2005;80:1196-1201 Ann Thorac SurgEduardo Crema, Lara B.P. Ribeiro, Juverson A. Terra, Jr and Alex A. Silva

MegaesophagusLaparoscopic Transhiatal Subtotal Esophagectomy for the Treatment of Advanced

http://ats.ctsnetjournals.org/cgi/content/full/80/4/1196located on the World Wide Web at:

The online version of this article, along with updated information and services, is

Print ISSN: 0003-4975; eISSN: 1552-6259. Southern Thoracic Surgical Association. Copyright © 2005 by The Society of Thoracic Surgeons.

is the official journal of The Society of Thoracic Surgeons and theThe Annals of Thoracic Surgery

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aparoscopic Transhiatal Subtotal Esophagectomyor the Treatment of Advanced Megaesophagusduardo Crema, PhD, MD, Lara B. P. Ribeiro, Juverson A. Terra, Jr, andlex A. Silva, MD

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

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Background. Chagas’ disease affects about 5 to 8 mil-ion individuals in Brazil, with 5% to 8% of them devel-ping megaesophagus. In view of the transformation ofhe esophagus into an inert tube unable to propel food tohe stomach, and in order to prevent complications, thelected treatment for advanced megaesophagus is subto-al esophagectomy. We evaluate here the outcome ofaparoscopic transhiatal subtotal esophagectomy in thereatment of advanced megaesophagus.

Methods. Thirty patients with advanced esophagopa-hy, 26 with chagasic and 4 with idiopathic megaesoph-gus, were submitted to transhiatal subtotal esophagec-omy without thoracotomy through laparoscopy and leftervicotomy. Contrast exams of the esophagus, stomach,nd duodenum (ESD), upper digestive tract endoscopyUDE), esophageal electromanometry, and 24-hourHmetry were performed during the preoperative andostoperative period. With respect to the surgical tech-

ique, pyloroplasty was not performed. The cervical

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2005 by The Society of Thoracic Surgeonsublished by Elsevier Inc

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sophagus was dissected through a left cervicotomy andhe esophagogastric anastomosis was performed betweenhe cervical segment of the esophagus and the posteriorall of the stomach.Results. No death or conversion to open surgery oc-

urred in the present series. Complications were ob-erved in 8 patients (26.7%): 6 cases of pneumothorax20%), 2 of cervical fistulas (6.7%), 7 of transient dyspho-ia (23.3%), and 1 of anastomotic esophagogastric steno-is (3.3%). One (3.3%) of the patients developed dyspha-ia for solid food after 36 months despite normal ESD,DE, electromanometry, and 24-hour pHmetry.Conclusions. The present results show that laparo-

copic transhiatal subtotal esophagectomy is a feasiblend safe procedure with an excellent postoperativeutcome.

(Ann Thorac Surg 2005;80:1196–201)

© 2005 by The Society of Thoracic Surgeons

n Latin America, at least 90 million (25%) individuals ofan estimated population of 360 million are at risk of

ontracting Chagas’ disease and 16 to 18 million areefinitely infected with Trypanosoma cruzi (T cruzi) (Worldealth Organization, 1991), the etiological agent of thisisease. The incidence of human T cruzi infection inrazil was 0.04% in 1999 (World Health Organization,999). In Brazil, Chagas’ disease is endemic and affects 5o 8 million individuals [1, 2], with a higher incidence inhe center-south region, mainly affecting a populationetween the second and fourth decades of life [3]. Theost common digestive manifestation of this disorder isegaesophagus, with an estimated 5% to 8% of patientsith Chagas’ disease developing this manifestation [4].Esophagectomy has a solid physiopathological basis.

he advanced form of megaesophagus is characterizedy dilatation with an increase in the organ (dolicho-egaesophagus), aperistalsis associated with tertiary

ontractions, an amplitude of contraction of the esopha-eal body lower than 20 mm Hg [5], and incomplete or nopening of the lower sphincter [6]. Because of thesendings, the resolution of dysphagia, the main objective

ccepted for publication Oct 26, 2004.

ddress reprint requests to Dr Crema, Rua Marcos Lombardi, 305, 38050-

f treatment, is impaired when performing any proce-ure in the esophagogastric transition. In addition, a

arger number of parasites in the esophageal tissue haseen observed for the advanced form of chagasic esoph-gopathy [7], and these patients show a decline in CD4nd circulating T lymphocytes compared to those withhe nonadvanced form of chagasic megaesophagus [8].

