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Ann Thorac Surg 2005;80:1196-1201
© 2005 The Society of Thoracic Surgeons

Original article: General thoracic

Laparoscopic Transhiatal Subtotal Esophagectomy for the Treatment of Advanced Megaesophagus

Eduardo Crema, PhD, MD * , Lara B.P. Ribeiro, Juverson A. Terra, Jr, Alex A. Silva, MD

Department of Digestive Surgery, Federal School of Medicine, Uberaba, Minas Gerais, Brazil

Accepted for publication October 26, 2004.

* Address reprint requests to Dr Crema, Rua Marcos Lombardi, 305, 38050-170, Uberaba, Minas Gerais, Brasil (Email: eduardocremafmtm{at}mednet.com.br).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
BACKGROUND: Chagas' disease affects about 5 to 8 million individuals in Brazil, with 5% to 8% of them developing megaesophagus. In view of the transformation of the esophagus into an inert tube unable to propel food to the stomach, and in order to prevent complications, the elected treatment for advanced megaesophagus is subtotal esophagectomy. We evaluate here the outcome of laparoscopic transhiatal subtotal esophagectomy in the treatment of advanced megaesophagus.

METHODS: Thirty patients with advanced esophagopathy, 26 with chagasic and 4 with idiopathic megaesophagus, were submitted to transhiatal subtotal esophagectomy without thoracotomy through laparoscopy and left cervicotomy. Contrast exams of the esophagus, stomach, and duodenum (ESD), upper digestive tract endoscopy (UDE), esophageal electromanometry, and 24-hour pHmetry were performed during the preoperative and postoperative period. With respect to the surgical technique, pyloroplasty was not performed. The cervical esophagus was dissected through a left cervicotomy and the esophagogastric anastomosis was performed between the cervical segment of the esophagus and the posterior wall of the stomach.

RESULTS: No death or conversion to open surgery occurred in the present series. Complications were observed in 8 patients (26.7%): 6 cases of pneumothorax (20%), 2 of cervical fistulas (6.7%), 7 of transient dysphonia (23.3%), and 1 of anastomotic esophagogastric stenosis (3.3%). One (3.3%) of the patients developed dysphagia for solid food after 36 months despite normal ESD, UDE, electromanometry, and 24-hour pHmetry.

CONCLUSIONS: The present results show that laparoscopic transhiatal subtotal esophagectomy is a feasible and safe procedure with an excellent postoperative outcome.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
In Latin America, at least 90 million (25%) individuals of an estimated population of 360 million are at risk of contracting Chagas' disease and 16 to 18 million are definitely infected with Trypanosoma cruzi (T cruzi) (World Health Organization, 1991), the etiological agent of this disease. The incidence of human T cruzi infection in Brazil was 0.04% in 1999 (World Health Organization, 1999). In Brazil, Chagas' disease is endemic and affects 5 to 8 million individuals [1, 2], with a higher incidence in the center-south region, mainly affecting a population between the second and fourth decades of life [3]. The most common digestive manifestation of this disorder is megaesophagus, with an estimated 5% to 8% of patients with Chagas' disease developing this manifestation [4].

Esophagectomy has a solid physiopathological basis. The advanced form of megaesophagus is characterized by dilatation with an increase in the organ (dolichomegaesophagus), aperistalsis associated with tertiary contractions, an amplitude of contraction of the esophageal body lower than 20 mm Hg [5], and incomplete or no opening of the lower sphincter [6]. Because of these findings, the resolution of dysphagia, the main objective of treatment, is impaired when performing any procedure in the esophagogastric transition. In addition, a larger number of parasites in the esophageal tissue has been observed for the advanced form of chagasic esophagopathy [7], and these patients show a decline in CD4 and circulating T lymphocytes compared to those with the nonadvanced form of chagasic megaesophagus [8].

Another unquestionable reason for the resection of this inert pouch is that emptying of the dilated esophagus continues to be incomplete after surgical procedures (Heller, Thal, and Merendino) performed above the esophagogastric transition and, consequently, the risk of bronchoaspiration of stasis fluid rich in gram-negative bacteria and fungi continues to be present [9]. In addition, the possibility exists of an association with concomitant neoplasia, which has been observed in megaesophagus at rates ranging from 3.2% to 9.28% in most studies [10–13], with Loviscek and colleagues [12] reporting an 18.92% prevalence of neoplasia in advanced megaesophagus. Furthermore, Brücher and colleagues [11] observed that the risk of developing esophageal cancer was about 140 times higher in patients with achalasia than in the general population.

