Hindawi Publishing Corporation
Gastroenterology Research and Practice
Volume 2012, Article ID 683213, 7 pages
Reviewof Minimally Invasive Esophagectomy and
T. Kim, S.N.Hochwald, G.A.Sarosi,A.M.Caban,G.Rossidis, andK.Ben-David
Department of Surgery, College of Medicine, University of Florida, P.O. Box 100109, Gainesville, FL 32610-0109, USA
Correspondence should be addressed to K. Ben-David, email@example.com
Received 19 March 2012; Revised 1 June 2012; Accepted 8 June 2012
Academic Editor: Yong Song Guan
Copyright © 2012 T. Kim et al. This is an open access article distributed under the Creative Commons Attribution License, which
permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Esophagectomy is a complex operation with significant morbidity and mortality. Minimally invasive esophagectomy (MIE) was
described in the 1990s in an effort to reduce operative morbidity. Since then many institutions have adopted and described their
series with this technique. This paper reviews the literature on the variety of MIE techniques, clinical and quality of life outcomes
with open versus MIE, and controversies surrounding MIE—such as prone positioning, stapling techniques, size of the gastric
conduit, and robotic techniques.
Esophagectomy for benign or malignant disease is a complex
operation with significant morbidity and mortality. The five-
year survival rate has been shown to be 19% to 46.5%,
stage esophageal cancer [1–3]. Despite these survival rates,
Orringer and his colleagues set the benchmark for postop-
erative outcomes with their reported series of 1,085 patients
who underwent open transhiatal esophagectomy from 1976
to 1998 with a hospital mortality and morbidity rate of 4%
and 13%, respectively . More recently, they published
an updated series of 2,007 patients who had an associated
hospital mortality rate of 1%, anastomotic leak rate of
9%, pneumonia rate of 2%, and intrathoracic hemorrhage,
laceration rates of <1% each .
In an effort to reduce the morbidity of esophagectomy,
minimally invasive methods began to be increasingly applied
in the 1990s. In 1998, Luketich et al. reported their initial
experience on 8 patients who underwent minimally invasive
esophagectomy (MIE) using either laparoscopic and/or tho-
and one cervical anastomotic leak, thus demonstrating
the potential safety and feasibility of minimally invasive
esophagectomy . Since then, many institutions have
reported their experiences in the adoption and refinement
of MIE for benign and malignant diseases of the esopha-
gus. Hence, this paper summarizes the literature to date,
including both larger single institution series on MIE and
also retrospective and prospective comparisons of open
versus MIE, and addresses the various lessons learned and
controversies surrounding MIE.
2.VariousTechniques of Esophagectomy
The two most commonly employed open techniques of
esophagectomy are transhiatal esophagectomy (THE) and
Ivor Lewis esophagectomy (ILE). First described in 1936,
THE involves laparotomy with blunt dissection of the
esophagus and cervical esophagogastric anastomosis .
ILE involves combined laparotomy with right thoracotomy
resection via left thoracotomy or left thoracoabdominal
approach or three-incision McKeown-type esophagectomy
[1, 2, 4, 9, 10]. In a previous report by Pennathur et
al. in 2010, the various open techniques were described
along with a few comparative studies on open versus MIE
[11, 12]. For the purpose of this paper, open techniques
of esophagectomy include any of the above procedures via
completely open approach (without any laparoscopic or
2Gastroenterology Research and Practice
thoracoscopic component): THE, ILE, esophagectomy via
left thoracotomy or left thoracoabdominal approach; MIE
techniques include both total laparoscopic/thoracoscopic
THE or ILE and also hybrid procedures with at least one
of the approaches being done via either laparoscopy or
thoracoscopy. Summarized in a review by Herbella, the
various techniques of MIE include any combination of
laparoscopy instead of laparotomy, thoracoscopy instead of
thoracotomy, and either cervical (THE) or intrathoracic
(ILE) anastomosis .
