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Endothoracic endoesophageal pull-through operation
J
THORAC CARDIOVASC SURG
1991;102:43-50
Endothoracic endoesophageal pull-through operation A new approach to cancers of the esophagus and proximal stomach Many thoracic surgeons have expressed concern about the complications inherent in transhiataI esophagectomy without thoracotomy. The technique of endothoracic endoesophageal pull-through uses a mucosal coring of normal esophagus beyond the tumor and leaves a muscular tube through which the substitute organ is passed. Mediastinal hemorrhage, tracheal injury, and chylothorax are eliminated.
Farrokh Saidi, MD, FACS, FRCS (by.invitation), Azizollah Abbassi, MD (by invitation), M. Behgam Shadmehr, MD (by invitation), and Gholamreza Khoshnevis-Asl, MD (by invitation), Tehran, Iran Sponsored by Clement A. Hiebert, Portland, Maine
firing esophagectomy for cancer the surgeon may justifiably extend the scope of resection with the idea of achieving possible cure. In the reconstructive phase of the operation, however, reduction of surgical trauma must remain the primary consideration. The revival of transhiatal esophagectomy without thoracotomy is based on the assumptions that avoiding thoracotomy results in lessened cardiopulmonary morbidity and that placing the anastomosis in the neck eliminates the mortality attending leakage from an intrathoracic anastomosis. I A further technical refinement in lowering operative trauma is now proposed, based on the simple maneuver of gently coring out the normal mucosal layer of the esophagus adjacent to a carcinoma rather than forcefully extracting the whole organ from within the mediastinum. This proposed extrathoracic endoesophageal approach is an essentially bloodless procedure in which the stripped mucosal layer is removed in continuity with the neoplastic specimen, the mediastinal structures protected in the blunt dissection, and the residual esophageal muscular tube used as the conduit through which stomach or colon
From the Departments of Thoracic and General Surgery, Modarress Hospital, School of Medicine, Beheshti University of Medical Sciences, Tehran, Iran. Supported by The Specialty Research Council of Beheshti University of Medical Sciences, Grant P/25/3/1468. Read at the Seventieth Annual Meeting of The American Association for Thoracic Surgery, Toronto, Ontario, Canada, May 7-9,1990. Address for reprints: Farrokh Saidi, MD, FACS, FRCS, Park Ave., Seventh St., No.3, Tehran, Iran 15137.
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is drawn to the neck for a primary cervical anastomosis. No restriction is placed on the actual extent of planned tumor resection.
Patients and methods Clinical material. BetweenOctober 1986and October 1989, 68 unselectedpatients with cancers of the esophagus and proximal stomach were operated on consecutively by the attending and resident surgical staff, Modarress Hospital, Beheshti University of Medical Sciences, Tehran, Iran. The majority of patientscame from the northern provinces of the country where esophagealcancer is particularly prevalent.2 The typical history included difficulty in swallowing solids or liquids, or both, with ensuing weight loss. The diagnosis was established in all cases by barium esophagogram and endoscopic tumor biopsy. No other staging was performed. Although emaciation was often severe,no patient was judged unable to tolerate the procedure,and onlythree received preoperativehyperalimentation. The primary goal for all patients was to reestablish the ability to swallow. In perhaps fivecases only did the surgeon believea curative resection had been achieved. Postoperative staging revealed the tumor of 18 patients in TNM stage II (26.4%),45 patients in stage III (66.2%), and 5 patients in stage IV (7.4%).3 Technique. The operative approach has been modifiedfrom that used in the original pilot series.t It is now adjusted for the level of esophagealor proximalgastric tumor location.The procedure has been called an endothoracic endoesophageal pullthrough operation (EEPT). Thus the 68 patients are dividedinto four groups: EEPT I for cancers of the cardia and loweresophagus, EEPT II for cancers of the middle esophagus, EEPT III for cancers of the cervicalesophagus,and EEPT IV for cancers of the proximal stomach (Fig. 1). An abdominal and a cervical incision are performed in all patients (Fig. 2). Patients with middle esophageal cancers also require a thoracotomy. The order in which the incisions are performed varies with the location of the tumor. The colon is
43
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44 Saidi et al.
" EEPT I
"
Number of
Thoracotomy
Esophageal
Patients
~equired
Substitute
3 1
1 9
1 4
NO
YES
Stomach
Stomach
NO
Stomach
NO
Colon
Fig. I. Sketches illustrating the definitions of the four types of EEPT with patient numbers and strategy of surgical management.
routinely prepared preoperatively in case the stomach is not suitable for replacement. Laparotomy. The abdomen is opened for (I) resection of tumors of the lower esophagus, the cardia, or proximal stomach followed by mobilization of either a gastric tube or colon segment for the pull-through or (2) mobilization of the whole stomach or colon segment as the replacement organ in patients with cancers of the cervical and middle thoracic esophagus. For middle esophageal cancers the laparotomy may either precede or follow thoracotomy for mobilization and resection of the cancer. The operative approach to cancers of the lower esophagus and cardia ma y be curative or pallia tive in concept, depending on the extent of tumor. Thus splenectomy and regional lymph node removal are optional. The Kocher maneuver is mandatory. Pyloroplasty is preferred to either pyloromyotomy or dilation of the pyloric muscle. The decision of whether stomach will reach to the neck after tumor resection can be made with reasonable confidence. Frozen section pathologic study of this distal resection margin must be negative for malignant cells. If not, total gastrectomy followed by mobilization of the left hemicolon as an esophageal substitute may be more prudent. For these distal tumors the operative approach is the standard transhiatal dissection: detachment of the left hepatic lobe, enlargement of the hiatus by midline anterior division of the diaphragm exposing pericardium, and transection of the two crura from their attachments to the vertebral column. The distal esophagus is then gently freed by digital dissection under direct vision with division of the two vagus nerves. At least 12
Table I. EEPT I-Cancer of the lower esophagus and cardia No. of patients Men Women Age (yr) Range Mean Tumor histology Squamouscell carcinoma Adenocarcinoma Leiomyosarcoma Resectability Morbidity Anastomotic leakage Respiratory complications Mortality(causesof death) Cerebrovascular Cardiovascular Unknown (died at home)
31 17 14 42-80 57.0 ± 7.7 16 14 1 30 (96.8%) 6 (22.2%) 3 (9.7%) 4(12.9%) 2 1 1
em of normal esophagus must be made available proximal (cephalad) to the gross tumor margin for the mucosal dissection to begin. (If it is not available, thoracotomy is necessary for proper completion of the dissection.) The situation is now ready for the novelty of the method. Instead of continuing an extraesophageal blunt dissection upward along normal esophagus, the extramucosal plane is used. Proper exposure is facilitated by tape retraction at the gastroesophageal junction, with the index finger steadying the esophagus from behind. A transverse circular myotomy is performed no less than 7 em above the palpable upper tumor margin. This is begun by transverse incision of the esophageal muscle anteriorly down to the mucosal layer. The two edges of the muscle spring apart. Coring of the mucosal layer is started by insinuating the tip of the left index finger into the submucosal plane pointed in an upward direction (Fig. 3). It is difficult to err, because this is the only anatomic plane that can be entered freely. The exploring finger follows upward, always feeling the inlying nasogastric tube through the velvety mucosa. The muscular layer is circumcised by extending the anterior incision around posteriorly where stripping is continued by inserting the fingertip upward behind the mucosal sleeve. Maintaining traction on the specimen side facilitates the stripping. Grasping the gaping edges of the upper muscular rim is not necessary. The exploring finger literally glides upward. The stripping is continued upward as far as the fingers can reach without creating undue pressure on the heart. Bleeding is scant. The specimen is now set aside, to be removed with its attached mucosal sleeve after completion of its freeing through the neck incision. A jejunostomy is brought out in the left lower quadrant for feeding. For cancers at the cervical or middle thoracic levels of the esophagus the entire stomach is mobilized. Both the right gastric and right gastroepiploic arterial supply are retained. Neck dissection. The neck is opened through a collar incision for an en bloc resection of a cervical esophageal cancer with or without a laryngectomy and unilateral radical neck dissection. If laryngectomy is included, the permanent tracheostomy is sit-
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Fig. 2. Position of the patient for the usual two incisions plus illustration (center) of principal considerations: level of gastric transection, preservation of right gastric and gastroepiploic arteries, Kocher maneuver, and pyloroplasty.
