Korean J Thorac Cardiovasc Surg 2013;46:241-248
□ Review □
ISSN: 2233-601X (Print) ISSN: 2093-6516 (Online)
− 241 −
Department of Surgery, Keio University School of Medicine
Received: May 26, 2013, Revised: July 8, 2013, Accepted: July 8, 2013
Corresponding author: Yuko Kitagawa, Department of Surgery, Keio University School of Medicine, 35 Shinanomachi, Shinjuku-ku, 160-8582,
(Tel) 81-3-3353-1211 (Fax) 81-3-3355-4707 (E-mail) email@example.com
C The Korean Society for Thoracic and Cardiovascular Surgery. 2013. All right reserved.
CC This is an open access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creative-
commons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the
original work is properly cited.
Current Status and Future Perspectives on Minimally Invasive
Hirofumi Kawakubo, M.D., Hiryoya Takeuchi, M.D., Yuko Kitagawa, M.D.
Esophageal cancer has one of the highest malignant potentials of any type of tumor. The 3-field lymph node dissection
is the standard procedure in Japan for surgically curable esophageal cancer in the middle or upper thoracic esophagus.
Minimally invasive esophagectomy is being increasingly performed in many countries, and several studies report its fea-
sibility and curability; further, the magnifying effect of the thoracoscope is another distinct advantage. However, few stud-
ies have reported that minimally invasive esophagectomy is more beneficial than open esophagectomy. A recent
meta-analysis revealed that minimally invasive esophagectomy reduces blood loss, respiratory complications, the total
morbidity rate, and hospitalization duration. A randomized study reported that the pulmonary infection rate, pain score,
intraoperative blood loss, hospitalization duration, and postoperative 6-week quality of life were significantly better with
the minimally invasive procedure than with other procedures. In the future, sentinel lymph node mapping might play a
significant role by obtaining individualized information to customize the surgical procedure for individual patients’ specific
Key words: 1. Esophageal neoplasms
2. Minimally invasive surgical procedures
3. Video-assisted thoracic surgery
4. Sentinel node navigation surgery
5. Lymph node dissection
The global incidence of esophageal cancer has increased in
the past decades [1,2], and it has one of the highest malignant
potentials of any type of tumor. As per the data of the
American Joint Committee on Cancer, the postoperative
5-year survival rate of stage I esophageal cancer is about
90%, and decreases to 45% for stage II, 20% for stage III,
and only 10% for stage IV patients . Although the effec-
tiveness of extended lympadenectomy for esophageal cancer
remains to be demonstrated by randomized prospective stud-
ies, better survival was obtained after 3-field lymph node dis-
section than 2-field lymph node dissection in Japan [4,5].
Three-field lymph node dissection, including dissection of cer-
vical, mediastinal, and abdominal lymph nodes, is the standard
procedure employed for surgically curable esophageal cancer
located in the middle or upper thoracic esophagus in Japan.
The majority of Western surgical groups differ with Japanese
groups on their strategy for surgical management of esoph-
ageal carcinoma. Many investigators in Europe and the United
States have reported that the results of concurrent chemo-
radiotherapy are comparable to those of surgery [6,7]; how-
Hirofumi Kawakubo, et al
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Table 1. Contraindication of minimally invasive esophagectomy
Extensive pleural adhesions
Tumor infiltrating adjacent structures
Impaired circulatory or pulmonary function prohibiting single-lung ventilation
A concomitant serious medical condition, such as sever diabetes mellitus, chronic renal failure, or liver cirrhosis
Patients refusal to undergo thoracoscopic surgery
Patients who received radiation (controversial)
ever, most of the surgical procedures in such studies are not
as radical as the Japanese standard procedures, and the overall
survival rate after surgery is lower than that of the Japanese
standard. Nevertheless, some Western surgeons have asserted
the importance of radical lymph node dissection [8,9].