Therefore, the only surgical procedure that theoretically would cure advanced megaesophagus is subtotal esophagectomy. Using this procedure, the thoracic and abdominal esophagus is resected while its cervical segment is preserved. Since the myenteric plexuses destroyed by the parasite are almost nonexistent in this segment, this region is not affected by the disease [14], with no decrease in the number of myenteric plexuses and/or their replacement with fibrous tissue, pathognomonic findings of chagasic esophagus, being observed in this segment [15].

Analysis of six publications, reporting a total of 348 patients submitted to subtotal esophagectomy by laparotomy and cervicotomy without thoracotomy for the treatment of benign diseases, showed that mortality was reduced, 3.7% (0% to 12.5%), perioperative and postoperative complications were acceptable, 45.5% (18.3% to 81.3%), and postoperative outcomes were excellent (96.4%) [3, 16–20]. Even better results were obtained when evaluating nine series of laparoscopic transhiatal subtotal esophagectomy with or without thoracoscopy. In these publications analyzing 429 patients (294 with malignant diseases and 135 with benign diseases), the mortality rate was 0.6% (0% to 3.6%) and the frequency of complications was 32.8% (0% to 53.6%) [21–29].

The objective of the present study was to evaluate the outcome of treatment of 30 patients with advanced megaesophagus submitted to transhiatal subtotal esophagectomy without thoracotomy and/or thoracoscopy performed through the laparoscopic route and left cervicotomy.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
Study Population
Thirty patients, 19 men and 11 women, with a mean age of 47.46 (27 to 65) years, were submitted to treatment of the advanced form of megaesophagus at the Department of Surgery, Federal School of Medicine, Uberaba, Brazil, between September 1996 and December 2002. The mean duration of surgical procedure was 255 (190 to 325) minutes, and all procedures were performed by the same team, with the responsible surgeon being one of the authors of the present study (EC). Thirteen (43.3%) of the 30 patients had been submitted to Heller cardiomyotomy 8 to 20 years before the study. All patients received information about the surgical procedure to be performed and the protocol was approved by the Medical Ethics Committee on Human Research of the Federal School of Medicine, Uberaba, Brazil.

During the preoperative period, all patients were submitted to T cruzi serology, contrast exams of the esophagus, stomach, and duodenum (ESD) (Fig 1), upper digestive tract endoscopy (UDE), electromanometry of the esophagus, 24-hour pHmetry, ultrasonography of the bladder and biliary tract to exclude the presence of cholelithiasis, which is associated with chagasic esophagopathy in 8.45% of cases [30], and pulmonary physiotherapeutic preparation for at least 7 days.



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  		Fig 1. Esophagogram of a patient before resection (advanced megaesophagus).

 
All patients were submitted to nutritional assessment before operation and once a week until discharge, which consisted of the determination of anthropometric (weight, height, arm muscle circumference, skinfold thickness, and creatinine-to-height ratio), biochemical (total protein, albumin, and transferrin), and immunologic factors (blood lymphocyte count and tuberculin purified protein derivative [PPD] skin test). Nutritional assessment revealed moderate malnutrition in all 30 patients. The patients presented weight loss ranging from 3 to 12 kg (mean of 6.2 kg), a mean body mass index of 21.42 (16.37 to 25.90), and a mean arm muscle circumference of 24.32 cm (19.13 to 28.8) (Table 1). An industrialized and balanced diet was thus administered through the enteral route using a nasoenteral tube positioned in the stomach at the time of endoscopic examination. The patients received 1.5 g/kg weight of diet per day for a mean period of 12 (8 to 23) days.