Table II. EEPT II-Cancer of the middle thoracic esophagus No. of patients Men Women Age (yr) Range Mean Tumor histology Squamouscell carcinoma Adenocarcinoma Resectability Morbidity Anastomotic leakage Respiratory complications Mortality (causesof death) Aspiration of gastric contents Adult respiratory distress syndrome Cerebrovascular
19 II 8 40-82 55.8 ± 9.9 19 0 19(100%) 0(0%) I (5.3%) 3 (15.8%)
ed in the lower skin flap. There must be enough length of normal esophagus below the lower margin of tumor to permit mucosal dissection beginning at or above the thoracic inlet. Mucosal stripping from the neck downward is performed in a manner comparable to that from below upward (Fig. 4). There are usually some filmy avascular strands between mucosa and muscle that must be cut, but bleeding stops spontaneously. The mucosal stripping is best accomplished simultaneously through the abdomen and neck, the two index fingers pushing to establish contact all around the mucosal sleeve (Fig. 5). Sometimes the index and middle fingers can both be inserted to assist in completing the stripping maneuver. The sleeve is transected at the gastroesophageal junction and the specimen removed upward through the neck with its attached mucosal sleeve of normal esophagus. For cancers of the lower esophagus the cervical esophagus is exposed through a left oblique antesternocleidomastoid incision with careful protection of the recurrent laryngeal nerve. After mucosal stripping the mucosal sleeve is transected in the neck, which allows abdominal removal of the tumor specimen with the attached sleeve. The nasogastric tube must remain in place after
Table III. EEPT III-Cancer of the cervical esophagus No. of patients Men Women Age (yr) Range Mean Tumor histology Squamouscell carcinoma Resectability Morbidity Anastomotic leakage Respiratorycomplications Mortality
o
4
4
35-63 48.5 ± 12.2 4
4 (100%) 0(0%) 0(0%) 0(0%)
extraction of the specimen and the mucosal sleeve for two reasons. First, its lower tip in the abdomen is sutured to the apex of the closed-off gastric fundus or colon segment to permit withdrawing the replacing organ through the muscular tunnel to the neck. Second, the tube acts as a taut guide to allow twofinger dilation of the empty muscular tube necessary for placing the stomach or colon within (Fig. 6). This gentle dilation is always performed in a lateral direction to avoid damage to extraesophageal mediastinal structures. The prepared stomach or colon is then guided to the neck without any holdup by pulling on the nasogastric tube with one hand while the other pushes upward from the abdominal incision. The utmost care is taken to avoid torsion. Gastrointestinal continuity is reestablished by esophagogastric anastomosis in the neck. A medium nasogastric tube is placed across this anastomosis for decompression. If total gastrectomy has been necessary, a left colon segment with the ascending branch of the left colic artery is brought up through the muscular tunnel in isoperistaltic fashion for esophagocolic anastomosis; its distal end is anastomosed to duodenum (Fig. 7). Thoracotomy. Opening the right thorax is advisable for middle thoracic esophageal cancers or if laparotomy and transhiatal dissection have not allowed sufficient exposure from below. These tumors are considered unresectable if the aorta, hilar vessels, or trachea are inseparably involved. The esophagus,
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Saidi et al.
The Journal of Thoracic and Cardiovascular Surgery
Fig. 3. Transhiatal transverse myotomy above tumor with initiation of index finger dissection, first anteriorly and then posteriorly.
Fig. 4. Transcervical transverse myotomy with scissors division of filmy avascular attachments between muscle and mucosa and beginning of downward digital dissection.
including its tumorous portion, is mobilized out of the posterior mediastinum from the gastroesophageal junction upward to a level 10 cm above the tumor. Transverse incision of the muscle layer of the esophagus down to mucosa permits cephalad mucosal stripping without the need for opening the upper mediastinal pleura (Fig. 8). Frozen section pathologic assessment of the margins is mandatory. The cut edges of the muscular tube are sutured to adjacent pleura to keep its lower end open. The specimen is removed by dividing the mucosal sleeve within the muscular tunnel at the thoracic inlet above and the esophagus at the gastroesophageal junction below. If prior laparotomy has not already been done, the abdomen
is opened, the hiatal gateway enlarged, and the stomach mobilized. The cervical esophagus is exposed through the oblique neck incision and the esophageal muscular tunnel dilated to allow stomach or colon to be drawn upward through it for cervical anastomosis. Postoperative management includes immediate chest x-ray films to allow prompt treatment of unsuspected pneumothorax, nasogastric decompression, oral feeding with small portions of clear liquid on day 4, an increase to soft solids by day 9, and the use of jejunostomy feedings when there is any concern about insufficient caloric intake or if there is any suggestion of anastomotic leakage.