Extended lympadenectomy is extremely invasive and leads
to high operative morbidity, particularly because of pulmonary
complications . Since the first report of thoracoscopic esoph-
agectomy by Cuschieri et al.  in 1992, the adoption of mini-
mally invasive esophagectomy has increased in many countries
. Minimally invasive esophagectomy might minimize injury
to the chest wall and is believed to reduce surgical
invasiveness. Moreover, several reports have indicated its feasi-
bility and curative efficacy [12-15]. Although the incidence of
minimally invasive surgery is increasing in Japan, only 20%
of esophagectomies performed in 2009 were conducted using
a minimally invasive approach . Three-field lymphadenec-
tomy is the standard surgical method employed in Japan; the
same degree of lymph node dissection must be performed even
for a minimally invasive esophagectomy. Minimally invasive
surgery is used less often for esophagectomy, considering the
technical challenges of esophagectomy accompanied by ex-
tensive lymphadenectomy, which is the Japanese standard sur-
Although thoracoscopic esophagectomy has been promoted
due to its minimal invasiveness, another distinctive advantage
of minimally invasive esophagectomy is the magnifying effect
of the thoracoscope, as very small structures can be clearly
identified. Thus, the surgery can be performed with more pre-
cision, preserving the nerves and vessels.
It has still not been clearly demonstrated whether mini-
mally invasive surgery is associated with lower morbidity and
mortality. Furthermore, the oncologic outcomes after mini-
mally invasive surgery are still controversial. Hence, a pro-
spective randomized study of open versus minimally invasive
surgery is needed. However, although the incidence of esoph-
ageal cancer is increasing, and it is among the 10 most com-
mon cancers worldwide, few patients are candidates for po-
tentially curative resection. In addition, a prospective random-
ized study would be difficult to complete within a reasonable
timeframe. Because the technique of minimally invasive sur-
gery is not standardized, even in high volume centers, it is
very difficult to set up multi-institutional studies.
INDICATIONS FOR MINIMALLY INVASIVE
Minimally invasive esophagectomy was initially used for
T1 and T2 esophageal tumors without neoadjuvant therapy
[12,16]. However, the indications for minimally invasive
esophagectomy have been expanded to include more ad-
vanced cancers. Now, the indications for minimally invasive
esophagectomy are almost the same as those for open
surgery. The right lung should be deflated during the thoraco-
scopic procedure to provide a good operative field. Patients
must be able to tolerate single-lung ventilation for a sufficient
time period. The following are the contraindications for mini-
mally invasive esophagectomy (Table 1): extensive pleural
adhesions; a tumor infiltrating adjacent structures; impaired
circulatory or pulmonary function prohibiting single-lung ven-
tilation; presence of concomitant serious medical conditions
such as severe diabetes mellitus, chronic renal failure, or liver
cirrhosis; and patients’ refusal to undergo thoracoscopic
surgery. Moreover, in our institution, patients who have re-
ceived radiation in the mediastinum are also contraindicated
for minimally invasive esophagectomy because the radiation
Minimally Invasive Esophagectomy
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Fig. 1. Hybrid position. (A) Prone position. (B) Left semiprone position. (C) Left lateral decubitus position.
might have destroyed the layered structure and have caused
tissue adhesions such that the layers cannot be recognized to
cut and divide. However, in some institutions, patients are
still indicated for minimally invasive surgery after undergoing
radiation in the mediastinum [17,18].
APPROACH FOR MINIMALLY INVASIVE
The two approaches for minimally invasive esophagectomy
are the prone position and the left lateral decubitus position.
Cushieri  reported on performing minimally invasive
esophagectomy in the prone position for 6 patients in 1994.
However, minimally invasive esophagectomy has been most
commonly performed in the left lateral decubitus position;
nevertheless, since the advantages of this surgery in the prone
position have been reported, this position has recently been
widely adopted. In the prone position, the mediastinum lies in
its usual middle position, and the chest and abdomen are free
of compression. During surgery in the prone position, the
right lung is partially collapsed by gravity, and the thoracic
cavity is insufflated with carbon dioxide up to 8 mmHg.
Cuschieri et al.  performed the first minimally invasive
esophagectomy in the prone position to reduce the incidence
of pulmonary infections noted following lateral thoracoscopy.
Opening and exposing the mediastinum by gravity and artifi-
cial pneumothorax in the prone position allows for optimum
visualization of the mediastinum, particularly the middle and
lower mediastinum. However, it is easier to explore the surgi-
cal field in the upper mediastinum in the left lateral decubitus
position, particularly around the left recurrent laryngeal nerve.