As with many new novel procedures, the initial pub-
lications involving minimally invasive esophagectomy were
mostly institutional series. Outcomes from these institu-
tional series included anastomotic leak rates of 4% to 11.7%,
pneumonia rates of 7.7% to 16.7%, major morbidity rates of
12.5% to 23%, and operative mortality rates of 0.9% to 6%
Luketich, one of the earlier pioneers of MIE, reported
his extensive experience from 1996 to 2002 on 222 patients
whounderwentMIEforeitherhigh-gradedysplasia(n = 47)
or invasive cancer (n
completed in 206 (92.8%) patients. Operative mortality was
1.4%. Morbidity included anastomotic leak rate of 11.7%,
pneumonia incidence of 7.7%, and recurrent laryngeal nerve
and most commonly employed approach is combined right
thoracoscopic and laparoscopic THE. If significant gastric
extension of the tumor is encountered, they prefer to resect
more stomach and perform an intrathoracic anastomosis,
that is minimally invasive ILE. The same group later
described their early experience with minimally invasive ILE
in 50 patients from 2002 to 2005 with an operative mortality
and leak rate of 6% each .
Rajan et al. also published a large series of 463 patients
in India who underwent minimally invasive esophagectomy
from 1997 to 2009. Interestingly, 71 percent of patients had
squamous cell carcinoma, and 29% had adenocarcinoma of
the esophagus. Operative mortality was 0.9%, and overall
morbidity was 16% . Similarly, Nguyen and colleagues
reported a series of 104 MIE procedures performed between
1998 and 2007. Most procedures were minimally invasive
THE or ILE (98 of 104) utilizing a circular staple technique.
Major complication rate was 12.5%, and minor com-
plication rate was 15.4%. Anastomotic leak rate was 9.6%,
and operative mortality was 2.9% . Consequently,
we reported our results in 105 consecutive patients who
underwent MIE utilizing a side-to-side 6cm linear stapled
technique from August 2007 to January 2011. Our mortality
was 1% (1/105), and morbidity included 7% transient
left recurrent laryngeal nerve injury, 9% pneumonia, 1%
wound infection, and 4% anastomotic leak rate . In
a separate study, we studied the effect of neoadjuvant
chemoradiation on outcomes after MIE and noted that
there were no significant differences in operative blood loss,
median operative time, total or individual complication
rates, pneumonia, atrial fibrillation, recurrent laryngeal
nerve injury, or anastomotic leaks between patients who
received neoadjuvant chemoradiation and patients who did
not . Finally, due to the proximity of our Veterans
175). MIE was successfully
Administration Hospital to the University Hospital, we were
able to demonstrate the feasibility of an MIE program at
the Veterans Hospital in our initial series of 18 consecutive
MIE. There was one (5.6%) 30-day mortality, 1 (5.6%)
anastomotic leak, and 3 (16.7%) postoperative pneumonias
In 2007, Gemmill and McCulloch published one of the
earlier systematic reviews of minimally invasive operations
for esophageal and gastric cancer based on an electronic
reviewed, 23 articles were found on minimally invasive
= 1398)—the operations spanning
any combination of thoracoscopy or thoracotomy with
laparoscopy, hand-assisted laparoscopy, or laparotomy (i.e.,
MIE or hybrid MIE). Twenty-one of the 23 were case studies,
and the remaining 2 were case-matched studies; there were
no randomized controlled studies of open versus MIE at
the time of this systematic review. For MIE or hybrid MIE,
30-day mortality was 2.3%, combined major and minor
morbidity was 46.2%, anastomotic leak rate was 7.7%, and
respiratory tract infection rate was 13.2%. The authors
stated that while there appears to be substantial literature
suggesting the feasibility and safety of minimally invasive
surgery for esophageal cancer, the quality of the studies
was poor . Flaws included (1) the predominance of
case series—low levels of evidence, (2) lack of valid direct
comparisons of open versus MIE, (3) heterogeneity of the
studies with regard to the type of MIE or hybrid MIE and,
thus, lack of generalizability, (4) selection bias—patients
selected for minimally invasive surgery are unlikely to have
been representative of the general population of esophageal
cancer patients (i.e., earlier stage, smaller tumors, and/or
less co-morbid), and (5) publication bias—surgeons with
unsatisfactory results may have been less inclined to publish
their data. Hence, the authors suggested a prospective
nonrandomized cooperative study by surgeons interested
in first establishing a consensus on both the appropriate
question and the appropriate procedure to be tested against
open esophagectomy. The study would allow for evaluation
of learning curves, power calculations based on observed
treatment effect, and development of quality measures; the
study would thus serves as an important and less costly
preliminary step before a randomized controlled trial.
