infarction. Another patient who underwent a thoraco- cancer, the choice of a particular minimally invasive ap-
scopic and laparoscopic esophagectomy with a cervical proach to esophagectomy in this series was based on the
anastomosis developed a bowel obstruction from a Richter location of the tumor and its extension. Our primary goal was
hernia at the 12 mm, bladed trocar site requiring a small to achieve a negative macroscopic and microscopic resection
bowel resection; this patient later developed an intraabdomi- margin. For patients with distal-third esophageal cancer, we
nal leak at the small bowel anastomosis with intraabdominal initially preferred the combined thoracoscopic and laparo-
sepsis and died of multiorgan failure on postoperative day 41. scopic approach with construction of a cervical anastomosis.5
We attributed this complication to the use of bladed trocars as This technique was chosen due to the inherent advantages
we do not routinely close 12 mm, nonbladed trocar sites at the such as the ability to detect and treat an anastomotic leak in
current time. The last patient underwent laparoscopic and the postoperative period. Additionally, a chest anastomosis
thoracoscopic Ivor Lewis esophagogastrectomy developed was avoided due to the technical challenges of performing a
bilateral adrenal hemorrhage on postoperative day 5 and was thoracoscopic esophagogastrostomy. However, construction
treated conservatively with discontinuation of prophylactic of a neck anastomosis is not necessary a safer alternative.
anticoagulation. Upon discharge on postoperative day 11, this Disadvantages of a neck esophagogastrostomy include exces-
patient developed hypoxemia, respiratory insufficiency, and sive tension on the anastomosis, an ischemic tip of the gastric
hemodynamic instability. A CT angiogram of the chest conduit resulting in a higher leak rate, risk for recurrent



FIGURE 11. Kaplan-Meier survival
plot, according to stage of disease, for
93 patients treated with minimally
invasive esophagectomy for esopha-
geal or gastric cardia cancer, or Bar-
rett esophagus with high-grade dys-
plasia. Survival plot includes surgical
deaths.

laryngeal nerve injury, and development of postoperative To date, the largest published study of MIE was re-
oropharyngeal dysfunction. In 2000, we performed the ﬁrst ported by Luketich et al.4 In that study, they reported the
totally laparoscopic and thoracoscopic Ivor Lewis resection outcomes in 222 patients who underwent primarily the tho-
in a patient with gastric cardia cancer, requiring resection of racoscopic and laparoscopic esophagectomy with a cervical
the gastric cardia and fundus whereby a cervical anastomosis anastomosis. A cervical anastomosis was chosen, again, due
is not a feasible option.7 Although feasible, the thoracoscopic to the ability to detect postoperative anastomotic leak and the
construction of an intrathoracic anastomosis was technically technical challenges in performing a thoracoscopic anasto-
challenging. By 2003, our technique evolved to predomi- mosis. They reported a conversion rate of 7.2% (5.4% to
nately the laparoscopic and thoracoscopic Ivor Lewis ap- thoracotomy and 1.8% to laparotomy). The median ICU stay
proach. This technique continues to be the current preferred was 1 day, and the median hospital stay was 7 days. The leak
operation for distal esophageal and gastric cardia cancer even rate was 11.7% with a 30-day mortality of 1.4%. The in-
if construction of a cervical anastomosis is feasible. However, hospital mortality was not reported. Luketich and coworkers9
the debate between transhiatal and transthoracic esophagec- subsequently published their results on 50 patients who un-
tomy continues in the literature. Even esophagectomy for derwent a minimally invasive Ivor Lewis esophagectomy.
benign disease, we favor the laparoscopic and thoracoscopic Construction of the esophagogastric anastomosis was per-
Ivor Lewis resection with an intrathoracic anastomosis rather formed through a mini-thoracotomy in most cases with only
than a transhiatal approach with a cervical anastomosis. 15 (30%) of 50 patients having a thoracoscopic construction
Important advantages in construction of a chest anastomosis of the esophagogastric anastomosis. The leak rate in that
include the ability to resect the tip of the gastric conduit, series was 6% with an operative mortality of 6%. In the
which is the most ischemic portion, and that the anastomosis current study, all of the 51 patients who underwent laparo-
is not under excessive tension.8 The Ivor Lewis approach is scopic and thoracoscopic Ivor Lewis esophagectomy had
also less invasive as it avoids the need for exposure and construction of a thoracoscopic esophagogastric anastomosis
resection of the cervical esophagus while avoiding a thora- without the need for conversion to a thoracotomy.
cotomy. In this series, the entirely laparoscopic and thoraco- Other lessons learned with regard to the technical detail
scopic Ivor Lewis resection was associated with a shorter of the operation include the use of preoperative gastric
operative time and less blood loss compared with the thora- ischemic conditioning, omission of a pyloroplasty, technical
coscopic and laparoscopic esophagectomy with cervical anas- detail for construction of the thoracoscopic esophagogastric
tomosis. For long segment Barrett esophagus and proximal anastomosis, and suture inversion of the gastric conduit
esophageal cancer, the thoracoscopic and laparoscopic staple-lines. There is a risk of gastric stasis and gastric outlet
esophagectomy with a cervical anastomosis is the ap- obstruction after vagotomy associated with esophagectomy.10
proach of choice. Pyloroplasty is commonly performed during an open esoph-



