Minimally Invasive Techniques for Resection

of Benign Esophageal Tumors

John Samphire, Philippe Nafteux, and James Luketich

With the emergence of minimally invasive surgery (MIS), laparoscopy and thoracoscopy have become
feasible and safe alternatives to open surgical procedures in the management of esophageal leiomyo-
mas. The indications for MIS resection of leiomyomas at our institution include the presence of
symptoms, confirmation of pathology to exclude malignancy, tumors greater than 2 cm in size or
tumors that show evidence of growth. Our approach of choice is right video-assisted thoracoscopic
surgery (VATS) for tumors of the thoracic esophagus and laparoscopy for tumors of the intra-abdom-
inal esophagus or gastroesophageal junction. A detailed description of these surgical approaches is
outlined in the following chapter. At our institution, nine patients, 8 males and 2 females with a mean
age of 54 years (range 42-67 years) had a minimally invasive surgical resection of an esophageal
leiomyoma between 1995 and 2001. The surgical approaches included right VATS enucleation (6) and
laparoscopic enucleation (3). There were no major morbidities, including postoperative leaks or mor-
talities. The mean hospital stay was 2.3 days. All tumors were benign leiomyomas with average size of
2.73 cm (range 0.9-8 cm) and there was no evidence of recurrence at a mean follow-up of 10 months.
Video-assisted enucleation has shown in our institution, as well as in others, that the procedure can
be performed safely with low mortality and morbidity. A VATS or laparoscopic approach to the
removal of leiomyomas should be the treatment of choice in centers experienced in minimally invasive
surgery.
© 2003 Elsevier Inc. All rights reserved.

Key Words: Minimally invasive surgery, esophagus, leiomyoma, benign tumors of the esophagus.

Introduction gery (VATS), is required for extraluminal–intra-

Benign tumors of the esophagus are quite rare.
They have a prevalence in autopsy studies of
0.45-0.59%1,2 and account for 5% of all esophageal
neoplasms.3 There have been a number of classi-
fication schemes proposed for benign esophageal
tumors2,4-7 but in surgical practice, the most use-
ful is that of Avezano et al8, who divided these
neoplasms into mucosal–intraluminal and ex-
traluminal–intramural. An endoscopic approach
is preferable for removal of mucosal–intralumi-
nal lesions. A transthoracic approach, either by
thoracotomy or video-assisted thoracoscopic sur-
From the Division of Thoracic and Foregut Surgery, UPMC
Presbyterian, Pittsburgh, PA, Philippe Nafteux, MD and Department
of Thoracic Surgery, UZ Gasthuisberg, 49 Herestraat, Leuven, Bel-
gium.
Address reprint requests to James D. Luketich, MD, Division of
Thoracic and Foregut Surgery, UPMC Presbyterian 200 Lothrop
Street (C-800), Pittsburgh, PA 15213.
© 2003 Elsevier Inc. All rights reserved.
1043-0679/03/1501-00005-4$30.00/0
doi:10.1016/S1043-0679(03)00005-4
mural tumors.9 Leiomyoma is by far the most
common intramural tumor, represents 70-80% of
all benign esophageal lesions,10,11 and will be the
focus of our discussion.
Over 85% of patients with benign esophageal
tumors are asymptomatic1 and are often discov-
ered as incidental endoscopic or radiological find-
ings. The most common presenting symptoms
are dysphagia, regurgitation, and retrosternal
discomfort, but patients can present with gastro-
intestinal bleeding or respiratory symptoms. The
diagnosis of benign esophageal neoplasms can
usually be made with barium esophagogram and
upper gastrointestinal endoscopy. A suspected
leiomyoma should not be endoscopically biopsied
to avoid increased risk of mucosal perforation
during enucleation.12 Endoscopic ultrasound has
emerged as a superior modality in the detection
and staging of smooth muscle tumors of the
esophagus.13 Computer tomography is also often
used to characterize location and size of the tu-
mor. If a hemangioma is suspected, contrast com-