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Table IV. EEPT IV-Cancer of the proximal stomach No. of patients Men Women Age (yr) Range Mean Tumor histology Adenocarcinoma Squamous cell carcinoma Resectability Bypass Morbidity Anastomotic leakage Respiratory complications Mortality (causes of death) Mediastinitis, septicemia Drug-induced C leukopenia
14 10
4
45-65 55.7 ± 6.6 13 I 13 (92.9%)
2 (16.7%) 2 (16.7%) 2 (14.3%)
')
Results Morbidity and mortality, including the causes of death, are indicated separately for each of the four groups in Tables I through IV. These tables also define relevant clinical details of the patient cohorts. There were no intraoperative deaths. Nine patients died postoperatively within 30 days, eight in the hospital within 10 days of operation and one suddenly at home of an unknown cause 2112 weeks after discharge. The operative mortality rate was 13.2%. The apparent causes of the eight hospital deaths were as follows: arrhythmias resulting in myocardial infarctions and cardiopulmonary arrest (n = 3), myocardial infarction alone (n = 1), gastric aspiration (n = I), acute respiratory distress syndrome (n = 1), leukopenic reaction to chloramphenicol (n = 1), and mediastinitis and/or septicemia (n = 1). The latter was the one death directly related to the technical procedure, after a cervical anastomotic leakage. Morbidity was related primarily to cervical anastomotic leaks (n = 8), four observed in the first 10 pilot study patients. The overall leakage rate was 13.3%. Except in the one patient with a fatal outcome, all leaks closedspontaneously within 4 to 20 days after onset. Two patients required mechanical ventilatory assistance beyond 72 hours postoperatively. Three patients had small localized empyemas responding to tube drainage. One patient had pneumonia, which responded with difficulty to bronchoscopic aspiration, chest physiotherapy, and intravenous antibiotics. Thus six surviving patients (8.8%) had major chest complications. There were six patients with recurrent nerve paresis, two permanent.
L
Fig. 5. Bimanual dissection of the mucosa from the esophageal muscular tube and the specimen removed.
The average blood loss at operation was 700 ml. Eleven patients (16.2%) required no transfusion; 43 (63.2%) received 500 to 1000 ml intraoperatively. The operations were performed by the attending and surgical resident staff under supervision, one surgical team working at a time. Stapling devices were not available. The average operating time was 6 hours. There were no instances of tracheal injury, chylothorax, or postoperative mediastinal bleeding. Swallowing capability was assessed in 53 of 57 surviving patients (93%). Swallowing was normal in 41 (77.4%),8 (51.1%) had occasional holdup of solid foods, and 4 (7.5%) could tolerate only liquids. The actuarial survival rate was 58% at 1 year, 25% at 2 years, and less than 10% at 3 years. Discussion
The prevalence of cancer of the esophagus in Iran is 180/ 100,000, the highest in the world.' The purpose of this technical study was to find the least traumatic surgical procedure for the large numbers of patients eligible for
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/
._, I ,I I
/
/
/
/
Fig. 6. Bimanual dilation of the esophageal muscular tube (sleeve) andthe replacing stomach drawn upward through it for cervical esophagogastric anastomosis.
Fig. 7. Isolation of a left colon segment with blood supply based on the ascending branch of the left colic artery and its isoperistaltic replacement through the esophageal muscular sleeve to the neck for esophagocolic anastomosis.
surgery. The principal aim was palliation of their dysphagia. The transhiatal extrathoracic approach to resection of cancers of the esophagus has gained appeal in the past
Fig. 8. Right posterolateral thoracotomy for a middle-third esophageal cancer, finger dissection ofthe superior mediastinal esophageal submucosal plane, and the specimen removed.
decade.s-? but concern has persisted that the blunt mediastinal dissectionmay be traumatic with occasionalmajor blood-letting, tracheal injury, and chylothorax."!' Although feeding esophageal arteries may be clipped to minimize bleeding, an approach in which dissection is performed within rather than outside the normal esophagus would have merit. The fear of damaging mediastinal structures, particularly for the lessexperiencedesophageal surgeon, would be markedly lessened. The concept of coring out the inner layer of a bowel segment and pulling another intact segment through the remaining outer layer is not new and is used with success in the Soave endorectal pull-through operation for Hirschsprung's disease. Just as perirectal structures are protected in that operation, so the endoesophageal pullthrough technique protects mediastinal structures. Apparently Rehn first proposed extraction of the esophageal mucous membrane to minimize bleeding.'? To the best of our knowledge, however, this proposalwas never applied clinically. The strong nonkeratinized epithelial lining of the normal esophagus and its filmy attachment to underlying layers make normal mucosal esophageal stripping eminently practical. The submucosa is looseand pliable. Feeding vessels penetrating the muscular layers at right angles become rapidly lost in the highly distensible submucosal layer. 13 Tiny filamentous strands between the mucosa and its submucosal bed, sometimes more obvious in the upper than in the lower esophagus, are generally avascular and readily cut under direct vision. In short, structural features of the normal esophagus permit an essentiallybloodless separationofits mucosal layer by developing a plane in its submucosal layer.
Volume 102 Number 1 July 1991
The importance of tumorfree distal and proximal resection margins has been emphasized repeatedly,14.15 as local recurrence would devaluate even a palliative resection. In the EEPT approach, after the hiatal gateway has been fully opened and the vagus nerves cut, a 10 em length of loweresophagus above the diaphragmatic level can be comfortably brought into view. If more than 5 to 6 em of a cancer of the loweresophagus or cardia extends above the gastroesophageal junction, however, a safe proximal resection margin may not be available at the level where mucosalstripping is to begin. There should be no hesitation in such circumstances to defer tumor resection to a thoracotomy after completing the abdominal part of the operation. By the same token, if attaining a safe distal resection margin means creating a gastric tube that would be too short to reach the neck without tension, there should be no hesitation in proceeding with total gastrectomy, with a left colon segment as the esophageal substitute. Similarly, the mucosal stripping technique can be applied to cancers of the cervical esophagus only if there is enough length of normal esophagus belowthe tumor margin and above the thoracic inlet. This last injunction would exclude esophageal cancers in the upper mediastinum from any consideration for the endoesophageal pullthrough technique. Fortunately, this is the least common location for esophageal cancers. The mucosal sleeve remainsattached to the specimen,regardless of where the tumor is located. A high resection rate was a goal and was achieved. Resection was possiblein 65 of the 68 patients (95.6%); twoothersunderwent successfulbypass.The effectiveness of the EEPT technique is dramatized by the absence of mediastinal hemorrhage, tracheobronchial injury, and chylothorax. No evidence existed that a snug muscular tube contributed to the 13.2%leakage rate; these cervical leaks healed spontaneously in the eight survivors. Gentleand thorough manual dilation of the esophageal muscletube is the key. Used as a conduit for either stomach or colon, the deepithelialized muscular tube distendsto accommodate a functional esophagealsubstitute. This isclearly evident on careful fluoroscopic observation of the postoperative barium esophagogram. In the absence of manometric studies, it can be assumed on clinical and radiographic grounds that contractions or spasm of the muscular tube are neither severe nor suffi-
ciently -persistent to interfere withcomfortable swallowing. Particularly in the patients in whom the colon was the replacementorgan, the muscular esophageal tube sleeve contained the colon within the posterior mediastinum, preventing any lateral kinking or redundancy.