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  		Table 1. Anthropometric Assessment of the 30 Patients (19 Men and 11 Women)
 
Twenty-six patients had chagasic megaesophagus and four idiopathic megaesophagus. The most frequent clinical manifestations in these patients were long-term severe dysphagia or even impairment of liquid diet ingestion, late and/or passive regurgitation when the patient is in dorsal decubitus, aspirative bronchopneumonia, and malnutrition. In the present study, relapsed megaesophagus and dilated esophagus with a body contraction amplitude lower than 20 mm Hg were considered to represent the advanced form, in addition to dolichomegaesophagus. The idiopathic form was considered in the case of patients with negative T cruzi serology who did not show the characteristic findings of chagasic megaesophagus upon anatomopathological examination of the resected surgical specimen, in addition to a negative polymerase chain reaction for T cruzi in tissue. The surgical technique used was transhiatal subtotal esophagectomy performed by laparoscopy and left cervicotomy.

Surgical Technique
The patients were placed in dorsal decubitus on the operating table with the legs abducted, with the surgeon being positioned between the legs, and an assistant (camera) on the left side of the patient. The monitor, when only one, was positioned on the right and at the head of the operating table. Five entry ports were used; two of 10 mm and three of 5 mm. With respect to the 10-mm ports, one was situated in the midline between the xiphoid appendix and the navel for a 30 degree eyepiece and the other was positioned in the left hemiclavicular line 5 cm from the costal margin (right hand of the surgeon). The 5-mm ports were positioned in the right hemiclavicular line (left hand of the surgeon), 1 cm left from the xiphoid appendix (aspirator) and 5 cm left from the umbilical scar (esophageal separator).

Using a 12 mm Hg pneumoperitoneum (CO2), the procedure was started by ample dissection of the esophagogastric transition, restoring the abdominal esophagus with a Penrose drain or a flexible separator (EndoFlex; Medline, Mundelein, IL). Dissection was continued under direct vision of the esophageal body, with identification of the pleurae and pericardium. Hemostasis was achieved by monopolar cauterization or by UltraCision (Ultracision Inc, Smithfield, RI) and/or clipping of the esophageal branches until the cervical region. The surgical dissection plane was close to the esophagus, thus avoiding damage to the pleurae and mediastinal structures. To obtain better access to the mediastinum during dissection of the thoracic esophagus, we routinely perform a median transection of the diaphragm and place the operating table in the Trendelenburg position.

After dissection of the abdominal and thoracic esophagus was completed, the stomach was prepared with release of the greater curvature. Monopolar electrocauterization (22 patients) and UltraCision (8 patients) was used for sectioning of the short gastric vessels and gastrocolic omentum. The gastroepiploic and left gastric vessels were ligated by double clipping with preservation of the arch of the greater and lesser curvature. No pyloroplasty was performed during surgical treatment of advanced megaesophagus. After preparation of the stomach, the cervical esophagus was dissected through a left cervicotomy. Due to the delicate traction of the surgical specimen, the esophagus and proximal part of the stomach in the cervical region were exteriorized and the esophagogastric transition was sectioned with a cutting linear stapler with a 75-mm green load. The passage of the esophagus and stomach was monitored during cervical traction of the esophagus under direct vision using an eyepiece positioned in the inferior mediastinum.

An esophagogastric anastomosis was performed with manual continuous 3.0 monofilament sutures on a single plane between the posterior wall of the gastric fundus and a segment of the cervical esophagus, whose extension was approximately 4 cm, so that the esophagogastric anastomosis would remain in the cervical region. No cervical or abdominal drainage was used.

During surgery, a nasoenteral tube was placed in the duodenum (10 patients) or gastric antrum (20 patients) for enteral nutritional support. The enteral diet was started on the second postoperative day and was maintained until the 10th day (28 patients), when an oral diet was administered after radiologic confirmation of the absence of fistulas and good passage of contrast dye through the anastomosis.

A chest roentgenogram was obtained from all patients at the end of surgery in the operating room. In addition, all patients were submitted to ESD (Fig 2) and UDE 3 months after surgery.



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  		Fig 2. Esophagogram of a patient after resection.

 
To analyze gastroesophageal reflux and esophagitis in the esophageal stump, 16 patients were later (3 to 60 months) submitted to ESD with a biopsy, esophagogastric manometry, and 24-hour pHmetry of the esophageal stump, with the sensor placed 2 cm above the esophagogastric anastomosis, with its precise position being determined at the time of endoscopic examination.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
No death or conversion to open surgery occurred in this series. None of the patients required ventilatory assistance during the postoperative period, with all patients being extubated in the operating room and sent to the ward. Only two patients (6.7%), who had previously been submitted to Heller cardiomyotomy, required transfusion of two units of concentrated red blood cells during or after surgery.

