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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-


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


phy can be helpful in making the diagnosis.14 al20 reported five endoscopic ultrasonographic
Although generally attributed to Ohsawa in features that are more characteristic of malig-
1933,15 the first resection of a benign esophageal nant myogenic tumors. They are 1) tumor diam-
neoplasm was reported one year prior by Sauer- eter of 3 cm or more, 2) nodular shape, 3) ulcer-
bruch.16 Since the first report by Everitt et al in ation depth of 5 mm or more, 4) a heterogeneous
199217 of a thoracoscopic resection of an esopha- internal echo, and 5) the presence of an anechoic
geal leiomyoma, there has been an increased in- area. They suggest that asymptomatic myogenic
terest in this minimally invasive technique. Both tumors of the esophagus with less than three of
laparoscopy and VATS for benign esophageal tu- these features indicates a benign tumor that does
mors offers a feasible alternative to thoracotomy not need to be excised.
or laparotomy with reduced surgical trauma, At our institution, we favor minimally invasive
morbidity and length of hospital stay.18,19 surgical removal for virtually all symptomatic
leiomyomas. Asymptomatic tumors greater than
2 cm in size or that show evidence of growth will
Indications be resected using minimally invasive techniques.
The indications for surgical management of Small incidental asymptomatic leiomyomas, less
leiomyoma with minimally invasive techniques than 2 cm in size generally can be observed.
are essentially the same as for open surgery. The Follow-up should include clinical assessment and
two major surgical indications are the presence of radiologic evaluation with endoscopic ultrasound,
symptoms and confirmation of pathology to ex- if available, or barium esophagogram at 1- or
clude malignancy. 2-year intervals.24
The management of asymptomatic patients is Other surgical indications include intralumi-
more controversial. The need for operative inter- nal pedunculated neoplasms that are not amena-
vention should be based on the likelihood of ble to endoscopic removal. These include large
symptom development and malignant degenera- tumors or tumors with a broad (greater than 2
tion. Some surgeons advocate removal of all cm) highly vascularized or calcified pedicle.25
leiomyomas regardless of size19 whereas others Patients with insufficient cardiopulmonary re-
use a size criterion for surgical intervention. Sev- serve or comorbid conditions that significantly
eral size criteria have been proposed as the min- impair their ability to tolerate general anesthesia
imal size for operative management, including form the only contraindication for minimally in-
⬎3 cm20 and ⬎5 cm.12 The size discrepancy stems vasive treatment of leiomyoma. Adhesions from a
from the lack of understanding of the natural previous operation or inflammatory condition are
history of these benign tumors. The rate of not contra-indications for laparoscopy or VATS.
growth of leiomyomas is not clear, but large tu- In these challenging cases, success of the mini-
mors of more than 5 cm in size are more likely to mally invasive approach is dependent on the de-
be symptomatic.3 Glanz and Grunebaum have gree of adhesions and the surgeon’s experience
shown that this tumor can remain stable over a with these techniques. In the case of a distal
long period of time.21 The rate of malignant esophageal leiomyoma, a contralateral VATS ap-
transformation to leiomyosarcoma appears rare, proach may be used to avoid dense adhesions.
if ever, with only two documented cases in the
literature.22,23 The correlation between tumor
size and malignancy in esophageal neoplasms has Technique
not been well shown, unlike in the stomach and Leiomyomas are usually solitary well-encapsu-
small intestine where stromal tumors larger than lated intramural lesions that can be easily enu-
6 cm and 4 cm, respectively, have a greater like- cleated without requiring esophageal resection.
lihood of being malignant.24 Based on their endo- The approach is dependent on the tumor loca-
scopic ultrasonographic experience, Tio and col- tion. Ninety percent of leiomyomas are located in
leagues13 proposed that intramural tumors with a the middle and distal one third of the esophagus.
diameter of less than 4 cm without evidence of At our institution, a tumor of the intrathoracic
bleeding, obstruction or malignancy at esopha- esophagus is usually approached from the right
goscopy and on endoscopic ultrasonography, can side. Alternately, tumors located in the distal one
PLEASE SUPPLY WORDING 37

Figure 1. Trocar position on the right chest for VATS approach.

