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 leiomyomas. 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-abdominal 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 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) 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 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 classification schemes proposed for benign esophageal tumors2,4-7 but in surgical practice, the most useful is that of Avezano et al8, who divided these neoplasms into mucosal–intraluminal and extraluminal–intramural. An endoscopic approach is preferable for removal of mucosal–intraluminal lesions. A transthoracic approach, either by thoracotomy or video-assisted thoracoscopic surFrom the Division of Thoracic and Foregut Surgery, UPMC Presbyterian, Pittsburgh, PA, Philippe Nafteux, MD and Department of Thoracic Surgery, UZ Gasthuisberg, 49 Herestraat, Leuven, Belgium. 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
gery (VATS), is required for extraluminal–intramural 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 discovered as incidental endoscopic or radiological findings. The most common presenting symptoms are dysphagia, regurgitation, and retrosternal discomfort, but patients can present with gastrointestinal 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 tumor. 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 angiography 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 Sauerbruch.16 Since the first report by Everitt et al in 199217 of a thoracoscopic resection of an esophageal leiomyoma, there has been an increased interest in this minimally invasive technique. Both laparoscopy and VATS for benign esophageal tumors 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 exclude malignancy. The management of asymptomatic patients is more controversial. The need for operative intervention should be based on the likelihood of symptom development and malignant degeneration. Some surgeons advocate removal of all leiomyomas regardless of size19 whereas others use a size criterion for surgical intervention. Several size criteria have been proposed as the minimal 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 tumors 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 likelihood of being malignant.24 Based on their endoscopic ultrasonographic experience, Tio and colleagues13 proposed that intramural tumors with a diameter of less than 4 cm without evidence of bleeding, obstruction or malignancy at esophagoscopy 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 malignant myogenic tumors. They are 1) tumor diameter of 3 cm or more, 2) nodular shape, 3) ulceration 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 intraluminal pedunculated neoplasms that are not amenable 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 reserve or comorbid conditions that significantly impair their ability to tolerate general anesthesia form the only contraindication for minimally invasive 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 minimally invasive approach is dependent on the degree of adhesions and the surgeon’s experience with these techniques. In the case of a distal esophageal leiomyoma, a contralateral VATS approach may be used to avoid dense adhesions.
Technique Leiomyomas are usually solitary well-encapsulated intramural lesions that can be easily enucleated without requiring esophageal resection. The approach is dependent on the tumor location. 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
37
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 rightsided 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 draping 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
midaxillary line. Cautery should be used to dissect 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 scapular tip. For distal third tumors, a single retracting 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 exposure of the distal esophagus. A fan retractor is used to retract the lung anteriorly and superiorly as the ultrasonic coagulating 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 esophagus.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 integrity. 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 myotomy is then re-approximated with interrupted 2-0 surgidac (USSC) (Fig 4). A 28-chest tube is inserted through the camera port for post-operative 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 rightsided approach. The patients routinely undergo a barium swallow 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 adequate exposure of the mass using the ultrasonic shears. For left-sided tumors, a circumferential dissection is needed in order to rotate the esophagus 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 esophageal muscularis propria is divided with electrocautery or ultrasonic shears to expose the esophageal 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 surgeons have used a hydrostatic balloon-dilator, in-
Figure 3. Enucleation of leiomyoma with blunt dissection.
PLEASE SUPPLY WORDING
39
Steep reverse trendelenburg positioning facilitates exposure. The distal esophagus is mobilized by dissection 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 reflected to the patient’s right side, preserving both anterior and posterior vagal truncks. The enucleation 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 gastroesophageal 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 established 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 retracted upward to expose the esophageal hiatus using a diamond flex retractor (Genzyme, Tucker, GA) and held in place with a self-retaining system (Mediflex; Welmed Inc, Wexford, PA).
Figure 5. Trocar position on abdomen for laparoscopic approach.
40
Samphire, Nafteux, and Luketich
are closed using musculofascial and intracuticular sutures.