Verhage et al. published their results of a systematic
review consisting of 10 case-control studies comparing
open to MIE. Blood loss for MIE (compared to open
esophagectomy) was uniformly lower in all studies, whereas
hospital and ICU length of stay, total complication rate,
and pulmonary complications were significantly lower with
MIE in most studies . This paper was limited by the
heterogeneity of the studies with regards to technique of
by Nagpal et al., consisting of 12 studies comparing open
esophagectomy(n = 612)andMIEorhybridMIE(n = 672),
concluded similar findings as noted by Verhage’s group.
There were no significant differences in 30-day mortality or
anastomotic leak rates. Blood loss, ICU length of stay, overall
hospital stay, and total morbidity were significantly lower in
the MIE group .
Gastroenterology Research and Practice3
Table 1: MIE outcomes in institutional series, case-control studies, and systematic reviews.
Type LeakPneumonia RLN injury Morbidity
Luketich et al. 
Bizekis et al. 
Rajan et al. 
Nguyen et al. 
Ben-David et al. 
Ben-David et al. 
Systematic reviews or meta-analyses
Gemmill and McCulloch 
Verhage et al. 
(10 case-control studies)
Nagpal et al. 
(12 case-control studies)
Dantoc et al. 
(17 case-control studies)
Total complications lower
Trends favoring MIE, but
Sgourakis et al. 
1008 Open versus MIE
Biere et al. 
1061 Open versus MIE
(1 randomized controlled trial and 9 case-control studies)
Mamidanna et al. 
MIE: minimally invasive esophagectomy.
RLN: recurrent laryngeal nerve.
A more recent systematic review by Dantoc et al.
comparing open to MIE consisted of 17 case-control studies,
and the review showed no significant differences in 30-day
survival or 5-year survival rates. Median number of lymph
nodes retrieved was significantly higher with MIE versus
open esophagectomy (16 versus 10) attributed to better
visualization with MIE . Furthermore, in a meta-analysis
by Sgourakis et al., 8 out of 71 screened trials comparing
open versus MIE or hybrid MIE were included in the final
study (n = 1,008). It was found that total complications
interval or CI 1.08–3.43 for open versus MIE). It should
be noted, however, that this comparison was performed
with only 3 studies. Anastomotic stricture rates were lower
with open esophagectomy (OR 0.11, 95% CI 0.04–0.31), but
this comparison was performed with only 2 studies .
Additionally, Biere et al. published their findings of a meta-
analysis in which 1 controlled clinical trial and 9 case-control
studies were included in the final study (n = 1,061). Trends
were observed in favor of MIE for the following outcomes:
major morbidity, pulmonary complications, anastomotic
leakage, mortality, length of stay, operating time, and
blood loss, but statistical significance was not reached .
The obvious limitation of these meta-analyses is that they
consist of primarily nonrandomized and retrospective case-
control studies. Ultimately, it was concluded in all three
meta-analyses that prospective randomized controlled trials
comparing open versus MIE were needed.