The left paratracheal lymph node, which must be dissected, is
located anterior to the left recurrent laryngeal nerve. An as-
sistant must skillfully rotate the trachea to expose the surgical
field. To achieve constant exposure of the anterior side of the
left recurrent laryngeal nerve is very difficult in the prone po-
sition; thus, we perform the upper mediastinal procedure in
the left lateral decubitus position. The patient is positioned in
the left semiprone position during the procedure; this position
enables optimal positioning, and the left lateral decubitus po-
sition and prone position can be achieved by rotating the sur-
gical table (Fig. 1A, B). Our approach for minimally invasive
surgery is a hybrid position: the left lateral decubitus position
was selected for the upper mediastinum procedure and the
prone position for the middle and lower mediastinum
procedure. This hybrid position enables us to immediately
convert to from thoracoscopic to open surgery in the event of
an emergency, which is an obvious disadvantage of the prone
Recently, the advantages of minimally invasive esoph-
agectomy in the prone position have been reported in a large
series of nonrandomized historical control studies. Better oper-
ative exposure, improved surgeon ergonomics, shorter oper-
ative time, less blood loss, and reduced pulmonary infection
were observed in the prone position than in the left lateral de-
cubitus position [20-22]. In their historical control study,
Noshiro et al.  reported the potential benefits of the prone
position for thoracoscopic esophagectomy even when accom-
panied by extensive lymphadenectomy. However, no random-
ized prospective studies have compared the two approaches,
which might be difficult because of the learning curve for both
the techniques and because the advantages of each technique
Hirofumi Kawakubo, et al
− 244 −
Fig. 2. Position for a minithoracotomy and the ports used in our
method. (A) Third intercostal space on the midaxillary line; 12-mm
trocar. (B) Fifth intercostal space on the posterior axillary line; 5-mm
trocar. (C) Seventh intercostal space on the midaxillary line; 12-mm
trocar. (D) Seventh intercostal space on the midaxillary line; 12-mm
trocar. (E) Tenth intercostal space; 12-mm trocar.
Fig. 3. Dissection of paratracheal
lymph nodes. (A) Along the right re-
current laryngeal nerve. (B) Along the
left recurrent laryngeal nerve.
are influenced by the patients and the surgical staff at each
institution. Thus, a standard approach cannot be determined.
1) Thoracoscopic procedures
The patient is positioned in the left semiprone position.
This position is optimal because the left lateral decubitus and
prone positions can be achieved by rotating the surgical table.
First, the patient is positioned in the left lateral decubitus
position. Five thoracic trocars and a small incision (4 cm) in
the fifth intercostal space are introduced into the right chest
(Fig. 2). After the azygos vein arch is divided using the Endo
GIA Universal system, the upper thoracic esophagus is mobi-
lized circumferentially, and the paraesophageal and para-
tracheal lymph nodes along the right and left recurrent lar-
yngeal nerves are dissected (Fig. 3). The thoracic duct is al-
ways resected. The right bronchial artery is divided, and the
left bronchial artery is always preserved to prevent bronchial
ischemia. Subsequently, the patient’s bed is rotated to the
prone position, and the thoracic cavity is insufflated with 7
mmHg of carbon dioxide to maintain right lung collapse dur-
ing thoracoscopy. The middle and lower esophagus is mobi-
lized, and the middle and lower paraesophageal, trans-
bronchial, and subcarinal nodes are dissected. The cervical
esophagus is divided using the Endo GIA Universal system.
The stumps of the esophagus are connected using a string to
deliver a gastric conduit to the neck through the posterior
2) Abdominal and cervical procedures
The patient is placed in the supine position. We perform
hand-assisted laparoscopic surgery to dissect the abdominal
lymph nodes and create a gastric conduit. A 7.5-cm horizontal
minilaparotomy incision is made in the upper right abdomen,
and 3 trocars are introduced under laparoscopic guidance. After
the left hand of the operator is inserted, the greater omentum
is divided 3 to 4 cm from the arcade of the gastroepiploic ves-
sels with the use of a vessel sealing system under an 8-mmHg
pneumoperitoneum (Ligasure Blunt chip; Covidien, Mansfield,
MA, USA). The left gastroepiploic and short gastric vessels are
Minimally Invasive Esophagectomy
− 245 −
divided along the splenic hilum, and the gastric fornix is
mobilized. The lesser omentum is divided along with preserva-
tion of the right gastric vessels. The abdominal esophagus is
isolated along the hiatus of the diaphragm, and the thoracic
esophagus is pulled into the abdominal space. After the lymph
node around the celiac axis is dissected, the left gastric artery
and vein are divided. The esophagus and stomach are pulled
out from the abdominal incision, creating a gastric conduit.