Endothoracic endoesophageal pull-through technique 4 9
REFERENCES 1. Orringer MB. Transhiatal esophagectomy without thoracotomy forcarcinoma of the thoracic esophagus. Ann Surg 1984;200:282-8. 2. Kmet J, Mahboubi E. Esophageal cancer in the Caspian Iittorial ofIran: initial studies. Science 1972;175:846-53. 3. American Joint Committee on Cancer. Beahrs P, Myers MH, eds. Manual forstaging of cancer. 2nded. Philadelphia, JB Lippincott, 1983:61-72. 4. SaidiF. Endoesophageal pull-through: a technique for the treatment of cancers of the cardia and lower esophagus. Ann Surg 1988;207:446-54. 5. Mahboubi E, Kmet J, Cook PJ, Day NE, Ghadman P, Salmasizadeh S. Oesophageal cancer studies in the Caspian littorial of Iran:theCaspian Cancer Registry. BrJ Cancer 1973;28:197-214. 6. Goldfaden D, Orringer MB, Appleman HD, Kalish R. Adenocarcinoma ofthedistal esophagus andgastric cardia. J THORAC CARDIOVASC SURG 1986;91:242-7. 7. Wong J. Transhiatal oesophagectomy forcarcinoma ofthe thoracic oesophagus. Br J Surg 1986;73:89-90. 8. Shahian DM, Neptune WB, Ellis FH Jr, Watkins E Jr. Transthoracic versus extrathoracic esophagectomy: mortality, morbidity, andlong-term survival. AnnThoracSurg 1986;41:237-46. 9. Liebermann-MeffertDMI,LuescherU,NeffU,RuediTP, Allgower M. Esophagectomy without thoracotomy: Is therea risk of intramediastinal bleeding? Ann Surg 1987; 206:184-92. 10. Finley RJ, Grace M, Duff JH. Esophagogastrectomy without thoracotomy forcarcinoma of the cardiaand lowerpartoftheesophagus. SurgGynecol Obstet1985;160:4956. 11. Baker JW, Schechter GL. Management of panesophageal cancer by bluntresection without thoracotomy and reconstruction withstomach. Ann Surg 1986;203:491-9. 12. Pinotti HW, Zilberstein B,Pollara W, RaiaA. Esophagectomy without thoracotomy. Surg Gynecol Obstet 1981; 152:345-6. 13. PotterSE,Holyoke EA.Observations ontheintrinsic blood supply of the esophagus. Arch Surg 1950;61 :944-8. 14. Skinner DB. En bloc resection for neoplasms of the esophagus and cardia. J THORAC CARDIOVASC SURG 1983; 85:59-71. 15. Tam PC, Cheung HC, Ma L, Siu KF, Wong J. Local recurrence aftersubtotal esophagectomy forsquamous cell carcinoma. Ann Surg 1987;205:189-94.
Discussion Dr. Clement A. Hiebert (Toronto, Ontario, Canada). This is a remarkable idea. I have used your technique on oneoccasion and found it everything you claim it to be: simple, bloodless, and logical. I mustadmit to a moment of trepidation as I first tugged on that mucosal sleeve. What would I do if it snapped offin the middle? It yielded only withpersistent tugging before giving way, much as a belt around the waist does
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when pulled through all the loops at once. The muscle sleeve stretched easily to accommodate the gastric tube, just as you said. Now I must share some concerns. Is it right to do this operation for a notoriously multicentric disease such as esophageal cancer? Is there the possibility of further compromising venous return at the thoracic inlet? Does the muscle sleeve retain its peristaltic commitment, and if so, does it aid or hinder swallowing? Dr. Saidi. I can simply answer Dr. Hiebert's philosophic concern by saying that the EEPT is a method of reconstruction after resection. I hope I have made it clear that no limitations or restrictions are placed on the surgeon's decision regarding the extent of the resection. If the aim is curative, so be it; if palliation is the principal purpose, this is not changed in any way. Survival depends primarily on the biologic nature and behavior of the tumor and therefore is not affected by the mode of reconstruction used. We have been pleased to establish for most patients-and unfortunately we have too many of them-the ability to eat comfortably as much food of any variety as they desire. The 7.6% with "poor" swallowing ability consists of four patients who could not swallow solids all the time, three of them having had anastomotic stricture. Dilation or revision of their stricture did overcome the problem. Yes, islands of mucosa can be left behind if the mucosal stripping is done in a hurried manner. On two occasions when the mucosal sleeve was pulled out too forcefully and did not come out in one piece we were able to extract the remaining mucosal shreds without much difficulty. The operations were done by the attending and resident surgical staff, and we did not have staplers available. We have not had a reason or need to switch to the transhiatal extraesophageal approach. I can assure you that with good surgical sense and gentleness it is a rather simple and straightforward operation. The postmortem specimen from a I3-year-old boy with cancer of the cervical esophagus, who was not part of the series of patients presented and who died of the tracheostomy tube eroding the innominate artery, showed that the esophageal muscular tunnel wraps itself around the contained colon loop. It makes one wonder if the venous circulation of the transplanted organ is not being compressed. Lacking manometric studies, I must rely on the functional results obtained in saying that the esophageal substitute within the muscular tunnel functions as a satisfactory swallowing gullet. I too was worried that our initially high rate of cervical anastomotic leakage might be due to a constriction of the muscular tunnel, as there were four leaks in the first 10 patients with cancer of the cardia and lower esophagus. However, greater care in the technical execution of the anastomosis resulted in only four more leaks in the next 58 cases. Dr. Mark B. Orringer (Ann Arbor, Mich.). This innovative technique relies on the unusual fat content of the esophageal submucosa, which allows more mobility of the overlying mucosa than in any other portion of the alimentary tract. This technique is a refinement of the mucosa-stripping inversion technique described by Akiyama! and our Chinese colleagues' I am concerned about leaving in a portion of the esophagus being resected for cancer, but that concern may be as unfounded as the concern about doing a transhiatal esophagectomy and leaving in some of the mediastinal lymph nodes contiguous with the organ. I have several questions. First, is there any real advantage of