Seminars in Thoracic and Cardiovascular Surgery, Vol 15, No 1 ( January), 2003: pp 35-43 35
36 Samphire, Nafteux, and Luketich
puted tomography scan or radionuclide angiogra-
phy can be helpful in making the diagnosis.14
Although generally attributed to Ohsawa in
1933,15 the first resection of a benign esophageal
neoplasm was reported one year prior by Sauer-
bruch.16 Since the first report by Everitt et al in
199217 of a thoracoscopic resection of an esopha-
geal leiomyoma, there has been an increased in-
terest in this minimally invasive technique. Both
laparoscopy and VATS for benign esophageal tu-
mors offers a feasible alternative to thoracotomy
or laparotomy with reduced surgical trauma,
morbidity and length of hospital stay.18,19
Indications
The indications for surgical management of
leiomyoma with minimally invasive techniques
are essentially the same as for open surgery. The
two major surgical indications are the presence of
symptoms and confirmation of pathology to ex-
clude malignancy.
The management of asymptomatic patients is
more controversial. The need for operative inter-
vention should be based on the likelihood of
symptom development and malignant degenera-
tion. Some surgeons advocate removal of all
leiomyomas regardless of size19 whereas others
use a size criterion for surgical intervention. Sev-
eral size criteria have been proposed as the min-
imal size for operative management, including
⬎3 cm20 and ⬎5 cm.12 The size discrepancy stems
from the lack of understanding of the natural
history of these benign tumors. The rate of
growth of leiomyomas is not clear, but large tu-
mors of more than 5 cm in size are more likely to
be symptomatic.3 Glanz and Grunebaum have
shown that this tumor can remain stable over a
long period of time.21 The rate of malignant
transformation to leiomyosarcoma appears rare,
if ever, with only two documented cases in the
literature.22,23 The correlation between tumor
size and malignancy in esophageal neoplasms has
not been well shown, unlike in the stomach and
small intestine where stromal tumors larger than
6 cm and 4 cm, respectively, have a greater like-
lihood of being malignant.24 Based on their endo-
scopic ultrasonographic experience, Tio and col-
leagues13 proposed that intramural tumors with a
diameter of less than 4 cm without evidence of
bleeding, obstruction or malignancy at esopha-
goscopy and on endoscopic ultrasonography, can
be followed at intervals of 3 months. Yamada et
al20 reported five endoscopic ultrasonographic
features that are more characteristic of malig-
nant myogenic tumors. They are 1) tumor diam-
eter of 3 cm or more, 2) nodular shape, 3) ulcer-
ation depth of 5 mm or more, 4) a heterogeneous
internal echo, and 5) the presence of an anechoic
area. They suggest that asymptomatic myogenic
tumors of the esophagus with less than three of
these features indicates a benign tumor that does
not need to be excised.
At our institution, we favor minimally invasive
surgical removal for virtually all symptomatic
leiomyomas. Asymptomatic tumors greater than
2 cm in size or that show evidence of growth will
be resected using minimally invasive techniques.
Small incidental asymptomatic leiomyomas, less
than 2 cm in size generally can be observed.
Follow-up should include clinical assessment and
radiologic evaluation with endoscopic ultrasound,
if available, or barium esophagogram at 1- or
2-year intervals.24
Other surgical indications include intralumi-
nal pedunculated neoplasms that are not amena-
ble to endoscopic removal. These include large
tumors or tumors with a broad (greater than 2
cm) highly vascularized or calcified pedicle.25
Patients with insufficient cardiopulmonary re-
serve or comorbid conditions that significantly
impair their ability to tolerate general anesthesia
form the only contraindication for minimally in-
vasive treatment of leiomyoma. Adhesions from a
previous operation or inflammatory condition are
not contra-indications for laparoscopy or VATS.
In these challenging cases, success of the mini-
mally invasive approach is dependent on the de-
gree of adhesions and the surgeon’s experience
with these techniques. In the case of a distal
esophageal leiomyoma, a contralateral VATS ap-
proach may be used to avoid dense adhesions.
Technique
Leiomyomas are usually solitary well-encapsu-
lated intramural lesions that can be easily enu-
cleated without requiring esophageal resection.
The approach is dependent on the tumor loca-
tion. Ninety percent of leiomyomas are located in
the middle and distal one third of the esophagus.
At our institution, a tumor of the intrathoracic
esophagus is usually approached from the right
side. Alternately, tumors located in the distal one
 PLEASE SUPPLY WORDING
Figure 1. Trocar position on the right chest for VATS approach.
third of the thoracic esophagus can be removed
through the left chest.26 Neoplasms located in the
intra-abdominal esophagus or gastroesophageal
junction can be accessed through laparoscopy.
VATS
For the enucleation of a leiomyoma using a right-
sided VATS approach, the patient is intubated
with a left-sided double lumen endotracheal tube.
The endotracheal tube position is confirmed by
bronchoscopy. The patient is positioned in the
full left lateral decubitus and the right lung is
deflated. The surgeon stands on the right side of
the table, the assistant on the left. Before drap-
ing the patient, a flexible gastroscope is inserted
in the esophagus. On the table, esophagoscopy
can confirm the precise tumor location for the
surgeon using transillumination and can confirm
esophageal mucosa integrity.
Four thoracoscopic ports are introduced into
the right hemithorax (Fig 1). The camera port
(10-mm, 30-degree viewing scope) is placed in
the seventh intercostal space just anterior to the
37
midaxillary line. Cautery should be used to dis-
sect through the intercostal muscle so as to
achieve complete port hemostasis and prevent
blood from dripping on the camera lens. Another
10-mm port is placed at the fourth intercostal
space anteriorly for lung retraction. The first
working port is placed in the eight interspace (10
mm) posterior to the line of the scapular tip, and
the second immediately below (5 mm) the scap-
ular tip. For distal third tumors, a single retract-
ing suture is placed in the central tendon of the
diaphragm (0-surgidac; US Surgical Corp.
[USSC]) using the Endo Stitch suturing device
(USSC). The suture is pulled out just over the
diaphragmatic insertion on the lateral chest wall
using the Endo Close device (USSC) through a
1-mm skin incision. This suture allows downward
retraction on the diaphragm giving excellent ex-
posure of the distal esophagus.
A fan retractor is used to retract the lung
anteriorly and superiorly as the ultrasonic coag-
ulating shears (USSC) are used to take down the
inferior pulmonary ligament. The mediastinal
38 Samphire, Nafteux, and Luketich