Esophageal Resection An esophageal resection is rarely needed in the treatment of leiomyomas. Seremetis et al29 reported an esophagectomy rate of 10% and more recently Bonavina et al18 reported a 4.5% rate of esophagectomy in 66 patients. The surgical indications for esophagectomy include: 1) a very large or annular leiomyoma that cannot be enucleated by a VATS or open technique, 2) esophageal 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 suspected 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 circumferentially around the esophagus is used to facilitate dissection and special care is taken to avoid injury to the membranous part of the airways and the proximal vagus nerves. Generous application of hemoclips is used during the posterior esophageal dissection to avoid chyle leaks from the thoracic duct. The phrenoesophageal ligament is left intact to avoid loss of the pneumoperitoneum during laparoscopy. The mediastinal pleura is left intact cranial to the azygos vein to help the gastric pullup maintain a mediastinal 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 abdominal 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 mobilized 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 gastric tube of approximately 5 cm in diameter using multiple firings of Endo GIA stapler. An additional 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 esophagogastric specimen is pulled up through the neck as the assistant watches from the abdomen and insures smooth passage and correct orientation of the gastric tube. After the specimen has been removed, a standard hand-sewn or stapled anastomosis is performed with a nasogastric tube inserted 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 esophagus and gastroesophageal junction (GEJ) that were resected between December 1995 and August 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 presenting 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
41
Table 1. Minimally Invasive Resection of Leiomyomas of the Esophagus Authors
Year
Patients
Complications
Bonavina18 Izumi30 Bardini9 Roviaro19 Luketich40
1995 1996 1997 1998 2002
6 3 5 7 9
Pseudodiverticulum (1) None Pseudodiverticulum (1) None None
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 mucosal 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 recurrence in all patients at a mean follow-up of 10 months (range 1-34 months) and there was complete 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 enucleation using 3 ports and a small utility thoracotomy (4-5 cm). There were no deaths or complications. 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 closure. Bonavina and colleagues18 reported successful enucleation in six of eight patients that underwent 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 thoracotomy eight months later. The length of hospital stay was significantly reduced when comparing VATS with thoracotomy (6.8 days versus 10.2
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 enucleation. 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 esophagectomy 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 reported deaths in patients treated with a minimally invasive enucleation. Postoperative esophageal leak is a serious complication that can arise because the mucosa is perforated during enucleation and inadequately repaired. The use of intra-operative endoscopy 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 intraoperative esophageal perforation was recorded but there are no postoperative esophageal leaks. There is no reported case of a leiomyoma recurrence in both the open and VATS literature. Gastroesophageal reflux can occur after enucleation of leiomyomas near the GEJ.32 This is probably the result of a disturbance of the esophageal 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 reported cases, the myotomy was not closed.9,19 Closure of the myotomy, whenever possible, is recommended 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 submucosa 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 authors 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 Symptomatic tumors and tumors demonstrating rapid growth should be removed. Historically, transthoracic resection has been the treatment of choice. There are no reported cases of VATS resection, however, the minimally invasive approach 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 hemangiomas are located in the middle esophagus.36 The symptoms are similar to other benign tumors although bleeding can be massive in case of tumor rupture. Hemangiomas have been treated with endoscopic resection,37 sclerotherapy,38 radiation therapy, and open thoracotomy. Minimally invasive surgery could certainly be used for resections of hemangiomas. There is one reported case of video-thoracoscopic resection by Ramo et al.39 An endoscopic stapler was fired under direct endoscopic visualization to control mucosal continuity and prevent stenotic complication.
Conclusion A minimally invasive approach to benign tumors of the esophagus as compared to open thoracotomy or laparotomy has many advantages. Videoassisted enucleation has been shown in our institution, 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 postoperative analgesic and improved cosmesis as compared to open approaches. However, the most significant advantage of minimally invasive surgery 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.