third of the thoracic esophagus can be removed midaxillary line. Cautery should be used to dis-
through the left chest.26 Neoplasms located in the sect through the intercostal muscle so as to
intra-abdominal esophagus or gastroesophageal achieve complete port hemostasis and prevent
junction can be accessed through laparoscopy. blood from dripping on the camera lens. Another
10-mm port is placed at the fourth intercostal
VATS space anteriorly for lung retraction. The first
working port is placed in the eight interspace (10
For the enucleation of a leiomyoma using a right-
mm) posterior to the line of the scapular tip, and
sided VATS approach, the patient is intubated
the second immediately below (5 mm) the scap-
with a left-sided double lumen endotracheal tube.
ular tip. For distal third tumors, a single retract-
The endotracheal tube position is confirmed by
ing suture is placed in the central tendon of the
bronchoscopy. The patient is positioned in the
full left lateral decubitus and the right lung is diaphragm (0-surgidac; US Surgical Corp.
deflated. The surgeon stands on the right side of [USSC]) using the Endo Stitch suturing device
the table, the assistant on the left. Before drap- (USSC). The suture is pulled out just over the
ing the patient, a flexible gastroscope is inserted diaphragmatic insertion on the lateral chest wall
in the esophagus. On the table, esophagoscopy using the Endo Close device (USSC) through a
can confirm the precise tumor location for the 1-mm skin incision. This suture allows downward
surgeon using transillumination and can confirm retraction on the diaphragm giving excellent ex-
esophageal mucosa integrity. posure of the distal esophagus.
Four thoracoscopic ports are introduced into A fan retractor is used to retract the lung
the right hemithorax (Fig 1). The camera port anteriorly and superiorly as the ultrasonic coag-
(10-mm, 30-degree viewing scope) is placed in ulating shears (USSC) are used to take down the
the seventh intercostal space just anterior to 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- and then following the greater curvature distally,
lar sutures. preserving the right gastroepiploic vessel. The
gastrohepatic ligament is dissected. After the
posterior attachments of the stomach and pylorus
Esophageal Resection are divided, the left gastric vessels are transected
An esophageal resection is rarely needed in the with an Endovascular GIA stapler. A pyloroplasty
treatment of leiomyomas. Seremetis et al29 re- is then performed followed by creation of a gas-
ported an esophagectomy rate of 10% and more tric tube of approximately 5 cm in diameter using
recently Bonavina et al18 reported a 4.5% rate of multiple firings of Endo GIA stapler. An addi-
esophagectomy in 66 patients. The surgical indi- tional 10-mm port is placed in the right lower
cations for esophagectomy include: 1) a very quadrant for the placement of a needle catheter
large or annular leiomyoma that cannot be enu- feeding jejunostomy. The jejunum is secured to
cleated by a VATS or open technique, 2) esoph- the anterior abdominal wall to prevent leaks and
ageal mucosa that is badly ulcerated or damaged torsion. The phrenoesophageal ligament is then
during enucleation and cannot be repaired in a divided and the gastric tube is tacked to the
satisfactory manner, 3) symptomatic multiple proximal stomach.
leiomyomas that cannot be enucleated or diffuse A 4- to 6-cm transverse cervical incision is
leiomyomatosis, and 4) leiomyosarcoma sus- made and the cervical esophagus is dissected and
pected and confirmed on biopsy. Based on our exposed (Fig 5). Special care is taken to avoid
extensive experience with minimally invasive injury of both left and right laryngeal nerves.
esophagectomy for malignant disease, this is our Once mobilization is completed, the esophago-
approach of choice for the indications listed gastric specimen is pulled up through the neck as
above. the assistant watches from the abdomen and in-
For a minimally invasive esophagectomy, the sures smooth passage and correct orientation of
patient would be positioned as for a right VATS the gastric tube. After the specimen has been
enucleation and the four ports would be placed in removed, a standard hand-sewn or stapled anas-
the same fashion (Fig 1). The intrathoracic tomosis is performed with a nasogastric tube in-
esophagus is mobilized for its full length using serted under direct vision. The gastric conduit is
the ultrasonic shears. The azygos vein is divided gently pulled back into the abdomen and secured
with the Endo GIA. A penrose drain placed cir- to the hiatus to prevent subsequent herniation of
cumferentially around the esophagus is used to abdominal contents. The abdominal incisions are
facilitate dissection and special care is taken to closed and the neck is drained and the wound
avoid injury to the membranous part of the air- closed loosely.
ways and the proximal vagus nerves. Generous
application of hemoclips is used during the pos-
terior esophageal dissection to avoid chyle leaks Results
from the thoracic duct. The phrenoesophageal We reviewed our minimally invasive experience
ligament is left intact to avoid loss of the pneu- of gastrointestinal stromal tumors of the esoph-
moperitoneum during laparoscopy. The medias- agus and gastroesophageal junction (GEJ) that
tinal pleura is left intact cranial to the azygos were resected between December 1995 and Au-
vein to help the gastric pullup maintain a medi- gust 2001.40 There were nine patients included
astinal location and prevent anastomotic leaks with a mean age of 54 years (range 42-67 years).
from entering the right chest. The chest is then There were seven men and two women. There
closed as described above. were three tumors located in the middle third of
The patient is then positioned in the supine the esophagus, three located in the distal third of
position. A pneumoperitoneum is established and the esophagus, and three at the GEJ. The pre-
five ports are placed in the anterior upper abdom- senting symptoms included dysphagia (33%),
inal wall (Fig 5). The left liver lobe is retracted heartburn (33%), abdominal discomfort (11%),
and steep reverse Trendelenburg positioning is bleeding (11%), or incidental finding (11%). Six
used as described in the laparoscopic enucleation patients with tumors in the middle and distal
of a leiomyoma. The entire stomach is then mo- thirds of the esophagus were treated with a right
bilized by first dividing the short gastric vessels VATS enucleation whereas three patients with
PLEASE SUPPLY WORDING 41