troduced under endoscopic guidance and inflated

with contrast medium, to compress the tumor
and facilitate separation of the tumor from both
the mucosal and muscular layers of the esopha-
gus.28 After enucleation, the tumor is placed in an
Endo Catch (USSC) and retrieved through the
antero-superior port. The right pleural cavity is
irrigated and intraoperative endoscopy with air
insufflation is performed to confirm mucosal in-
tegrity. If there is a perforation, the mucosa can
usually be closed thoracoscopically over a bougie
to avoid stricture formation.
After the tumor has been removed, the myot-
omy is then re-approximated with interrupted
2-0 surgidac (USSC) (Fig 4). A 28-chest tube is
inserted through the camera port for post-oper-
ative drainage. The lung is then reinflated and
the port sites are closed. For the left-sided VATS,
the port placement is the same as for the right-
sided approach.
The patients routinely undergo a barium swal-
low on the first postoperative day and oral intake

Figure 2. Esophageal myotomy exposing intramural

leiomyoma.

pleura overlying the esophageal tumor is then

opened. The dissection is performed with care to
preserve the vagus trunck and its branches. The
azygos vein is divided with an Endovascular GIA
stapler (USSC) if the added exposure is required.
The esophagus is mobilized to achieve ade-
quate exposure of the mass using the ultrasonic
shears. For left-sided tumors, a circumferential
dissection is needed in order to rotate the esoph-
agus and visualize the tumor well. Two penrose
drains can be placed around the esophagus to
facilitate dissection and an Endo Babcock grasper
can be used to rotate the esophagus.27 The esoph-
ageal muscularis propria is divided with electro-
cautery or ultrasonic shears to expose the esoph-
ageal leiomyoma (Fig 2). An 0-silk suture is
placed in the tumor for retraction. The mass is
then enucleated using a combination of sharp
and blunt dissection with the ultrasonic shears
and Endo Peanut (USSC) (Fig 3). Care is taken
not to enter the esophageal lumen. Some sur- Figure 3. Enucleation of leiomyoma with blunt dissec-
geons have used a hydrostatic balloon-dilator, in- tion.
 PLEASE SUPPLY WORDING 39