Lastly, a large United Kingdom population-based study
by Mamidanna et al. analyzed the Hospital Episode Statistics
data from April 2005 to March 2010 and included 7,502
esophagectomies, 1,155 (15.4%) of which were MIE—
with marked increase in the proportion of MIE (24.7%)
open and MIE groups, respectively, in 30-day mortality
(4.3% versus 4.0%) and overall morbidity (38.0% versus
39.2%). Reintervention rate was higher with MIE compared
to open (21% versus 17.6%, P = 0.006) . Despite the
seeming equipoise in outcomes between open and MIE in
the above study, there were significant limitations of this
as commented in editorials by Rice and Blackstone  and
Pennathur and Luketich .
Based on these large studies on MIE, total complication
rates range from 38% to 46.2% and operative mortality rates
range from 1.3% to 4.3% (Table 1). The numerous studies
comparing open versus MIE (case-control studies and
meta-analyses or systematic reviews) suggest that oncologic
outcome and survival are not significantly different, whereas
overall morbidity might be similar or possibly improved
with MIE. However, the ultimate message is that better
data is necessary to claim the benefits of MIE over open
4 Gastroenterology Research and Practice
esophagectomy. Consequently, Biere et al. published the
study protocol on the “TIME” trial or traditional invasive
versus minimally invasive esophagectomy, which will be the
first prospective, multicenter, randomized study comparing
open versus MIE . In this study proposal, patients
will be randomized to either traditional open Ivor Lewis
esophagectomy or MIE. For the MIE group, THE is the
preferred method while the Ivor Lewis esophagectomy (i.e.,
an intrathoracic anastomosis) will be performed if more of a
gastric resection margin is necessary based on location of the
3.1. Prone Positioning. Some surgeons have reported on
thoracoscopic mobilization of the esophagus in prone posi-
tion as a potentially more ergonomic approach with less
pulmonary morbidity. Palanivelu et al. published a series
of 130 patients who underwent MIE with thoracoscopic
esophageal mobilization in prone position using a right
prone posterior approach, thus allowing for left lung ven-
tilation with possible intermittent ventilation of the right
lung. Mean operative time was 220 minutes (range 160
to 450 minutes). Median ICU stay was 1 day (range 1 to
32 days). Postoperative pneumonia rate was only 1.54%
. From a respiratory standpoint, the authors advocate
prone positioning by arguing for reduction in venous shunt
and possibly prevention of postoperative atelectasis, due to
allowing of partial intermittent right lung ventilation, as
opposed to single (left) lung ventilation. Functional residual
capacity and ventilation-perfusion matching are better in
prone, compared to supine, position.
Noshiro et al. published their experience with prone
positioning during MIE and aggressive mediastinal lym-
phadenectomy. Compared with left lateral decubitus posi-
tioning, prone positioning was associated with lower blood
loss and better exposure of the operative field around the
left recurrent laryngeal nerve (i.e., identification of the left
subclavian artery to allow for dissection around the left
recurrent laryngeal nerve). Recurrent laryngeal nerve injury
rates were not significantly different between prone and left
lateral decubitus-positioned patients. No local recurrences
were observed along the left recurrent laryngeal nerve at a
median of 22-month followup after surgery .
comparison of prone versus left lateral decubitus position
during thoracoscopic esophageal mobilization that operative
123min, P < 0.01) . Complication rate, number of
lymph nodes procured, length of stay, and intraoperative
blood loss were not significantly different between prone and
left lateral positions.
Jarral et al. addressed the controversy of prone versus left
lateral decubitus position during the thoracoscopic phase of
three-stage minimally invasive esophagectomy in a review of
31 papers, 7 of which represented the best evidence available.
The authors’ conclusions were that the studies are small
in size, have significant limitations, and do not uniformly
demonstrate superiority in outcomes with either technique
3.2. Gastric Conduit. Luketich et al. reported an increase in
gastric tip necrosis and anastomotic leaks when a narrower
gastric tube (3-4cm in diameter) was employed; thus, they
emphasized the importance of creating a gastric tube of 5-
6cm in diameter . In an editorial on MIE, Wee and
Morse also recommend creating a gastric tube of 5cm in
diameter . Additionally, a case series of 77 patients who
underwent intended MIE by Berrisford et al. reported a
higher than expected gastric tube ischemia rate of 13% using
an ideal gastric tube diameter of 4cm .