References 1. Plachta A: Benign tumors of the esophagus. Am J Gastroenterol 38:639-652, 1962 2. Moersch HJ, Harrington SW: Benign tumor of the esophagus. Ann Otol Rhino Laryngol 53:800-817, 1944 3. Scmidt HW, Clagett OT, Harrison EG: Benign tumors and cysts of the esophagus. J Thorac Cardiovasc Surg 41:717-723, 1961 4. Sweet RH, Soutter L, Valenzuela CT: Muscle wall tumors of the esophagus. J Thorac Surg 27:13-31, 1954 5. Nemir P, Wallace HW, Fallahnejad M: Diagnosis and surgical management of benign disease of the esophagus. Curr Probl Surg 13:1-74, 1976 6. Reed CE: Benign tumors of the esophagus. Chest Surg Clin North Am 4:769-783, 1994 7. Herrera JL: Benign and metastatic tumors of the esophagus. Gastroenterol Clin North Am 20:775-789, 1991 8. Avezzano EA, Fleischer DE, Merida MM, et al: Giant fibropolyps of the esophagus. Am J Gastroenterol 85:299302, 1990 9. Bardini R, Asolati M: Thoracoscopic resection of benign tumors of the esophagus. Int Surg 82:5-6, 1997 10. Peracchia A, Rosati R, Bardini R: Thoracoscopic removal of tumors of the esophagus, in Gossot D, Hunter JG, and Toouli J (eds), Endosurgery. Edinburgh, Churchill Livingstone, 1996, pp 267-273 11. Gossot D, Fourquier P, Meteini ME, et al: Technical aspects of endoscopic removal of benign tumors of the esophagus. Surg Endosc 7:102-103, 1993 12. Little AG: Esophageal leiomyoma, diverticulum and duplication cysts, in Yim APC, Hazelrigg SR, Izzat MB, Landreneau RJ, Mack MJ, Naunheim KS, and Ferguson TB (eds), Minimal Access Cardiothoracic Surgery. Philadelphia, PA, W.B. Saunders, 2000, pp 261-265 13. Tio TL, Tyt GNJ, den Hartog Jager FCA: Endoscopic ultrasonography for the evaluation of smooth muscle tumors in the upper gastrointestinal tract: An experience with 42 cases. Gastrointes Endosc 36:342-350, 1990
PLEASE SUPPLY WORDING
14. Palchick BA, Alpert MA, Holmes RA, et al: Esophageal hemangioma: Diagnosis with computed tomography and radionuclide angiography. S Med J 76:1582-1584, 1983 15. Ohsawa T: Surgery of the esophagus. Arch F Jap Chir 10:605-695, 1933 16. Sauerbruch F: Presentations in the field of thoracic surgery. Arch F Klin Chir 173:457-463, 1932 17. Everitt NJ, Glinatsis M, McMahon MJ: Thoracoscopic enucleation of leiomyoma of the esophagus. Br J Surg 79:643, 1992 18. Bonavina L, Segalin A, Rosati R, et al: Surgical therapy of esophageal leiomyoma. J Am Coll Surg 181:527-262, 1995 19. Roviaro GC, Maciocco M, Varoli F, et al: Videothoracoscopic treatment of esophageal leiomyoma. Thorax 53: 190-192, 1998 20. Yamada Y, Kida M, Sakaguchi T: A study on myogenic tumors of the upper gastrointestinal tract by endoscopic ultrasonography-with special reference to the differential diagnosis of benign and malignant lesions. Dig Endosc 4:396-408, 1992 21. Glanz I, Grunebaum M: The radiological approach to leiomyoma of the esophagus with a long term follow up. Clin Radiol 28:197-200, 1977 22. Biasini A: Su di un caso di fibroleiomyoma dell’esofago ipobronchiale in transformazione maligna asportazione per via transpleurodiaframmatica ed esofago-gastrostomia guarigione. Pathologica 41:260-267, 1949 23. Calmenson M, Claggett OT: Surgical removal of leiomyomas of the esophagus. Am J Surg 72:745-747, 1946 24. Shamji F, Todd TRJ: Benign tumors, in Pearson FG, Cooper JD, Deslauriers J, Ginsberg RJ, Hiebert CA, Patterson GA, and Urschel Jr. HC (eds), Esophageal Surgery. Philadelphia, PA, Churchill Livingstone, 2002, pp 637-654 25. Smith GS, Isaacson MB, Dempsey GLF: Laparoscopic excision of esophageal leiomyoma through an anterior esophagotomy. Dis Esophagus 14:278-279, 2001 26. Infante M, Maurizio MD, Alloisio M, et al: Thoracoscopic resection of an esophageal stromal tumor through the left pleural cavity. Surg Laparosc Endosc 11:273-276, 2001 27. Taniguchi E, Kamiike W, Iwase K, et al: Thoracoscopic enucleation of a large leiomyoma located on the left side of the esophageal wall. Surg Endosc 11:280-282, 1997
43
28. Mafune K, Tanaka Y: Thoracoscopic enucleation of an esophageal leiomyoma with balloon-dilator assistance. Surg Today 27:189-192, 1997 29. Seremetis MG, Lyons WS, De Guzman VC, et al: Leiomyomata of the esophagus: An analysis of 838 cases. Cancer 38:2166-2177, 1976 30. Izumi Y, Inoue H, Endo M: Combined endoluminal-intracavitary thoracoscopic enucleation of leiomyoma of the esophagus. Surg Endosc 10:457-458, 1996 31. Rendina EA, Venuta F, Pescarmona ED, et al: Leiomyoma of the esophagus. Scand J Thorac Cardiovasc Surg 24:79-82, 1990 32. Ala-Kulju K, Salo A: Smooth muscle tumours of oesophagus. Scand J Thorac Cardiovasc Surg 21:65-68,1987 33. Postlethwait RW, Lowe JE: Benign tumors and cysts of the esophagus, in Shakelford RT, Zuidema GD, and Orringer MB (eds), Shackelford’s Surgery of the Alimentary Tract, Vol. I. Philadelphia, PA, W.B. Saunders, 1996, pp 369-386 34. Coutinho DS de S, Soga J, Yoshikawa T, et al: Granular cell tumors of the esophagus: A report of two cases and a review of the literature. Am J Gastroenterol 80:758-762, 1985 35. Giacobbe A, Faciorusso D, Conoscitore P, et al: Granular cell tumor of the esophagus. Am J Gastroenterol 83:13981400, 1998 36. Govoni AF: Hemangioma of the esophagus. Gastrointest Radiol 7:113-117, 1982 37. Yoshikane H, Suzuki T, Yoshioka N, et al: Hemangioma of the esophagus: Endosographic imaging and endoscopic resection. Endoscopy 27:267-269, 1995 38. Aoki T, Okagawa K, Uemura Y, et al: Successful treatment of an esophageal hemangioma by endoscopic injection sclerotherapy: Report of a case. Surg Today 27:450452, 1997 39. Ramo OJ, Salo JA, Baradini R, et al: Treatment of a submucosal hemangioma of the esophagus using simultaneous video-assisted thoracoscopy and esophagoscopy: Description of a new minimally invasive technique. Endoscopy 29:S27, 1997 40. Luketich JD, Perry Y, Samphire J, et al: Minimally invasive surgical treatment of esophago-gastric leiomyomas: A single institution experience. Presented Pennsylvania Association of Thoracic Surgery, Miami, FL, October 1620, 2002.