Steep reverse trendelenburg positioning facili-

tates exposure.
The distal esophagus is mobilized by dissec-
tion of the gastrohepatic and phrenoesophageal
ligaments. Both right and left crus are identified.
We routinely take down some of the short gastric
vessels using ultrasonic shears and clips where
necessary. The gastroesophageal fat pad is re-
flected to the patient’s right side, preserving both
anterior and posterior vagal truncks. The enucle-
ation of the leiomyoma is then performed in a
similar manner as described in the right VATS
approach for lesions in the distal esophagus. For
patients with documented preoperative gastro-
esophageal reflux disease or significant dissection
of the hiatus, we routinely perform a short floppy
Nissen fundoplication, using 2-0 surgidac with
the Endo Stitch suturing device performed over a
50 French bougie. A crural repair is completed
using 0-surgidac sutures. For gastric leiomyomas,
a wedge resection of stomach using the Endo GIA
stapler may be performed. The abdominal ports

Figure 4. Closure of myotomy.

is initiated on the same day if no esophageal leak

is identified. Patients are usually discharged on
the second or third postoperative day.

Laparoscopy
For intraabdominal or gastroesophageal junction
leiomyomas, our standard laparoscopic approach
to the esophageal hiatus is used. The patient is
placed in the supine position. The surgeon stands
on the patient’s right side and the assistant on
the left. Five abdominal ports are placed on the
anterior upper abdominal wall as illustrated in
Figure 5. The first port (10 mm) is placed in the
right paramedian position by a cut-down into the
peritoneum. A CO2 pneumoperitoneum is estab-
lished to a pressure of 15 mm Hg. The remaining
four 5-mm ports are placed under laparoscopic
visualization. The left lobe of the liver is re-
tracted upward to expose the esophageal hiatus
using a diamond flex retractor (Genzyme,
Tucker, GA) and held in place with a self-retain- Figure 5. Trocar position on abdomen for laparoscopic
ing system (Mediflex; Welmed Inc, Wexford, PA). approach.
40 Samphire, Nafteux, and Luketich
are closed using musculofascial and intracuticu-
lar sutures.
Esophageal Resection
An esophageal resection is rarely needed in the
treatment of leiomyomas. Seremetis et al29 re-
ported an esophagectomy rate of 10% and more
recently Bonavina et al18 reported a 4.5% rate of
esophagectomy in 66 patients. The surgical indi-
cations for esophagectomy include: 1) a very
large or annular leiomyoma that cannot be enu-
cleated by a VATS or open technique, 2) esoph-
ageal mucosa that is badly ulcerated or damaged
during enucleation and cannot be repaired in a
satisfactory manner, 3) symptomatic multiple
leiomyomas that cannot be enucleated or diffuse
leiomyomatosis, and 4) leiomyosarcoma sus-
pected and confirmed on biopsy. Based on our
extensive experience with minimally invasive
esophagectomy for malignant disease, this is our
approach of choice for the indications listed
above.
For a minimally invasive esophagectomy, the
patient would be positioned as for a right VATS
enucleation and the four ports would be placed in
the same fashion (Fig 1). The intrathoracic
esophagus is mobilized for its full length using
the ultrasonic shears. The azygos vein is divided
with the Endo GIA. A penrose drain placed cir-
cumferentially around the esophagus is used to
facilitate dissection and special care is taken to
avoid injury to the membranous part of the air-
ways and the proximal vagus nerves. Generous
application of hemoclips is used during the pos-
terior esophageal dissection to avoid chyle leaks
from the thoracic duct. The phrenoesophageal
ligament is left intact to avoid loss of the pneu-
moperitoneum during laparoscopy. The medias-
tinal pleura is left intact cranial to the azygos
vein to help the gastric pullup maintain a medi-
astinal location and prevent anastomotic leaks
from entering the right chest. The chest is then
closed as described above.
The patient is then positioned in the supine
position. A pneumoperitoneum is established and
five ports are placed in the anterior upper abdom-
inal wall (Fig 5). The left liver lobe is retracted
and steep reverse Trendelenburg positioning is
used as described in the laparoscopic enucleation
of a leiomyoma. The entire stomach is then mo-
bilized by first dividing the short gastric vessels
and then following the greater curvature distally,
preserving the right gastroepiploic vessel. The
gastrohepatic ligament is dissected. After the
posterior attachments of the stomach and pylorus