agectomy to prevent the risk of delayed gastric emptying in transhiatal esophagectomy to avoid the chest, where thora-
the postoperative period. We performed a pyloroplasty in our coscopy with adhesiolysis is a difficult and time-consuming
initial 31 MIE cases with 1 patient (3.2%) developing delayed task. If a surgical option is proposed for a patient with T4
gastric emptying. Our technique has since evolved to con- disease, a thoracotomy is still the procedure of choice. Pre-
struct a tubular gastric conduit rather than leaving a large vious gastric surgery is not a contraindication to MIE. In this
gastric reservoir. Construction of the gastric conduit into a series, 1 patient had a prior Roux-en-Y gastric bypass for the
tube improves gastric emptying. Bemelman et al11 reported treatment of morbid obesity and another patient had a prior
that patients with a tubulized stomach without pyloroplasty laparoscopic Nissen fundoplication. Both of these patients
have the lowest incidence of delayed gastric emptying com- underwent successful laparoscopic and thoracoscopic Ivor
pared with patients with whole stomach as the conduit (3% Lewis resections without the need for conversion to open
vs. 38%, respectively). In our series of 73 cases without a surgery. In the patient with a history of Roux-en-Y gastric
pyloroplasty, there was a 6.8% rate of delayed gastric emp- bypass, the esophagus, the gastrojejunostomy, and the entire
tying. However, treatment consisting of endoscopic balloon Roux limb were resected. The gastric remnant was then used
dilatation, with or without Botulinum toxin injection, was to reestablish intestinal continuity.14 During the period of this
successful in all cases. Hence, pyloroplasty during MIE is no study, only 1 patient was advised to undergo definitive
longer routinely performed as its benefits (improves gastric chemoradiation therapy or an open esophagectomy because
emptying) does not outweigh its risks (leak at surgical site) of liver cirrhosis with portal hypertension.
and increase in operating time. We have also adopted the The outcomes of MIE in this series seem to be compa-
practice of preoperative ischemic gastric conditioning.6 This rable to those of transthoracic and transhiatal series.15–22
practice arose from the work of Akiyama et al,12 who per- Operative times in this series have improved from 350 min-
formed preoperative embolization of the left gastric and utes in the first 50 cases to 242 minutes in the latter cases,
splenic vessels and found a significant improvement in gastric which is now shorter than most reports for open esophagec-
blood flow within the conduit at the time of esophagectomy. tomy (256 –331 minutes). The improvement in operative time
Additionally, Holscher et al13 reported that laparoscopic isch- in this series is attributed to standardization of the steps of the
emic conditioning of the gastric conduit is feasible and safe operation and the surgeon’s improvement in laparoscopic and
and may contribute to the reduction of postoperative morbid- thoracoscopic skills. The rate of major complications in
ity and mortality after 83 esophagogastrectomy with gastric
this series was 12.5% with an anastomotic leak rate of
pull-up. In this study, some patients in the latter part of our
9.6%. These leak rates are comparable to the leak rates for
series underwent laparoscopic staging with interruption of the
open transthoracic and transhiatal esophagectomies (4.6%-
left gastric vessels. With regard to the technical detail of
16%).15–22 The types of major complications observed in our
construction of a thoracic anastomosis, the thoracoscopic
series are also similar to those following open esophagec-
esophagogastric anastomosis had been constructed using
tomy. Therefore, we do not believe that major complications
hand-sewn, linear stapler, and circular stapler techniques.
However, the current preferred anastomotic technique is the are necessarily related to the laparoscopic or thoracoscopic
use of a circular stapler with the anvil placed transorally to techniques. There were 2 emergent intraoperative conver-
position in the esophageal stump.8 The circular stapler is sions to laparotomy due to bleeding during division of the left
placed transthoracically between the ribs, through the tip of gastric vessels in 1 patient and the short gastric vessels in
the opened gastric conduit, for construction of an end-to-side another patient with a history of Child’s C liver cirrhosis. In
esophagogastric anastomosis. A gastrotomy is performed at this series, anastomotic strictures occurred in 26% of patients.
the tip of the gastric conduit, the most ischemic portion of the The rate of anastomotic stricture after open esophagectomy
conduit, and is then resected with a linear stapler. This has been reported to be 10% to 36%.16 –18,22 Finally, the
technique was developed from our experience with laparo- in-hospital mortality in this series was 2.9%, which is com-
scopic construction of an end-to-side gastrojejunostomy us- parable to that of open esophagectomy (2.1%-6% from large
ing the 25-mm circular stapler during laparoscopic gastric published series).22,23 A major determinant of outcome after
bypass for the treatment of morbid obesity. We routinely esophagectomy is the annual hospital’s volume. Patti et al24
oversew the circular anastomosis with several interrupted, reported that hospital performing more than 6 esophagecto-
tension, relieving sutures. Finally, although uncommon, an- mies per year have a 4.8% mortality compared with a mor-
other reason for postoperative leaks is breakdown of the tality rate of 16% in hospital performing less than 6 opera-
gastric conduit staple-lines. In this series, 1 patient developed tions per year. Although this study did not compare the
a large dehiscence of the gastric conduit staple-line. Routine outcome of minimally invasive to that of open surgery, our
suture inversion of the gastric conduit staple-line is now a group previously compared the outcomes of MIE to that of
standard practice at our institution. open transhiatal and transthoracic esophagectomy and found
There are few relative contraindications for MIE, which that patients who underwent MIE had shorter operative times,
include morbid obesity and T4 cancers. Thoracoscopy is less blood loss, fewer transfusions, and shortened intensive
technically challenging to perform in morbidly obese patients care unit and hospital courses than patients who underwent
(body mass index greater than 40). In the obese and in transthoracic or blunt transhiatal esophagectomy.25 However,
patients with a previous right thoracotomy, we favor the additional studies including a prospective, multicenter, ran-
hybrid approach using the laparoscopic hand-assisted blunt domized trial comparing the outcomes of minimally inva-