The following complications were detected in 8 patients (26.7%), with one patient presenting more than one complication: 6 cases of pneumothorax (20%), 2 cases of cervical fistulas (6.7%), and 7 cases of transient dysphonia (23.3%). The 6 patients with pneumothorax were submitted to chest drainage during the immediate postoperative period. Clinical resolution of the cervical fistulas in the 2 patients was achieved by drainage of the cervical region, clinical treatment, and enteral nutritional support. One (3.3%) of the patients who developed a cervical fistula after 2 months showed stenosis in the cervical anastomosis (3.3%), with clinical resolution after three dilatations. Among the patients with dysphonia, the condition resolved spontaneously after the first month in 5 and after the third month in the other 2.

Contrast radiologic examination of the esophagus, performed 3 months after surgical procedure, demonstrated good passage of the contrast medium through the anastomosis and good gastric emptying in all cases. Endoscopic examination detected no esophagitis in the esophageal stump in any of the patients and showed an ample anastomosis. A biopsy obtained from 16 patients at least 3 months after surgery did not detect reflux esophagitis. Manometry demonstrated that the anastomosis was located in a positive pressure region (cervical), with the analysis of 16 patients so far revealing a mean pressure of 67.32 mm Hg (45.4 to 111.8 mm Hg), and pHmetry was normal in all 16 patients studied. Despite normal exams (ESD, UDE, electromanometry, and 24-hour pHmetry), one patient developed dysphagia for solid food after 36 months and continues to be under ambulatory observation.


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
The laparoscopic approach has been extensively studied due to its numerous advantages compared to open surgery. In laparoscopic surgeries, incisional trauma is minimized [22, 27], causing fewer painful symptoms [22, 29], a low incidence of complications [22] including less impaired pulmonary function [31], and a lower response to surgical stress induced by hormones [32, 33] and cytokines [34–36]. In addition, patients are discharged early, can rapidly return to their normal activities [22, 29], and their aesthetic appearance is favorable [22]. However, the benefits of laparoscopy in major surgeries such as esophagectomy are still being investigated.

Because advanced megaesophagus is a benign incapacitating disease that affects young individuals, its treatment requires a surgical approach with low morbidity and mortality and a good and long-lasting outcome. Esophagectomy satisfies these conditions and the laparoscopic transhiatal subtotal technique has been shown to be the best approach to the treatment of benign disorders of the esophagus. Laparoscopic transhiatal esophagectomy is considered to provide a better definition and precision of mediastinal dissection, less blood loss, and fewer pleuropulmonary complications [21], and does not require ventilatory assistance during the postoperative period [37]. In the present series, morbidity was low (26.7%), confirming the smaller number of intraoperative and postoperative complications resulting from this technique. Similar results have been reported by others [21, 22].

In contrast to other studies [21–24, 26], no pyloroplasty or pyloromyotomy was performed in the present series because solid and fluid emptying in the stomach of patients with chagasic esophagopathy was independent of the vagal trunks sectioned at the time of surgery. Sader [38] believes that pyloroplasty is imperative to prevent gastric stasis and regurgitation. However, these complications were not diagnosed in any of the present patients. On the other hand, rates of delayed gastric emptying ranging from 7.1% to 25% have been reported by other investigators [23, 26] who performed pyloromyotomy and/or pyloroplasty. In addition, in the present study the entire stomach was used without sectioning of the lesser curvature, in contrast to other authors who adopted the technique of gastric tube formation [23, 25–27, 29]. Swanstrom and Hanson [29] reported that a gastric tube improves the rate of gastric emptying and avoids the need for pyloromyotomy. In addition to being unnecessary, we believe that pyloromyotomy causes reflux from the duodenum to the stomach, which is now in an intrathoracic and negative pressure situation, consequently triggering gastritis and reflux esophagitis.