this technique in terms of blood loss? As experience with transhiatal esophagectomy is gained, more of the operation is done through the hiatus under direct vision, and blood lossdiminishes. In our last 18 transhiatal esophagectomies, one patient received 1 unit of blood; none of the others required transfusions. Because Dr. Saidi's technique does not achieve as high a margin above tumor as with a standard transhiatal esophagectomy and a portion of the muscular wall of the esophagus near the tumor is left behind, is there any difference in local tumor control or recurrence involving the unresected native esophagus? Third, is any difficulty encountered in pulling the mobilized colon graft up through the narrow muscular tunnel? That is, would not injury to the vascular pedicle be more likely with this approach? Finally, my greatest concern in performing a cervical esophagogastric anastomosis is protection of the proximal remaining esophagus. Once you have circumcised the esophageal muscle in the neck and begun traction and upward pulling, trauma to the proximal end of esophagus above the myotomy may occur, perhaps explaining the 14% prevalence of anastomotic leakage, which certainly is a higher figure than we would accept. REFERENCES I. Akiyama H. Esophagectomy without thoracotomy. In: Stipa S, Belsey RH, Moraldi A, eds. Medical and surgical problems of the esophagus. Serono Symposia. Vol: 43. London: Academic Press, 1981:339-44. 2. WU TQ, Jiang XM. Treatment of carcinoma of the gastric cardia by inversion esophagectomy and without thoracotomy (in Chinese). Chin Med J 1979;59:358-60. (Referenced in: Huang GJ, K'ai WY, eds. Carcinoma of the esophagus and gastric cardia. Berlin: Springer-Verlag, 1984:320-1.) Dr. Saidi. Thank you, Dr. Orringer; I will answer your questions in the reverse order asked. The proximal end of the cervical esophagus, once esophageal circumcision in the neck is completed, is kept aside until anastomosis and is not traumatized in any way. We have not had any difficulty in pulling the colon loop to the neck, because it goes through a channel of predetermined length and width, which incidentally, is also the shortest possibleanatomic route between the abdomen and the neck. Opening the hiatal gateway wide, which includes cutting the two crura, brings the inferior mediastinum into full view,allowing ready access to the esophagus at least 12 to 15 cm above the gastroesophageal junction. The mucosal stripping can be started at a satisfactory level above the tumor for cancers of the lower esophagus and cardia, verifying absence of tumor by frozen section at the transection line. If mucosal stripping cannot be started under direct vision some 7 to 10 em proximal to the tumor, resection is performed through the chest after the stomach is mobilized in the abdomen. There is essentially no bleeding during the reconstruction phase of the operation, as we have had no postoperative or excessive intraoperative bleeding. As you quite rightly pointed out, the whole concept of the operation is based on known anatomic features of the normal esophagus. The muscular layer of the esophagus, in particular, has the beautiful characteristic of being able to expand enormously and remain expanded.
THORAC CARDIOVASC SURG
1991;102:43-50
Endothoracic endoesophageal pull-through operation A new approach to cancers of the esophagus and proximal stomach Many thoracic surgeons have expressed concern about the complications inherent in transhiataI esophagectomy without thoracotomy. The technique of endothoracic endoesophageal pull-through uses a mucosal coring of normal esophagus beyond the tumor and leaves a muscular tube through which the substitute organ is passed. Mediastinal hemorrhage, tracheal injury, and chylothorax are eliminated.
Farrokh Saidi, MD, FACS, FRCS (by.invitation), Azizollah Abbassi, MD (by invitation), M. Behgam Shadmehr, MD (by invitation), and Gholamreza Khoshnevis-Asl, MD (by invitation), Tehran, Iran Sponsored by Clement A. Hiebert, Portland, Maine
firing esophagectomy for cancer the surgeon may justifiably extend the scope of resection with the idea of achieving possible cure. In the reconstructive phase of the operation, however, reduction of surgical trauma must remain the primary consideration. The revival of transhiatal esophagectomy without thoracotomy is based on the assumptions that avoiding thoracotomy results in lessened cardiopulmonary morbidity and that placing the anastomosis in the neck eliminates the mortality attending leakage from an intrathoracic anastomosis. I A further technical refinement in lowering operative trauma is now proposed, based on the simple maneuver of gently coring out the normal mucosal layer of the esophagus adjacent to a carcinoma rather than forcefully extracting the whole organ from within the mediastinum. This proposed extrathoracic endoesophageal approach is an essentially bloodless procedure in which the stripped mucosal layer is removed in continuity with the neoplastic specimen, the mediastinal structures protected in the blunt dissection, and the residual esophageal muscular tube used as the conduit through which stomach or colon
From the Departments of Thoracic and General Surgery, Modarress Hospital, School of Medicine, Beheshti University of Medical Sciences, Tehran, Iran. Supported by The Specialty Research Council of Beheshti University of Medical Sciences, Grant P/25/3/1468. Read at the Seventieth Annual Meeting of The American Association for Thoracic Surgery, Toronto, Ontario, Canada, May 7-9,1990. Address for reprints: Farrokh Saidi, MD, FACS, FRCS, Park Ave., Seventh St., No.3, Tehran, Iran 15137.
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is drawn to the neck for a primary cervical anastomosis. No restriction is placed on the actual extent of planned tumor resection.
Patients and methods Clinical material. BetweenOctober 1986and October 1989, 68 unselectedpatients with cancers of the esophagus and proximal stomach were operated on consecutively by the attending and resident surgical staff, Modarress Hospital, Beheshti University of Medical Sciences, Tehran, Iran. The majority of patientscame from the northern provinces of the country where esophagealcancer is particularly prevalent.2 The typical history included difficulty in swallowing solids or liquids, or both, with ensuing weight loss. The diagnosis was established in all cases by barium esophagogram and endoscopic tumor biopsy. No other staging was performed. Although emaciation was often severe,no patient was judged unable to tolerate the procedure,and onlythree received preoperativehyperalimentation. The primary goal for all patients was to reestablish the ability to swallow. In perhaps fivecases only did the surgeon believea curative resection had been achieved. Postoperative staging revealed the tumor of 18 patients in TNM stage II (26.4%),45 patients in stage III (66.2%), and 5 patients in stage IV (7.4%).3 Technique. The operative approach has been modifiedfrom that used in the original pilot series.t It is now adjusted for the level of esophagealor proximalgastric tumor location.The procedure has been called an endothoracic endoesophageal pullthrough operation (EEPT). Thus the 68 patients are dividedinto four groups: EEPT I for cancers of the cardia and loweresophagus, EEPT II for cancers of the middle esophagus, EEPT III for cancers of the cervicalesophagus,and EEPT IV for cancers of the proximal stomach (Fig. 1). An abdominal and a cervical incision are performed in all patients (Fig. 2). Patients with middle esophageal cancers also require a thoracotomy. The order in which the incisions are performed varies with the location of the tumor. The colon is
43
The Journal of Thoracic and Cardiovascular Surgery
44 Saidi et al.
" EEPT I
"
Number of
Thoracotomy
Esophageal
Patients
~equired
Substitute
3 1
1 9
1 4
NO
YES
Stomach
Stomach
NO
Stomach
NO
Colon
Fig. I. Sketches illustrating the definitions of the four types of EEPT with patient numbers and strategy of surgical management.