are divided, the left gastric vessels are transected
with an Endovascular GIA stapler. A pyloroplasty
is then performed followed by creation of a gas-
tric tube of approximately 5 cm in diameter using
multiple firings of Endo GIA stapler. An addi-
tional 10-mm port is placed in the right lower
quadrant for the placement of a needle catheter
feeding jejunostomy. The jejunum is secured to
the anterior abdominal wall to prevent leaks and
torsion. The phrenoesophageal ligament is then
divided and the gastric tube is tacked to the
proximal stomach.
A 4- to 6-cm transverse cervical incision is
made and the cervical esophagus is dissected and
exposed (Fig 5). Special care is taken to avoid
injury of both left and right laryngeal nerves.
Once mobilization is completed, the esophago-
gastric specimen is pulled up through the neck as
the assistant watches from the abdomen and in-
sures smooth passage and correct orientation of
the gastric tube. After the specimen has been
removed, a standard hand-sewn or stapled anas-
tomosis is performed with a nasogastric tube in-
serted under direct vision. The gastric conduit is
gently pulled back into the abdomen and secured
to the hiatus to prevent subsequent herniation of
abdominal contents. The abdominal incisions are
closed and the neck is drained and the wound
closed loosely.
Results
We reviewed our minimally invasive experience
of gastrointestinal stromal tumors of the esoph-
agus and gastroesophageal junction (GEJ) that
were resected between December 1995 and Au-
gust 2001.40 There were nine patients included
with a mean age of 54 years (range 42-67 years).
There were seven men and two women. There
were three tumors located in the middle third of
the esophagus, three located in the distal third of
the esophagus, and three at the GEJ. The pre-
senting symptoms included dysphagia (33%),
heartburn (33%), abdominal discomfort (11%),
bleeding (11%), or incidental finding (11%). Six
patients with tumors in the middle and distal
thirds of the esophagus were treated with a right
VATS enucleation whereas three patients with
 PLEASE SUPPLY WORDING
Table 1. Minimally Invasive Resection of Leiomyomas of the Esophagus
Authors Year
Bonavina18 1995
Izumi30 1996
Bardini9 1997
Roviaro19 1998
Luketich40 2002
GEJ tumors were managed with laparoscopic
enucleation. Two patients were treated with a
Collis–Nissen for a hiatus hernia associated with
significant gastroesophageal reflux disease. One
of the GEJ tumors required intraoperative muco-
sal repair with an Endo-GIA for an esophageal
perforation. There were no major morbidities,
including postoperative leaks or mortalities. The
mean hospital stay was 2.3 days. All tumors were
benign leiomyomas with average size of 2.73 cm
(range 0.9-8 cm). There was no evidence of re-
currence in all patients at a mean follow-up of 10
months (range 1-34 months) and there was com-
plete resolution of presenting symptoms.
In the literature, there are a small number of
publications on minimal invasive treatment of
benign stromal tumors of the esophagus and GEJ
(Table 1).9,18,19,30 Roviaro et al19 published on
7 patients that underwent thoracoscopic enucle-
ation using 3 ports and a small utility thora-
cotomy (4-5 cm). There were no deaths or com-
plications. One patient was converted to
thoracotomy for a large horseshoe-shaped mass
that was biopsied preoperatively. Bardini and
Asolati9 reported on five patients who were also
successfully enucleated through a thoracoscopic
approach. The only postoperative complication
was the development of a pseudodiverticulum
that was resected with a thoracotomy one year
later. This patient did not have a myotomy clo-
sure. Bonavina and colleagues18 reported success-
ful enucleation in six of eight patients that un-
derwent a right VATS approach. A formal
thoracotomy was performed in one patient due to
the inability to exclude the lung and a mucosal
tear in the second patient. They also reported a
patient with a pseudodiverticulum in whom the
muscle layer was not re-approximated at the time
of enucleation requiring repair through a thora-
cotomy eight months later. The length of hospital
stay was significantly reduced when comparing
VATS with thoracotomy (6.8 days versus 10.2
41
Patients Complications
6 Pseudodiverticulum (1)
3 None
5 Pseudodiverticulum (1)
7 None
9 None
days, P ⬍ 0.05). No patients required analgesics
after post-operative day one. Izumi et al. reported
the use of an intraluminal balloon push-out
method on three VATS cases.30 They felt the
instrument facilitated a faster and safer enucle-