sive esophagectomy to that of open esophagectomy are 6. Nguyen NT, Longoria M, Sabio A, et al. Preoperative laparoscopic
needed. ligation of the left gastric vessels in preparation for esophagectomy. Ann
Thorac Surg. 2006;81:2318 –2320.
7. Nguyen NT, Follette DM, Lemoine PH, et al. Minimally invasive Ivor
CONCLUSION Lewis esophagectomy. Ann Thorac Surg. 2001;72:593–596.
Minimally invasive esophagectomy is safe and effec- 8. Nguyen NT, Longoria M, Chang K, et al. Thoracolaparoscopic modifi-
tive and offers a reasonable alternative to the conventional cation of the Ivor Lewis esophagogastrectomy. J Gastrointest Surg.
2006;10:450 – 454.
open esophagectomy. The low morbidity and mortality in this 9. Bizekis C, Kent MS, Luketich JD, et al. Initial experience with mini-
series compares favorably with that observed for an open mally invasive Ivor Lewis esophagectomy. Ann Thorac Surg. 2006;82:
esophagectomy. Although controversy continues as to the 402– 407.
best operative approach for open esophagectomy (transhiatal 10. Fok M, Cheng SW, Wong J. Pyloroplasty versus no drainage in gastric
vs. transthoracic), lessons learned from this large experience replacement of the esophagus. Am J Surg. 1991;162:447– 452.
11. Bemelman WA, Taat CW, Slors JF, et al. Delayed postoperative emp-
of minimally invasive esophagectomy favor the entirely lapa-
tying after esophageal resection is dependent on the size of the gastric
roscopic and thoracoscopic Ivor Lewis resection with con- substitute. J Am Coll Surg. 1995;180:461– 464.
struction of a tension-free, intrathoracic esophagogastric 12. Akiyama S, Kodera Y, Sekiguchi H, et al. Preoperative embolization
anastomosis using a circular stapler. The stomach is the pre- therapy for esophageal operation. J Surg Oncol. 1998;69:219 –223.
ferred conduit and a pyloroplasty can be safely omitted. Because 13. Holscher AH, Schneider PM, Gutschow C, et al. Laparoscopic ischemic
of the technical complexity of this challenging gastrointestinal conditioning of the stomach for esophageal replacement. Ann Surg.
2007;245:241–246.
operation, minimally invasive esophagectomy has not been 14. Nguyen NT, Tran CL, Gelfand DV, et al. Laparoscopic and thoraco-
widely adopted. Surgeons interested in learning this complex scopic Ivor Lewis esophagectomy after Roux-en-Y gastric bypass.
operation should attend a mini-fellowship with an appropriate J Gastrointest Surg. 2006;82:1910 –1913.
balance of lectures, laboratory, and clinical experience. Mini- 15. Swanson SJ, Batirel H, Bueno R, et al. Transthoracic esophagectomy
mally invasive esophagectomy should continue to be performed with radical mediastinal and abdominal lymph node dissection and
cervical esophagogastrostomy for esophageal carcinoma. Ann Thorac
at centers with a high volume of open and laparoscopic esoph- Surg. 2001;72:1918 –1925.
ageal surgery and by surgeons with experience in advanced 16. Millikan KW, Silverstein J, Hart V, et al. A 15-year review of esopha-
laparoscopic and thoracoscopic techniques. Lastly, similar to the gectomy for carcinoma of the esophagus and cardia. Arch Surg. 1995;