routinely prepared preoperatively in case the stomach is not suitable for replacement. Laparotomy. The abdomen is opened for (I) resection of tumors of the lower esophagus, the cardia, or proximal stomach followed by mobilization of either a gastric tube or colon segment for the pull-through or (2) mobilization of the whole stomach or colon segment as the replacement organ in patients with cancers of the cervical and middle thoracic esophagus. For middle esophageal cancers the laparotomy may either precede or follow thoracotomy for mobilization and resection of the cancer. The operative approach to cancers of the lower esophagus and cardia ma y be curative or pallia tive in concept, depending on the extent of tumor. Thus splenectomy and regional lymph node removal are optional. The Kocher maneuver is mandatory. Pyloroplasty is preferred to either pyloromyotomy or dilation of the pyloric muscle. The decision of whether stomach will reach to the neck after tumor resection can be made with reasonable confidence. Frozen section pathologic study of this distal resection margin must be negative for malignant cells. If not, total gastrectomy followed by mobilization of the left hemicolon as an esophageal substitute may be more prudent. For these distal tumors the operative approach is the standard transhiatal dissection: detachment of the left hepatic lobe, enlargement of the hiatus by midline anterior division of the diaphragm exposing pericardium, and transection of the two crura from their attachments to the vertebral column. The distal esophagus is then gently freed by digital dissection under direct vision with division of the two vagus nerves. At least 12
Table I. EEPT I-Cancer of the lower esophagus and cardia No. of patients Men Women Age (yr) Range Mean Tumor histology Squamouscell carcinoma Adenocarcinoma Leiomyosarcoma Resectability Morbidity Anastomotic leakage Respiratory complications Mortality(causesof death) Cerebrovascular Cardiovascular Unknown (died at home)
31 17 14 42-80 57.0 ± 7.7 16 14 1 30 (96.8%) 6 (22.2%) 3 (9.7%) 4(12.9%) 2 1 1
em of normal esophagus must be made available proximal (cephalad) to the gross tumor margin for the mucosal dissection to begin. (If it is not available, thoracotomy is necessary for proper completion of the dissection.) The situation is now ready for the novelty of the method. Instead of continuing an extraesophageal blunt dissection upward along normal esophagus, the extramucosal plane is used. Proper exposure is facilitated by tape retraction at the gastroesophageal junction, with the index finger steadying the esophagus from behind. A transverse circular myotomy is performed no less than 7 em above the palpable upper tumor margin. This is begun by transverse incision of the esophageal muscle anteriorly down to the mucosal layer. The two edges of the muscle spring apart. Coring of the mucosal layer is started by insinuating the tip of the left index finger into the submucosal plane pointed in an upward direction (Fig. 3). It is difficult to err, because this is the only anatomic plane that can be entered freely. The exploring finger follows upward, always feeling the inlying nasogastric tube through the velvety mucosa. The muscular layer is circumcised by extending the anterior incision around posteriorly where stripping is continued by inserting the fingertip upward behind the mucosal sleeve. Maintaining traction on the specimen side facilitates the stripping. Grasping the gaping edges of the upper muscular rim is not necessary. The exploring finger literally glides upward. The stripping is continued upward as far as the fingers can reach without creating undue pressure on the heart. Bleeding is scant. The specimen is now set aside, to be removed with its attached mucosal sleeve after completion of its freeing through the neck incision. A jejunostomy is brought out in the left lower quadrant for feeding. For cancers at the cervical or middle thoracic levels of the esophagus the entire stomach is mobilized. Both the right gastric and right gastroepiploic arterial supply are retained. Neck dissection. The neck is opened through a collar incision for an en bloc resection of a cervical esophageal cancer with or without a laryngectomy and unilateral radical neck dissection. If laryngectomy is included, the permanent tracheostomy is sit-
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Fig. 2. Position of the patient for the usual two incisions plus illustration (center) of principal considerations: level of gastric transection, preservation of right gastric and gastroepiploic arteries, Kocher maneuver, and pyloroplasty.
Table II. EEPT II-Cancer of the middle thoracic esophagus No. of patients Men Women Age (yr) Range Mean Tumor histology Squamouscell carcinoma Adenocarcinoma Resectability Morbidity Anastomotic leakage Respiratory complications Mortality (causesof death) Aspiration of gastric contents Adult respiratory distress syndrome Cerebrovascular
19 II 8 40-82 55.8 ± 9.9 19 0 19(100%) 0(0%) I (5.3%) 3 (15.8%)
ed in the lower skin flap. There must be enough length of normal esophagus below the lower margin of tumor to permit mucosal dissection beginning at or above the thoracic inlet. Mucosal stripping from the neck downward is performed in a manner comparable to that from below upward (Fig. 4). There are usually some filmy avascular strands between mucosa and muscle that must be cut, but bleeding stops spontaneously. The mucosal stripping is best accomplished simultaneously through the abdomen and neck, the two index fingers pushing to establish contact all around the mucosal sleeve (Fig. 5). Sometimes the index and middle fingers can both be inserted to assist in completing the stripping maneuver. The sleeve is transected at the gastroesophageal junction and the specimen removed upward through the neck with its attached mucosal sleeve of normal esophagus. For cancers of the lower esophagus the cervical esophagus is exposed through a left oblique antesternocleidomastoid incision with careful protection of the recurrent laryngeal nerve. After mucosal stripping the mucosal sleeve is transected in the neck, which allows abdominal removal of the tumor specimen with the attached sleeve. The nasogastric tube must remain in place after
Table III. EEPT III-Cancer of the cervical esophagus No. of patients Men Women Age (yr) Range Mean Tumor histology Squamouscell carcinoma Resectability Morbidity Anastomotic leakage Respiratorycomplications Mortality
o
4
4
35-63 48.5 ± 12.2 4
4 (100%) 0(0%) 0(0%) 0(0%)
extraction of the specimen and the mucosal sleeve for two reasons. First, its lower tip in the abdomen is sutured to the apex of the closed-off gastric fundus or colon segment to permit withdrawing the replacing organ through the muscular tunnel to the neck. Second, the tube acts as a taut guide to allow twofinger dilation of the empty muscular tube necessary for placing the stomach or colon within (Fig. 6). This gentle dilation is always performed in a lateral direction to avoid damage to extraesophageal mediastinal structures. The prepared stomach or colon is then guided to the neck without any holdup by pulling on the nasogastric tube with one hand while the other pushes upward from the abdominal incision. The utmost care is taken to avoid torsion. Gastrointestinal continuity is reestablished by esophagogastric anastomosis in the neck. A medium nasogastric tube is placed across this anastomosis for decompression. If total gastrectomy has been necessary, a left colon segment with the ascending branch of the left colic artery is brought up through the muscular tunnel in isoperistaltic fashion for esophagocolic anastomosis; its distal end is anastomosed to duodenum (Fig. 7). Thoracotomy. Opening the right thorax is advisable for middle thoracic esophageal cancers or if laparotomy and transhiatal dissection have not allowed sufficient exposure from below. These tumors are considered unresectable if the aorta, hilar vessels, or trachea are inseparably involved. The esophagus,
46
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The Journal of Thoracic and Cardiovascular Surgery
Fig. 3. Transhiatal transverse myotomy above tumor with initiation of index finger dissection, first anteriorly and then posteriorly.