Another unquestionable reason for the resection of thisnert pouch is that emptying of the dilated esophagusontinues to be incomplete after surgical proceduresHeller, Thal, and Merendino) performed above thesophagogastric transition and, consequently, the risk ofronchoaspiration of stasis fluid rich in gram-negativeacteria and fungi continues to be present [9]. In addi-

ion, the possibility exists of an association with concom-tant neoplasia, which has been observed in megaesoph-gus at rates ranging from 3.2% to 9.28% in most studies10–13], with Loviscek and colleagues [12] reporting an8.92% prevalence of neoplasia in advanced megaesoph-gus. Furthermore, Brücher and colleagues [11] observedhat the risk of developing esophageal cancer was about40 times higher in patients with achalasia than in theeneral population.Therefore, the only surgical procedure that theoreti-

ally would cure advanced megaesophagus is subtotal

sophagectomy. Using this procedure, the thoracic and

0003-4975/05/$30.00doi:10.1016/j.athoracsur.2004.10.059

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bdominal esophagus is resected while its cervical seg-ent is preserved. Since the myenteric plexuses de-

troyed by the parasite are almost nonexistent in thisegment, this region is not affected by the disease [14],ith no decrease in the number of myenteric plexuses

nd/or their replacement with fibrous tissue, pathogno-onic findings of chagasic esophagus, being observed in

his segment [15].Analysis of six publications, reporting a total of 348

atients submitted to subtotal esophagectomy by lapa-otomy and cervicotomy without thoracotomy for thereatment of benign diseases, showed that mortality waseduced, 3.7% (0% to 12.5%), perioperative and postop-rative complications were acceptable, 45.5% (18.3% to1.3%), and postoperative outcomes were excellent96.4%) [3, 16–20]. Even better results were obtainedhen evaluating nine series of laparoscopic transhiatal

ubtotal esophagectomy with or without thoracoscopy. Inhese publications analyzing 429 patients (294 with ma-ignant diseases and 135 with benign diseases), the mor-ality rate was 0.6% (0% to 3.6%) and the frequency ofomplications was 32.8% (0% to 53.6%) [21–29].

The objective of the present study was to evaluate theutcome of treatment of 30 patients with advancedegaesophagus submitted to transhiatal subtotal esoph-

gectomy without thoracotomy and/or thoracoscopyerformed through the laparoscopic route and leftervicotomy.

aterial and Methods

tudy Populationhirty patients, 19 men and 11 women, with a mean agef 47.46 (27 to 65) years, were submitted to treatment ofhe advanced form of megaesophagus at the Departmentf Surgery, Federal School of Medicine, Uberaba, Brazil,etween September 1996 and December 2002. The meanuration of surgical procedure was 255 (190 to 325)inutes, and all procedures were performed by the same

eam, with the responsible surgeon being one of theuthors of the present study (EC). Thirteen (43.3%) of the0 patients had been submitted to Heller cardiomyotomy

to 20 years before the study. All patients receivednformation about the surgical procedure to be per-ormed and the protocol was approved by the Medicalthics Committee on Human Research of the Federalchool of Medicine, Uberaba, Brazil.During the preoperative period, all patients were sub-itted to T cruzi serology, contrast exams of the esopha-

us, stomach, and duodenum (ESD) (Fig 1), upper diges-ive tract endoscopy (UDE), electromanometry of thesophagus, 24-hour pHmetry, ultrasonography of theladder and biliary tract to exclude the presence ofholelithiasis, which is associated with chagasic esoph-gopathy in 8.45% of cases [30], and pulmonary physio-herapeutic preparation for at least 7 days.

All patients were submitted to nutritional assessmentefore operation and once a week until discharge, which

onsisted of the determination of anthropometric A

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weight, height, arm muscle circumference, skinfoldhickness, and creatinine-to-height ratio), biochemicaltotal protein, albumin, and transferrin), and immuno-ogic factors (blood lymphocyte count and tuberculinurified protein derivative [PPD] skin test). Nutritionalssessment revealed moderate malnutrition in all 30atients. The patients presented weight loss ranging

rom 3 to 12 kg (mean of 6.2 kg), a mean body mass indexf 21.42 (16.37 to 25.90), and a mean arm muscle circum-erence of 24.32 cm (19.13 to 28.8) (Table 1). An industri-lized and balanced diet was thus administered throughhe enteral route using a nasoenteral tube positioned inhe stomach at the time of endoscopic examination. Theatients received 1.5 g/kg weight of diet per day for aean period of 12 (8 to 23) days.Twenty-six patients had chagasic megaesophagus and

our idiopathic megaesophagus. The most frequent clinical

ig 1. Esophagogram of a patient before resection (advancedegaesophagus).

able 1. Anthropometric Assessment of the 30 Patients (19en and 11 Women)

Median Ranges

ge (years) 47.46 27–65MI 21.42 16.37–25.90MC (cm) 24.32 19.13–28.8

MC � arm muscle circumference; BMI � body mass index.