development of other minimally invasive surgical operations, 130:617– 624.
there certainly will be scrutiny by the surgical community, 17. Graham AJ, Finley RJ, Clifton JC, et al. Surgical management of
adenocarcinoma of the cardia. Am J Surg. 1998;175:418 – 421.
particularly during the developmental stage. The evolution of
18. Gluch L, Smith RC, Bambach CP, et al. Comparison of outcomes
minimally invasive esophagectomy will surely follow a similar following transhiatal or Ivor Lewis esophagectomy for esophageal
path and only time will ensure that the most logical and least carcinoma. World J Surg. 1999;23:271–275.
invasive approach to esophagectomy will prevail. 19. Orringer MB, Marshall B, Iannettoni MD. Transhiatal esophagectomy:
clinical experience and refinements. Ann Surg. 1999;230:392– 400.
REFERENCES 20. Anikin VA, McManus KG, Graham AN, et al. Total thoracic esopha-
1. Nguyen NT, Root J, Zainabadi K, et al. Accelerated growth of bariatric gectomy for esophageal cancer. J Am Coll Surg. 1997;185:525–529.
surgery with the introduction of minimally invasive surgery. Arch Surg. 21. Lozac’h P, Topart P, Perramant M. Ivor Lewis procedure for epidermoid
2005;140:1198 –1202. carcinoma of the esophagus. A series of 264 patients. Semin Surg Oncol.
2. Nguyen NT, Silver M, Robinson M, et al. Result of a national audit of 1997;13:238 –244.
bariatric surgery performed at academic centers: a 2004 university health 22. Karl RC, Schreiber R, Boulware D, et al. Factors affecting morbidity,
system consortium benchmarking project. Arch Surg. 2006;141:445– mortality, and survival in patients undergoing Ivor Lewis esophagogas-
449. trectomy. Ann Surg. 2000;231:635– 643.
3. Kawahara K, Maekawa T, Okabayashi K, et al. Video-assisted thoraco- 23. Hagen JA, DeMeester SR, Peters JH, et al. Curative resection for
scopic esophagectomy for esophageal cancer. Surg Endosc. 1999;13: esophageal adenocarcinoma: analysis of 100 en bloc esophagectomies.
218 –223. Ann Surg. 2001;234:520 –531.
4. Luketich JD, Alvelo-Rivera M, Buenaventura PO, et al. Minimally 24. Patti MG, Corvera CU, Glasgow RE, et al. A hospital’s annual rate of
invasive esophagectomy: outcomes in 222 patients. Ann Surg. 2003;238: esophagectomy influences the operative mortality rate. J Gastrointest
486 – 495. Surg. 1998;2:186 –192.
5. Nguyen NT, Roberts P, Follette DM, et al. Thoracoscopic and laparo- 25. Nguyen NT, Follette DM, Wolfe BM, et al. Comparison of minimally
scopic esophagectomy for benign and malignant disease: lessons learned invasive esophagectomy with transthoracic and transhiatal esophagec-
from 46 consecutive procedures. J Am Coll Surg. 2003;197:902–913. tomy. Arch Surg. 2000;135:920 –925.


Minimally Invasive Esophagectomy

Recommended

Recommended

More Related Content

What's hot

What's hot (20)

Similar to Minimally Invasive Esophagectomy

Similar to Minimally Invasive Esophagectomy (20)

Recently uploaded

Recently uploaded (20)

Minimally Invasive Esophagectomy