Fig. 4. Transcervical transverse myotomy with scissors division of filmy avascular attachments between muscle and mucosa and beginning of downward digital dissection.
including its tumorous portion, is mobilized out of the posterior mediastinum from the gastroesophageal junction upward to a level 10 cm above the tumor. Transverse incision of the muscle layer of the esophagus down to mucosa permits cephalad mucosal stripping without the need for opening the upper mediastinal pleura (Fig. 8). Frozen section pathologic assessment of the margins is mandatory. The cut edges of the muscular tube are sutured to adjacent pleura to keep its lower end open. The specimen is removed by dividing the mucosal sleeve within the muscular tunnel at the thoracic inlet above and the esophagus at the gastroesophageal junction below. If prior laparotomy has not already been done, the abdomen
is opened, the hiatal gateway enlarged, and the stomach mobilized. The cervical esophagus is exposed through the oblique neck incision and the esophageal muscular tunnel dilated to allow stomach or colon to be drawn upward through it for cervical anastomosis. Postoperative management includes immediate chest x-ray films to allow prompt treatment of unsuspected pneumothorax, nasogastric decompression, oral feeding with small portions of clear liquid on day 4, an increase to soft solids by day 9, and the use of jejunostomy feedings when there is any concern about insufficient caloric intake or if there is any suggestion of anastomotic leakage.
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Table IV. EEPT IV-Cancer of the proximal stomach No. of patients Men Women Age (yr) Range Mean Tumor histology Adenocarcinoma Squamous cell carcinoma Resectability Bypass Morbidity Anastomotic leakage Respiratory complications Mortality (causes of death) Mediastinitis, septicemia Drug-induced C leukopenia
14 10
4
45-65 55.7 ± 6.6 13 I 13 (92.9%)
2 (16.7%) 2 (16.7%) 2 (14.3%)
')
Results Morbidity and mortality, including the causes of death, are indicated separately for each of the four groups in Tables I through IV. These tables also define relevant clinical details of the patient cohorts. There were no intraoperative deaths. Nine patients died postoperatively within 30 days, eight in the hospital within 10 days of operation and one suddenly at home of an unknown cause 2112 weeks after discharge. The operative mortality rate was 13.2%. The apparent causes of the eight hospital deaths were as follows: arrhythmias resulting in myocardial infarctions and cardiopulmonary arrest (n = 3), myocardial infarction alone (n = 1), gastric aspiration (n = I), acute respiratory distress syndrome (n = 1), leukopenic reaction to chloramphenicol (n = 1), and mediastinitis and/or septicemia (n = 1). The latter was the one death directly related to the technical procedure, after a cervical anastomotic leakage. Morbidity was related primarily to cervical anastomotic leaks (n = 8), four observed in the first 10 pilot study patients. The overall leakage rate was 13.3%. Except in the one patient with a fatal outcome, all leaks closedspontaneously within 4 to 20 days after onset. Two patients required mechanical ventilatory assistance beyond 72 hours postoperatively. Three patients had small localized empyemas responding to tube drainage. One patient had pneumonia, which responded with difficulty to bronchoscopic aspiration, chest physiotherapy, and intravenous antibiotics. Thus six surviving patients (8.8%) had major chest complications. There were six patients with recurrent nerve paresis, two permanent.
L
Fig. 5. Bimanual dissection of the mucosa from the esophageal muscular tube and the specimen removed.
The average blood loss at operation was 700 ml. Eleven patients (16.2%) required no transfusion; 43 (63.2%) received 500 to 1000 ml intraoperatively. The operations were performed by the attending and surgical resident staff under supervision, one surgical team working at a time. Stapling devices were not available. The average operating time was 6 hours. There were no instances of tracheal injury, chylothorax, or postoperative mediastinal bleeding. Swallowing capability was assessed in 53 of 57 surviving patients (93%). Swallowing was normal in 41 (77.4%),8 (51.1%) had occasional holdup of solid foods, and 4 (7.5%) could tolerate only liquids. The actuarial survival rate was 58% at 1 year, 25% at 2 years, and less than 10% at 3 years. Discussion
The prevalence of cancer of the esophagus in Iran is 180/ 100,000, the highest in the world.' The purpose of this technical study was to find the least traumatic surgical procedure for the large numbers of patients eligible for
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Thoracic and Cardiovascular Surgery
/
._, I ,I I
/
/
/
/
Fig. 6. Bimanual dilation of the esophageal muscular tube (sleeve) andthe replacing stomach drawn upward through it for cervical esophagogastric anastomosis.