Table 1. Minimally Invasive Resection of Leiomyomas of the Esophagus


Authors Year Patients Complications
Bonavina18 1995 6 Pseudodiverticulum (1)
Izumi30 1996 3 None
Bardini9 1997 5 Pseudodiverticulum (1)
Roviaro19 1998 7 None
Luketich40 2002 9 None

GEJ tumors were managed with laparoscopic days, P ⬍ 0.05). No patients required analgesics
enucleation. Two patients were treated with a after post-operative day one. Izumi et al. reported
Collis–Nissen for a hiatus hernia associated with the use of an intraluminal balloon push-out
significant gastroesophageal reflux disease. One method on three VATS cases.30 They felt the
of the GEJ tumors required intraoperative muco- instrument facilitated a faster and safer enucle-
sal repair with an Endo-GIA for an esophageal ation. There were no deaths or complications in
perforation. There were no major morbidities, this small group of patients.
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 Complications
(range 0.9-8 cm). There was no evidence of re- The surgical therapy for esophageal leiomyoma is
currence in all patients at a mean follow-up of 10 safe with low mortality and morbidity. Rendina et
months (range 1-34 months) and there was com- al31 reported an operative mortality rate of 1.3%
plete resolution of presenting symptoms. and 10.5% for open enucleation and esophagec-
In the literature, there are a small number of tomy respectively. Bonavina et al.18 published a
publications on minimal invasive treatment of 0% mortality rate in 57 patients treated by open
benign stromal tumors of the esophagus and GEJ enucleation and three patients managed with
(Table 1).9,18,19,30 Roviaro et al19 published on open esophagectomy. There have been no re-
7 patients that underwent thoracoscopic enucle- ported deaths in patients treated with a mini-
ation using 3 ports and a small utility thora- mally invasive enucleation.
cotomy (4-5 cm). There were no deaths or com- Postoperative esophageal leak is a serious
plications. One patient was converted to complication that can arise because the mucosa
thoracotomy for a large horseshoe-shaped mass is perforated during enucleation and inade-
that was biopsied preoperatively. Bardini and quately repaired. The use of intra-operative en-
Asolati9 reported on five patients who were also doscopy with air insuflation is an important step
successfully enucleated through a thoracoscopic to safeguard against this complication. Seremetis
approach. The only postoperative complication et al.29 reported no postoperative esophageal
was the development of a pseudodiverticulum leaks in open enucleations in an analysis of 838
that was resected with a thoracotomy one year cases. In review of the thoracoscopic literature,
later. This patient did not have a myotomy clo- one case of a recognized and repaired intraoper-
sure. Bonavina and colleagues18 reported success- ative esophageal perforation was recorded but
ful enucleation in six of eight patients that un- there are no postoperative esophageal leaks.
derwent a right VATS approach. A formal There is no reported case of a leiomyoma recur-
thoracotomy was performed in one patient due to rence in both the open and VATS literature.
the inability to exclude the lung and a mucosal Gastroesophageal reflux can occur after enu-
tear in the second patient. They also reported a cleation of leiomyomas near the GEJ.32 This is
patient with a pseudodiverticulum in whom the probably the result of a disturbance of the esoph-
muscle layer was not re-approximated at the time ageal motility or lower esophageal sphincter
of enucleation requiring repair through a thora- mechanism. An anti-reflux procedure can be
cotomy eight months later. The length of hospital added at the time of enucleation if the lower
stay was significantly reduced when comparing esophageal sphincter mechanism is disturbed
VATS with thoracotomy (6.8 days versus 10.2 during the operation. There is no evidence to
42 Samphire, Nafteux, and Luketich

support or refute the need of a fundoplication Conclusion


procedure in esophageal leiomyomas of the GEJ.
A minimally invasive approach to benign tumors
The most common complication reported in
of the esophagus as compared to open thoracot-
the VATS literature is the development of a
omy or laparotomy has many advantages. Video-
pseudodiverticulum after enucleation. In both re- assisted enucleation has been shown in our insti-
ported cases, the myotomy was not closed.9,19 Clo- tution, as well as in others, that the procedure
sure of the myotomy, whenever possible, is rec- can be performed safely with low mortality and
ommended to prevent this complication. morbidity. The VATS approach results in a
shorter hospital stay, decreased need for postop-
erative analgesic and improved cosmesis as com-
Other Tumors pared to open approaches. However, the most
significant advantage of minimally invasive sur-
The most common intramural tumors after
gery is patients’ quick recovery and return to
leiomyomas include granular cell tumors (GCTs)
normal daily activities. A VATS or laparoscopic
and hemangiomas. GCTs are rare and are felt to
approach to the removal of leiomyomas should be
arise from neural cells within the esophageal wall
the treatment of choice in centers experienced in
with electron microscopic features and staining
minimally invasive surgery.
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.
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