In the present study, mortality was zero among the 30 patients submitted to laparoscopic transhiatal esophagectomy with cervicotomy and without thoracotomy, a finding also reported by other authors [21, 22, 24, 26–29]. Furthermore, no conversion to open surgery was necessary. In contrast, treating benign and malignant disorders, DePaula and colleagues [21] reported a conversion rate of 8.3% and Luketich and colleagues [25] of 7.2%.

The most common complications observed in the present series were pulmonary ones (20%), which were also the most frequent in the studies of Nguyen and colleagues [27] (17%), Luketich and colleagues [24] (40.2%), and Fernando and colleagues [23] (32.1%), in which laparoscopic esophagectomy was combined with thoracoscopy. Respiratory complications reported in eight publications [21–27, 29] on laparoscopic transhiatal esophagectomy, with or without thoracoscopy, showed a mean incidence of 26.3% (17% to 55.5%). Nguyen and colleagues [27], comparing esophagectomy performed by laparoscopy and thoracoscopy with transhiatal and transthoracic esophagectomy, did not detect a significant difference in the incidence of respiratory complications among the three groups.

In the present study, a high incidence of postoperative transient dysphonia (23.3%) was observed, a result similar to that reported by DePaula and colleagues [21] (25%). In contrast, Swanstrom and Hanson [29] obtained an even higher rate (66.6%), with this complication being the most frequent in their series. Improvement of dysphonia after the third month has been reported in almost all studies. However, Luketich and colleagues [24] observed definitive dysphonia in 2 patients (2.6%), while no dysphonia was reported in the series of Nguyen and colleagues [27].

The mean incidence of transient dysphonia was 23.6% (0% to 66%) in four publications on laparoscopic transhiatal esophagectomy with or without thoracoscopy (n = 116) [21, 24, 27, 29]. Analyzing four publications on open transhiatal esophagectomy (n = 166), a mean of 18.9% (5% to 25%) was found [3, 17–19]. Consequently, the rate of dysphonia is higher when the laparoscopic transhiatal approach is used compared with open surgery. Presumably, the etiologic factor of dysphonia is the dissection by the cervical route of the upper thoracic esophagus and/or removal of a sometimes voluminous (megaesophagus) surgical specimen through this route, provoking a traumatic inflammatory process in the left recurrent nerve.

In the present series, the incidence of cervical fistulas was 6.7% (2 patients), similar to the mean 5.9% (0% to 11.7%) rate reported in the literature [21, 22, 24–29]. Comparison of this incidence of cervical fistulas resulting from laparoscopic esophagectomy with or without thoracoscopy with that resulting from open esophagectomy, which is 20.3% (8.2% to 37.5%) [3, 12, 17–20], shows a significant difference between the two procedures in favor of the laparoscopic approach.

Another complication of cervical esophagogastric anastomosis is stenosis. This complication is more frequent than fistulas and manifests late [39]. In the present study, anastomotic esophagogastric stenosis was observed in 1 patient (3.3%), a rate similar to that reported by Fernando and colleagues [23] (3.6%).

As a late complication, dysphagia for solid food was observed in 1 patient (3.33%), manifesting 36 months after surgery despite radiologic and endoscopic permeability of the anastomosis. Swanstrom and Hanson [29] detected moderate dysphagia in 22.2% of cases after esophagectomy and Fernando and colleagues [23] in 28.6%, while DePaula and colleagues [21] did not observe dysphagia in their patients.

Domene and colleagues [22] believe that the postoperative complications of laparoscopic and thoracoscopic esophagectomy are similar to those resulting from open surgery and do not decrease with the thoracoscopic approach, thus not offering clear advantages over the traditional method. However, we agree with the opinion of other authors that minimally invasive esophagectomy is associated with a lower incidence of postoperative complications [25, 26] and lower mortality compared with the open procedure [16, 20, 27, 28], in addition to a shorter hospital stay [24, 26], faster recovery [27], and early return to normal activities [24, 25, 29].

In the present series, laparoscopic transhiatal esophagectomy showed low morbidity and no mortality. This procedure is technically feasible and safe with an excellent postoperative outcome in center with experience in advanced minimally invasive surgical techniques.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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ANN THORAC SURG ASIAN CARDIOVASC THORAC ANN EUR J CARDIOTHORAC SURG
J THORAC CARDIOVASC SURG ICVTS ALL CTSNet JOURNALS