Based on anecdotal reports of gastric ischemic con-
ditioning and low anastomotic leak rates, Nguyen et al.
performed a retrospective comparative study of 81 patients
who underwent MIE after laparoscopic gastric ischemic
“conditioning” via division of the left gastric artery during
staging laparoscopy versus 71 patients who underwent
esophagectomy without “conditioning.” There were no sig-
nificant differences in anastomotic leak rate (11% for condi-
tioning versus 8.5% without conditioning) or stricture rate
(30% versus 25%) . In the LOGIC trial, a randomized
controlled trial of laparoscopic gastric ischemic conditioning
prior to MIE, perfusion of the gastric conduit tip—as
measured by laser Doppler fluximetry—was not improved
by conditioning, although the number of study patients was
only 16 .
3.3. Esophagogastric Anastomosis. Regarding the technique
of esophagogastric anastomosis, Luketich et al. described,
as others have, employing a 25mm EEA stapler via a small
gastrotomy . A modification to this was described by
Campos et al. in which a circular stapled anastomosis is
performed using a transoral anvil. Their study included
37 patients who underwent minimally invasive ILE using
this new stapled technique; anastomotic leak rate was 2.7%,
and stricture rate was 13.5%, all of which were treated
successfully with endoscopic dilations . We previously
have described our technique of completely thoracoscopic
side-to-side stapled 6cm anastomosis during minimally
invasive ILE by placing the anvil portion of the stapler
through the esophagostomy (which is guided by a large
bore nasogastric tube or Bougie dilator) and the cartridge
through the gastrotomy. In this small study, there were no
postoperative strictures .
Maas et al. performed a review of 12 studies describing
various intrathoracic anastomotic techniques during min-
imally invasive ILE, including descriptions of handsewn
techniques and mostly stapled techniques. The stapled
techniques were either transthoracic or transoral, and the
transthoracic stapled techniques varied with regard to (1)
left lateral decubitus versus prone positioning; (2) circular
versus linear stapled; (3) end-to-side versus side-to-side; (4)
or linear staple gun and Z-stitch for securing the anvil on
the proximal esophageal side. Anastomotic leak rates ranged
Gastroenterology Research and Practice5
from 0 to 10%, and anastomotic stricture rates ranged from
0 to 27.5% .
3.4. Management of Leak (OR versus Stent). Regarding the
management of esophagogastric anastomotic leak, mini-
mally invasive options such as endoscopic stenting have been
increasingly described. We described our development of an
algorithm for the management of endoscopic perforations,
due to the need for multiple diagnostic modalities and
therapeutic interventions in a short period of time. For
esophageal perforations, an initial attempt at esophageal
stent placement or clipping was performed if feasible [42,
43]. Nguyen et al. performed a retrospective comparative
study of conventional treatments versus endoscopic stenting
for esophagogastric anastomotic leaks. Nine patients were
treated with conventional therapy, which included neck
drainage (n = 4), cervical esophagostomy (n = 2), thoraco-
scopic drainage with or without repair or T-tube placement
(n = 3), and 9 patients were treated with endoscopic stenting
with or without percutaneous drainage. Control of leak
was seen in 89% versus 100% in the conventional versus
60-day mortality was 0% for both groups . The above
data suggest that nonoperative, endoscopic management
of esophageal perforations or esophagogastric anastomotic
leaks is safe and feasible and may have comparable outcomes
to conventional treatment. A prospective, controlled study
is necessary to demonstrate any significant benefit with less
invasive, endoscopic interventions.