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1198 CREMA ET AL Ann Thorac SurgLAPAROSCOPIC TRANSHIATAL ESOPHAGECTOMY 2005;80:1196–201

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anifestations in these patients were long-term severeysphagia or even impairment of liquid diet ingestion, latend/or passive regurgitation when the patient is in dorsalecubitus, aspirative bronchopneumonia, and malnutri-

ion. In the present study, relapsed megaesophagus andilated esophagus with a body contraction amplitude lower

han 20 mm Hg were considered to represent the advancedorm, in addition to dolichomegaesophagus. The idiopathicorm was considered in the case of patients with negative Truzi serology who did not show the characteristic find-ngs of chagasic megaesophagus upon anatomopatho-ogical examination of the resected surgical specimen,n addition to a negative polymerase chain reaction for

cruzi in tissue. The surgical technique used wasranshiatal subtotal esophagectomy performed by lapa-oscopy and left cervicotomy.

urgical Techniquehe patients were placed in dorsal decubitus on theperating table with the legs abducted, with the surgeoneing positioned between the legs, and an assistant

camera) on the left side of the patient. The monitor,hen only one, was positioned on the right and at theead of the operating table. Five entry ports were used;

wo of 10 mm and three of 5 mm. With respect to the0-mm ports, one was situated in the midline betweenhe xiphoid appendix and the navel for a 30 degreeyepiece and the other was positioned in the left hemi-lavicular line 5 cm from the costal margin (right hand ofhe surgeon). The 5-mm ports were positioned in theight hemiclavicular line (left hand of the surgeon), 1 cmeft from the xiphoid appendix (aspirator) and 5 cm leftrom the umbilical scar (esophageal separator).

Using a 12 mm Hg pneumoperitoneum (CO2), therocedure was started by ample dissection of the esopha-ogastric transition, restoring the abdominal esophagusith a Penrose drain or a flexible separator (EndoFlex;edline, Mundelein, IL). Dissection was continued un-

er direct vision of the esophageal body, with identifica-ion of the pleurae and pericardium. Hemostasis waschieved by monopolar cauterization or by UltraCisionUltracision Inc, Smithfield, RI) and/or clipping of thesophageal branches until the cervical region. The surgi-al dissection plane was close to the esophagus, thusvoiding damage to the pleurae and mediastinal struc-ures. To obtain better access to the mediastinum duringissection of the thoracic esophagus, we routinely per-

orm a median transection of the diaphragm and placehe operating table in the Trendelenburg position.

After dissection of the abdominal and thoracic esoph-gus was completed, the stomach was prepared withelease of the greater curvature. Monopolar electrocau-erization (22 patients) and UltraCision (8 patients) wassed for sectioning of the short gastric vessels andastrocolic omentum. The gastroepiploic and left gastricessels were ligated by double clipping with preservationf the arch of the greater and lesser curvature. Noyloroplasty was performed during surgical treatment ofdvanced megaesophagus. After preparation of the

tomach, the cervical esophagus was dissected through a m

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eft cervicotomy. Due to the delicate traction of theurgical specimen, the esophagus and proximal part ofhe stomach in the cervical region were exteriorized andhe esophagogastric transition was sectioned with a cuttinginear stapler with a 75-mm green load. The passage of thesophagus and stomach was monitored during cervicalraction of the esophagus under direct vision using anyepiece positioned in the inferior mediastinum.An esophagogastric anastomosis was performed withanual continuous 3.0 monofilament sutures on a single

lane between the posterior wall of the gastric fundusnd a segment of the cervical esophagus, whose exten-ion was approximately 4 cm, so that the esophagogastricnastomosis would remain in the cervical region. Noervical or abdominal drainage was used.

During surgery, a nasoenteral tube was placed in theuodenum (10 patients) or gastric antrum (20 patients)

or enteral nutritional support. The enteral diet wastarted on the second postoperative day and was main-ained until the 10th day (28 patients), when an oral dietas administered after radiologic confirmation of the

bsence of fistulas and good passage of contrast dyehrough the anastomosis.

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

ig 2. Esophagogram of a patient after resection.

onths after surgery.