A collar incision is made above the suprasternal notch.
After dissecting the paraesophageal lymph node along the re-
current laryngeal nerves and supraclavicular lymph node, the
gastric conduit is pulled out from the cervical incision through
the posterior mediastinal route. An esophagogastrostomy is
performed with a circular stapler.
3) Postoperative management
All of the patients are admitted to the intensive care unit
for stabilization and overnight intubation following surgery.
Thereafter, patients are detubated the next day and discharged
to the general surgical unit on postoperative day 3. Patients
are administered epidural analgesia during the first 5 post-
operative days and are encouraged to move out of bed after
being detubated in order to regain early mobilization from the
first day after surgery. Subsequently, patients are discharged
when they can consume solid food without aspiration.
CURRENT EVIDENCE FOR MINIMALLY
1) Learning curve
Esophagectomy necessitates a certain amount of learning;
extensive mediastinal lymph node dissection might require ad-
ditional experience; and minimally invasive surgery requires
much more experience. The benefits of minimally invasive
esophagectomy tend to relate to the number of cases
experienced. On the basis of patient experience, Leketich et
al.  concluded that minimally invasive esophagectomy
was not beneficial for 8 patients, of uncertain value for 77
patients, and beneficial for 222 patients. Osugi et al.  re-
ported that basic skills seem to be acquired during the first
17 cases, and the most remarkable difference was observed
between the first 36 cases and the others. According to a re-
port by Ninomiya et al. , they safely mastered the basic
skills of minimally invasive surgery in a relatively short peri-
od of time after only 10 cases of esophageal cancer under the
direction of an experienced surgeon and a regular surgical
team. Although the surgeon had little experience with esoph-
ageal surgery at the beginning, supervision and instruction
from another fully trained surgeon allowed the surgeon to
safely perform minimally invasive esophagectomy during the
induction period. The primary education of the regular surgi-
cal team by post-accreditation supervision is essential for safe
and rapid to start minimally invasive esophagectomy.
2) Surgical data
A few large comparable studies have reported that mini-
mally invasive esophagectomy is more beneficial than open
esophagectomy. Two recent studies have been published: one
was a meta-analysis and the other a multicenter, open-label,
randomized control trial of minimally invasive surgery versus
Nagpal et al.  reported a meta-analysis of 12 studies. The
studies included a total of 672 patients undergoing minimally
invasive surgery and 612 undergoing open esophagectomy. The
primary outcomes of their study were 30-day mortality and
anastomotic leaks. The secondary outcomes included surgical
outcomes, other postoperative outcomes, and oncological out-
comes in terms of lymph nodes retrieved. Minimally invasive
esophagectomy reduced blood loss, respiratory complications,
total morbidity rates, and duration of hospitalization.
Biere et al.  from the Netherlands published the TIME
trial (traditional invasive vs. minimally invasive esophagectomy)
data in the Lancet. This was the first report of a multicenter,
open-label, randomized control trial to compare minimally in-
vasive esophagectomy and open esophagectomy. They pre-
sented evidence of short-term benefits of the minimally in-
vasive technique for patients with resectable cancer of the
esophagus or gastroesophageal junction. They randomly as-
signed 56 patients to the open esophagectomy group and 59
to the minimally invasive esophagectomy group at 5 study cen-
ters in 3 countries between June 1, 2009 and March 31, 2011.
Sixteen patients (29%) in the open esophagectomy group devel-
oped pulmonary infection in the first 2 weeks compared with
5 patients (9%) in the minimally invasive group (relative risk
Hirofumi Kawakubo, et al
− 246 −
[RR], 0.30; 95% confidence interval [CI], 0.12 to 0.76;
p=0.005). Nineteen (34%) of 56 patients in the open esoph-
agectomy group developed a pulmonary infection during hospi-
talization compared with 7 (12%) of 59 patients in the mini-
mally invasive esophagectomy group (RR, 0.35; 95% CI, 0.16
to 0.78; p=0.005). Furthermore, secondary endpoints, including
pain score, intraoperative blood loss, duration of hospitalization,
and quality of life at 6 weeks after surgery, were significantly
better following the minimally invasive procedure than in the
open group. However, the pathological parameters, number of
lymph nodes retrieved, and postoperative mortality rate did not
differ significantly between the two treatment groups. Inhospital
mortality rates were low in both the minimally invasive and
open groups (2 [3%] of 59 patients vs. 1 [2%] of 56 patients).