3.5. Quality of Life Parameters. Quality of life is increasingly
becoming an important outcome assessment for patients
who have undergone esophagectomy. Parameswaran et al.
and Nafteux et al. performed a comparative analysis of
outcomes, including health-related quality of life (HRQoL)
after open versus MIE. At 3 months, postoperative fatigue,
general pain, and gastrointestinal pain were all less with
MIE [45, 46]. Sundaram et al. evaluated perioperative
outcomes, survival, and quality of life (QoL) after open
versusMIEattheirinstitution(n = 104).RegardingQoL,the
authors employed the European Organization for Research
and Treatment of Cancer QoL and esophageal module
questionnaires, and patients were surveyed more than 1 year
after their surgery. There was no significant difference in any
of the quality of life parameters between open versus MIE
A symptom assessment study was performed by Mehran
et al. retrospectively comparing the functional benefits of
open esophagectomy with MIE. Propensity matching was
used to generate 44 pairs (of open versus MIE). Patients were
validated questionnaires. The reflux score was slightly worse
in the MIE group (P = 0.02), and there was no significant
the open group were satisfied with the overall result. Overall,
functional outcomes were comparable between open and
3.6. Robotic Esophagectomy. Thoracoscopic robot-assisted
MIE is increasingly being utilized. Weksler et al. performed
a retrospective comparison of 11 patients who underwent
thoracoscopic robot-assisted MIE versus 26 who underwent
MIE. No significant differences were seen in operative
time, blood loss, postoperative complications, duration of
mechanical ventilation, or length of stay. No significant
advantages were seen with robot-assisted MIE . Galvani
et al. at the University of Illinois reported on 18 patients who
underwentrobotic-assisted THE.Althoughanastomotic leak
occurred in 6 (33%) patients, other parameters such as mean
estimated blood loss of 54mL and low cardiopulmonary
suggested safety and feasibility of robotic-assisted THE .
This study, albeit the largest series published at that time,
was limited by its small size and lack of a control group for
comparison. Hence, Watson performed a review of robotic-
assisted MIE and concluded that the data on robotic-assisted
MIE suggest safety, feasibility, and equivalent outcomes
compared to open or MIE. However, there is no data to
suggest improved outcomes with robotic-assisted MIE in
terms of operative morbidity, pain, length of stay, operative
time, or total costs .
3.7. Question of Regionalization, Volume, and Training.
Enestvedt et al. reported trends in the management of
esophageal cancer, based on provider volume, among 618
esophageal surgeon respondents to a survey. Regarding the
adoption and continuation of MIE, a higher proportion of
the high volume surgeons—defined as surgeons performing
greater than 15 esophagectomies in 1 year—performed MIE
compared to the low volume surgeons (26.0 versus 16.5%,
P = 0.045). The majority of high volume surgeons (87%)
practiced in an academic setting and had cardiothoracic
training. Cited reasons for discontinuing the practice of
MIE were length of case, procedure-related morbidity and
mortality, and learning curve .
We previously have reported results of a database
study on esophagectomies performed in Florida which
demonstrated significantly lower risk-adjusted postoperative
mortality (OR 0.54, CI 0.32, 0.92) and similar leak rates of
8.2% in centers with higher volume compared with lower
The data suggest that operative mortality is not significantly
different between open and MIE, and operative morbidity
in a few studies is improved after MIE. Furthermore,
comparisons of functional result after open versus MIE
without pyloric drainage demonstrate little difference. The
data however are severely limited in that the majority of
the studies are either retrospective case series, or case-
control studies, or meta-analyses of retrospective case-
control studies—all limited by both selection and publi-
cation bias. Prospective, randomized studies are necessary
if any conclusion is to be made about the superiority of
one surgical therapy over the other. It is also not clear that
6 Gastroenterology Research and Practice
open or MIE. The data also does not demonstrate superior
outcomes as a result of prone positioning or gastric ischemic
conditioning. Leaks are increasingly being managed via
less invasive, endoscopic stenting with good outcomes,
but controlled, prospective studies are necessary to make
any conclusions about outcomes after endoscopic stenting
versus conventional treatments. The data does certainly
centers by experienced esophageal surgeons. Overall, MIE
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