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To analyze gastroesophageal reflux and esophagitis inhe esophageal stump, 16 patients were later (3 to 60

onths) submitted to ESD with a biopsy, esophagogas-ric manometry, and 24-hour pHmetry of the esophagealtump, with the sensor placed 2 cm above the esophago-astric anastomosis, with its precise position being de-ermined at the time of endoscopic examination.

esults

o death or conversion to open surgery occurred in thiseries. None of the patients required ventilatory assis-ance during the postoperative period, with all patientseing extubated in the operating room and sent to theard. Only two patients (6.7%), who had previously been

ubmitted to Heller cardiomyotomy, required transfu-ion of two units of concentrated red blood cells duringr after surgery.The following complications were detected in 8 pa-

ients (26.7%), with one patient presenting more than oneomplication: 6 cases of pneumothorax (20%), 2 cases ofervical fistulas (6.7%), and 7 cases of transient dysphonia23.3%). The 6 patients with pneumothorax were submit-ed to chest drainage during the immediate postoperativeeriod. Clinical resolution of the cervical fistulas in the 2atients was achieved by drainage of the cervical region,linical treatment, and enteral nutritional support. One3.3%) of the patients who developed a cervical fistulafter 2 months showed stenosis in the cervical anastomo-is (3.3%), with clinical resolution after three dilatations.mong the patients with dysphonia, the condition re-

olved spontaneously after the first month in 5 and afterhe third month in the other 2.

Contrast radiologic examination of the esophagus, per-ormed 3 months after surgical procedure, demonstratedood passage of the contrast medium through the anas-omosis and good gastric emptying in all cases. Endo-copic examination detected no esophagitis in the esoph-geal stump in any of the patients and showed an amplenastomosis. A biopsy obtained from 16 patients at leastmonths after surgery did not detect reflux esophagitis.anometry demonstrated that the anastomosis was lo-

ated in a positive pressure region (cervical), with thenalysis of 16 patients so far revealing a mean pressure of7.32 mm Hg (45.4 to 111.8 mm Hg), and pHmetry wasormal in all 16 patients studied. Despite normal exams

ESD, UDE, electromanometry, and 24-hour pHmetry),ne patient developed dysphagia for solid food after 36onths and continues to be under ambulatory

bservation.

omment

he laparoscopic approach has been extensively studiedue to its numerous advantages compared to open sur-ery. In laparoscopic surgeries, incisional trauma is min-

mized [22, 27], causing fewer painful symptoms [22, 29],low incidence of complications [22] including less

mpaired pulmonary function [31], and a lower response

o surgical stress induced by hormones [32, 33] and e

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ytokines [34–36]. In addition, patients are dischargedarly, can rapidly return to their normal activities [22, 29],nd their aesthetic appearance is favorable [22]. How-ver, the benefits of laparoscopy in major surgeries suchs esophagectomy are still being investigated.Because advanced megaesophagus is a benign inca-

acitating disease that affects young individuals, its treat-ent requires a surgical approach with low morbidity

nd mortality and a good and long-lasting outcome.sophagectomy satisfies these conditions and the lapa-oscopic transhiatal subtotal technique has been showno be the best approach to the treatment of benignisorders of the esophagus. Laparoscopic transhiatalsophagectomy is considered to provide a better defini-ion and precision of mediastinal dissection, less bloodoss, and fewer pleuropulmonary complications [21], andoes not require ventilatory assistance during the post-perative period [37]. In the present series, morbidityas low (26.7%), confirming the smaller number of intra-perative and postoperative complications resulting fromhis technique. Similar results have been reported bythers [21, 22].In contrast to other studies [21–24, 26], no pyloroplasty

r pyloromyotomy was performed in the present seriesecause solid and fluid emptying in the stomach ofatients with chagasic esophagopathy was independentf the vagal trunks sectioned at the time of surgery. Sader38] believes that pyloroplasty is imperative to preventastric stasis and regurgitation. However, these compli-ations were not diagnosed in any of the present patients.n the other hand, rates of delayed gastric emptying

anging from 7.1% to 25% have been reported by othernvestigators [23, 26] who performed pyloromyotomynd/or pyloroplasty. In addition, in the present study thentire stomach was used without sectioning of the lesserurvature, in contrast to other authors who adopted theechnique of gastric tube formation [23, 25–27, 29]. Swan-trom and Hanson [29] reported that a gastric tubemproves the rate of gastric emptying and avoids theeed for pyloromyotomy. In addition to being unneces-ary, we believe that pyloromyotomy causes reflux fromhe duodenum to the stomach, which is now in anntrathoracic and negative pressure situation, conse-uently triggering gastritis and reflux esophagitis.In the present study, mortality was zero among the 30

atients submitted to laparoscopic transhiatal esopha-ectomy with cervicotomy and without thoracotomy, anding also reported by other authors [21, 22, 24, 26–29].urthermore, no conversion to open surgery was neces-ary. In contrast, treating benign and malignant disor-ers, DePaula and colleagues [21] reported a conversionate of 8.3% and Luketich and colleagues [25] of 7.2%.