3) Oncological results
Few reports are available regarding the long-term outcomes
following minimally invasive esophagectomy. In many of the
reports, the number of patients and follow-up periods are in-
sufficient [13,16,29,30]. Luketich et al.  observed that pa-
tient survival at 40 months after surgery was about 70% for
stage I patients, but it was as low as 30% and 20% for stage
II and III patients, respectively. On the other hand, Smithers
et al.  analyzed patients who underwent resection using
one of three esophagectomy techniques, including open, thor-
acoscopic-assisted, or a thoracoscopic/laparoscopic approach
(total minimally invasive esophagectomy), to assess post-
operative variables, adequacy of cancer clearance, and patient
survival from a prospective database of all the patients treated
for cancer of the esophagus or the esophagogastric junction
. The number of patients undergoing each procedure was
as follows: open, 114; thoracoscopic-assisted, 309; and total
minimally invasive esophagectomy, 23. The nodal harvest for
each of the defined regions dissected was not significantly
different when the approaches were compared. Further, no
difference was observed in the time to recurrence among the
3 groups for patients with invasive cancer, and no difference
in patient survival was observed among the groups either.
The concepts regarding the sentinel lymph node (SLN), in-
traoperative lymphatic mapping, and sentinel lymphadenec-
tomy appear promising. We have performed radio-guided
SLN mapping for cT1aN0 or cT2N0 esophageal cancer to
verify the feasibility of SLN mapping. An SLN is defined as
the lymph node that is first to receive lymphatic drainage
from a tumor site . The SLN is believed to be likely to
be the first micrometastasis site along the lymphatic drainage
route from the primary lesion. If the SLN is recognized and
is negative for metastasis, there might be no metastasis to
other lymph nodes. The pathologic status of the SLN is con-
sidered to predict the status of all of the regional lymph no-
des and might thus avoid unnecessary radical lymph node
SLN mapping and biopsy were first applied to melanoma
and subsequently extended to breast cancer and many other
solid tumors [33-36]. These techniques can benefit patients by
avoiding various complications that might result from un-
necessary radical lymph node dissection in cases wherein the
SLN is negative for metastasis. We developed a radio-guided
method to detect SLN in esophageal cancer  rather than
the conventional blue-dye method. One day (within 16 hours)
before surgery, a 2.0-mL volume of technetium-99 m tin col-
loid solution (150 MBq) is injected into the submucosal layer
at 4 quadrants around the primary tumor using an endoscopic
puncture needle. Preoperative lymphoscintigraphy is usually
obtained 3 to 4 hours after injection. The distribution of
SLNs in esophageal cancers extends broadly from the cervical
to abdominal areas. Takeuchi et al.  reported our results
of a radio-guided SLN navigation validation study of esoph-
ageal cancer; 75 consecutive patients who were diagnosed
preoperatively with T1N0M0 or T2N0M0 primary esophageal
cancer were enrolled. SLNs were identified in 71 (95%) of
75 patients. The mean number of identified SLNs per case
was 4.7; further, 29 (88%) of the 33 patients with LN meta-
stasis revealed positive SLNs, and the diagnostic accuracy on
the basis of SLN status was 94%.
Intraoperative SLN (i.e., radio-labeled lymph node) sam-
pling is performed using a handheld gamma probe (GPS
Navigator; Covidien, Tokyo, Japan). In addition, gamma
probing is feasible for thoracoscopic or laparoscopic sampling
of the SLN using a special gamma detector, which is in-
troducible from trocar ports. An SLN located in the cervical
Minimally Invasive Esophagectomy
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area can be identified by percutaneous gamma probing. All
SLNs were sent for an intraoperative pathology examination.
SLN mapping was successful during thoracoscopic esoph-
agectomy as well as during a conventional surgical procedure.
In the future, SLN mapping might play a significant role in
eliminating the necessity of uniform application of a highly in-
vasive surgery by obtaining individual information to permit
adjustments and modifications to the surgical procedure for
patients. If SLN is recognized and is negative for metastasis,
unnecessary extended lymph node dissection could be avoided.
Thus, thoracoscopic surgery with SLN mapping and navigation
might become a promising strategy for minimally invasive in-
dividualized surgery for early stage esophageal cancer.
CONFLICT OF INTEREST
No potential conflict of interest relevant to this article was
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