ation. There were no deaths or complications in
this small group of patients.
Complications
The surgical therapy for esophageal leiomyoma is
safe with low mortality and morbidity. Rendina et
al31 reported an operative mortality rate of 1.3%
and 10.5% for open enucleation and esophagec-
tomy respectively. Bonavina et al.18 published a
0% mortality rate in 57 patients treated by open
enucleation and three patients managed with
open esophagectomy. There have been no re-
ported deaths in patients treated with a mini-
mally invasive enucleation.
Postoperative esophageal leak is a serious
complication that can arise because the mucosa
is perforated during enucleation and inade-
quately repaired. The use of intra-operative en-
doscopy with air insuflation is an important step
to safeguard against this complication. Seremetis
et al.29 reported no postoperative esophageal
leaks in open enucleations in an analysis of 838
cases. In review of the thoracoscopic literature,
one case of a recognized and repaired intraoper-
ative esophageal perforation was recorded but
there are no postoperative esophageal leaks.
There is no reported case of a leiomyoma recur-
rence in both the open and VATS literature.
Gastroesophageal reflux can occur after enu-
cleation of leiomyomas near the GEJ.32 This is
probably the result of a disturbance of the esoph-
ageal motility or lower esophageal sphincter
mechanism. An anti-reflux procedure can be
added at the time of enucleation if the lower
esophageal sphincter mechanism is disturbed
during the operation. There is no evidence to
42 Samphire, Nafteux, and Luketich
support or refute the need of a fundoplication
procedure in esophageal leiomyomas of the GEJ.
The most common complication reported in
the VATS literature is the development of a
pseudodiverticulum after enucleation. In both re-
ported cases, the myotomy was not closed.9,19 Clo-
sure of the myotomy, whenever possible, is rec-
ommended to prevent this complication.
Other Tumors
The most common intramural tumors after
leiomyomas include granular cell tumors (GCTs)
and hemangiomas. GCTs are rare and are felt to
arise from neural cells within the esophageal wall
with electron microscopic features and staining
properties similar to Schwann cells.6,33 Most
GCTs in the esophagus are found in the submu-
cosa and are located in the distal esophagus.
Multiple lesions are present in 20% of cases. The
clinical presentation and diagnostic evaluation
are similar to leiomyomas. The management of
these tumors remains controversial. Some au-
thors have argued that they should be surgically
removed on diagnosis because of the difficulty in
distinguishing benign from malignant forms,33
whereas others advocate biopsy and endoscopic
follow-up of small asymptomatic GCT.34,35 Symp-
tomatic tumors and tumors demonstrating rapid
growth should be removed. Historically, trans-
thoracic resection has been the treatment of
choice. There are no reported cases of VATS
resection, however, the minimally invasive ap-
proach can certainly be applied.
Hemangiomas are rare vascular tumors that
originate from the esophageal submucosa. They
range from small simple cystic structures to large
multinodular masses. The majority of hemangio-
mas are located in the middle esophagus.36 The
symptoms are similar to other benign tumors
although bleeding can be massive in case of tu-
mor rupture. Hemangiomas have been treated
with endoscopic resection,37 sclerotherapy,38 radi-
ation therapy, and open thoracotomy. Minimally
invasive surgery could certainly be used for resec-
tions of hemangiomas. There is one reported case
of video-thoracoscopic resection by Ramo et al.39
An endoscopic stapler was fired under direct en-
doscopic visualization to control mucosal continu-
ity and prevent stenotic complication.
Conclusion
A minimally invasive approach to benign tumors
of the esophagus as compared to open thoracot-
omy or laparotomy has many advantages. Video-
assisted enucleation has been shown in our insti-
tution, as well as in others, that the procedure
can be performed safely with low mortality and
morbidity. The VATS approach results in a
shorter hospital stay, decreased need for postop-
erative analgesic and improved cosmesis as com-
pared to open approaches. However, the most
significant advantage of minimally invasive sur-
gery is patients’ quick recovery and return to
normal daily activities. A VATS or laparoscopic
approach to the removal of leiomyomas should be
the treatment of choice in centers experienced in
minimally invasive surgery.
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