The most common complications observed in theresent series were pulmonary ones (20%), which werelso the most frequent in the studies of Nguyen andolleagues [27] (17%), Luketich and colleagues [24]40.2%), and Fernando and colleagues [23] (32.1%), inhich laparoscopic esophagectomy was combined with

horacoscopy. Respiratory complications reported in

ight publications [21–27, 29] on laparoscopic transhiatal

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sophagectomy, with or without thoracoscopy, showed aean incidence of 26.3% (17% to 55.5%). Nguyen and

olleagues [27], comparing esophagectomy performed byaparoscopy and thoracoscopy with transhiatal and trans-horacic esophagectomy, did not detect a significantifference in the incidence of respiratory complicationsmong the three groups.In the present study, a high incidence of postoperative

ransient dysphonia (23.3%) was observed, a result sim-lar to that reported by DePaula and colleagues [21]25%). In contrast, Swanstrom and Hanson [29] obtainedn even higher rate (66.6%), with this complication beinghe most frequent in their series. Improvement of dys-honia after the third month has been reported in almostll studies. However, Luketich and colleagues [24] ob-erved definitive dysphonia in 2 patients (2.6%), while noysphonia was reported in the series of Nguyen andolleagues [27].

The mean incidence of transient dysphonia was 23.6%0% to 66%) in four publications on laparoscopic transhi-tal esophagectomy with or without thoracoscopy (n �16) [21, 24, 27, 29]. Analyzing four publications on openranshiatal esophagectomy (n � 166), a mean of 18.9%5% to 25%) was found [3, 17–19]. Consequently, the ratef dysphonia is higher when the laparoscopic transhiatalpproach is used compared with open surgery. Presum-bly, the etiologic factor of dysphonia is the dissection byhe cervical route of the upper thoracic esophagus and/oremoval of a sometimes voluminous (megaesophagus)urgical specimen through this route, provoking a trau-atic inflammatory process in the left recurrent nerve.In the present series, the incidence of cervical fistulasas 6.7% (2 patients), similar to the mean 5.9% (0% to

1.7%) rate reported in the literature [21, 22, 24–29].omparison of this incidence of cervical fistulas resulting

rom laparoscopic esophagectomy with or without thora-oscopy with that resulting from open esophagectomy,hich is 20.3% (8.2% to 37.5%) [3, 12, 17–20], shows a

ignificant difference between the two procedures inavor of the laparoscopic approach.

Another complication of cervical esophagogastricnastomosis is stenosis. This complication is more fre-uent than fistulas and manifests late [39]. In the presenttudy, anastomotic esophagogastric stenosis was ob-erved in 1 patient (3.3%), a rate similar to that reportedy Fernando and colleagues [23] (3.6%).As a late complication, dysphagia for solid food was

bserved in 1 patient (3.33%), manifesting 36 monthsfter surgery despite radiologic and endoscopic perme-bility of the anastomosis. Swanstrom and Hanson [29]etected moderate dysphagia in 22.2% of cases aftersophagectomy and Fernando and colleagues [23] in8.6%, while DePaula and colleagues [21] did not observeysphagia in their patients.Domene and colleagues [22] believe that the postoper-

tive complications of laparoscopic and thoracoscopicsophagectomy are similar to those resulting from openurgery and do not decrease with the thoracoscopicpproach, thus not offering clear advantages over the

raditional method. However, we agree with the opinion

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f other authors that minimally invasive esophagectomys associated with a lower incidence of postoperativeomplications [25, 26] and lower mortality compared withhe open procedure [16, 20, 27, 28], in addition to a shorterospital stay [24, 26], faster recovery [27], and early return

o normal activities [24, 25, 29].In the present series, laparoscopic transhiatal esopha-

ectomy showed low morbidity and no mortality. Thisrocedure is technically feasible and safe with an excel-

ent postoperative outcome in center with experience indvanced minimally invasive surgical techniques.

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2005;80:1196-1201 Ann Thorac SurgEduardo Crema, Lara B.P. Ribeiro, Juverson A. Terra, Jr and Alex A. Silva

MegaesophagusLaparoscopic Transhiatal Subtotal Esophagectomy for the Treatment of Advanced

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