Fig. 7. Isolation of a left colon segment with blood supply based on the ascending branch of the left colic artery and its isoperistaltic replacement through the esophageal muscular sleeve to the neck for esophagocolic anastomosis.
surgery. The principal aim was palliation of their dysphagia. The transhiatal extrathoracic approach to resection of cancers of the esophagus has gained appeal in the past
Fig. 8. Right posterolateral thoracotomy for a middle-third esophageal cancer, finger dissection ofthe superior mediastinal esophageal submucosal plane, and the specimen removed.
decade.s-? but concern has persisted that the blunt mediastinal dissectionmay be traumatic with occasionalmajor blood-letting, tracheal injury, and chylothorax."!' Although feeding esophageal arteries may be clipped to minimize bleeding, an approach in which dissection is performed within rather than outside the normal esophagus would have merit. The fear of damaging mediastinal structures, particularly for the lessexperiencedesophageal surgeon, would be markedly lessened. The concept of coring out the inner layer of a bowel segment and pulling another intact segment through the remaining outer layer is not new and is used with success in the Soave endorectal pull-through operation for Hirschsprung's disease. Just as perirectal structures are protected in that operation, so the endoesophageal pullthrough technique protects mediastinal structures. Apparently Rehn first proposed extraction of the esophageal mucous membrane to minimize bleeding.'? To the best of our knowledge, however, this proposalwas never applied clinically. The strong nonkeratinized epithelial lining of the normal esophagus and its filmy attachment to underlying layers make normal mucosal esophageal stripping eminently practical. The submucosa is looseand pliable. Feeding vessels penetrating the muscular layers at right angles become rapidly lost in the highly distensible submucosal layer. 13 Tiny filamentous strands between the mucosa and its submucosal bed, sometimes more obvious in the upper than in the lower esophagus, are generally avascular and readily cut under direct vision. In short, structural features of the normal esophagus permit an essentiallybloodless separationofits mucosal layer by developing a plane in its submucosal layer.
Volume 102 Number 1 July 1991
The importance of tumorfree distal and proximal resection margins has been emphasized repeatedly,14.15 as local recurrence would devaluate even a palliative resection. In the EEPT approach, after the hiatal gateway has been fully opened and the vagus nerves cut, a 10 em length of loweresophagus above the diaphragmatic level can be comfortably brought into view. If more than 5 to 6 em of a cancer of the loweresophagus or cardia extends above the gastroesophageal junction, however, a safe proximal resection margin may not be available at the level where mucosalstripping is to begin. There should be no hesitation in such circumstances to defer tumor resection to a thoracotomy after completing the abdominal part of the operation. By the same token, if attaining a safe distal resection margin means creating a gastric tube that would be too short to reach the neck without tension, there should be no hesitation in proceeding with total gastrectomy, with a left colon segment as the esophageal substitute. Similarly, the mucosal stripping technique can be applied to cancers of the cervical esophagus only if there is enough length of normal esophagus belowthe tumor margin and above the thoracic inlet. This last injunction would exclude esophageal cancers in the upper mediastinum from any consideration for the endoesophageal pullthrough technique. Fortunately, this is the least common location for esophageal cancers. The mucosal sleeve remainsattached to the specimen,regardless of where the tumor is located. A high resection rate was a goal and was achieved. Resection was possiblein 65 of the 68 patients (95.6%); twoothersunderwent successfulbypass.The effectiveness of the EEPT technique is dramatized by the absence of mediastinal hemorrhage, tracheobronchial injury, and chylothorax. No evidence existed that a snug muscular tube contributed to the 13.2%leakage rate; these cervical leaks healed spontaneously in the eight survivors. Gentleand thorough manual dilation of the esophageal muscletube is the key. Used as a conduit for either stomach or colon, the deepithelialized muscular tube distendsto accommodate a functional esophagealsubstitute. This isclearly evident on careful fluoroscopic observation of the postoperative barium esophagogram. In the absence of manometric studies, it can be assumed on clinical and radiographic grounds that contractions or spasm of the muscular tube are neither severe nor suffi-
ciently -persistent to interfere withcomfortable swallowing. Particularly in the patients in whom the colon was the replacementorgan, the muscular esophageal tube sleeve contained the colon within the posterior mediastinum, preventing any lateral kinking or redundancy.
Endothoracic endoesophageal pull-through technique 4 9
REFERENCES 1. Orringer MB. Transhiatal esophagectomy without thoracotomy forcarcinoma of the thoracic esophagus. Ann Surg 1984;200:282-8. 2. Kmet J, Mahboubi E. Esophageal cancer in the Caspian Iittorial ofIran: initial studies. Science 1972;175:846-53. 3. American Joint Committee on Cancer. Beahrs P, Myers MH, eds. Manual forstaging of cancer. 2nded. Philadelphia, JB Lippincott, 1983:61-72. 4. SaidiF. Endoesophageal pull-through: a technique for the treatment of cancers of the cardia and lower esophagus. Ann Surg 1988;207:446-54. 5. Mahboubi E, Kmet J, Cook PJ, Day NE, Ghadman P, Salmasizadeh S. Oesophageal cancer studies in the Caspian littorial of Iran:theCaspian Cancer Registry. BrJ Cancer 1973;28:197-214. 6. Goldfaden D, Orringer MB, Appleman HD, Kalish R. Adenocarcinoma ofthedistal esophagus andgastric cardia. J THORAC CARDIOVASC SURG 1986;91:242-7. 7. Wong J. Transhiatal oesophagectomy forcarcinoma ofthe thoracic oesophagus. Br J Surg 1986;73:89-90. 8. Shahian DM, Neptune WB, Ellis FH Jr, Watkins E Jr. Transthoracic versus extrathoracic esophagectomy: mortality, morbidity, andlong-term survival. AnnThoracSurg 1986;41:237-46. 9. Liebermann-MeffertDMI,LuescherU,NeffU,RuediTP, Allgower M. Esophagectomy without thoracotomy: Is therea risk of intramediastinal bleeding? Ann Surg 1987; 206:184-92. 10. Finley RJ, Grace M, Duff JH. Esophagogastrectomy without thoracotomy forcarcinoma of the cardiaand lowerpartoftheesophagus. SurgGynecol Obstet1985;160:4956. 11. Baker JW, Schechter GL. Management of panesophageal cancer by bluntresection without thoracotomy and reconstruction withstomach. Ann Surg 1986;203:491-9. 12. Pinotti HW, Zilberstein B,Pollara W, RaiaA. Esophagectomy without thoracotomy. Surg Gynecol Obstet 1981; 152:345-6. 13. PotterSE,Holyoke EA.Observations ontheintrinsic blood supply of the esophagus. Arch Surg 1950;61 :944-8. 14. Skinner DB. En bloc resection for neoplasms of the esophagus and cardia. J THORAC CARDIOVASC SURG 1983; 85:59-71. 15. Tam PC, Cheung HC, Ma L, Siu KF, Wong J. Local recurrence aftersubtotal esophagectomy forsquamous cell carcinoma. Ann Surg 1987;205:189-94.
Discussion Dr. Clement A. Hiebert (Toronto, Ontario, Canada). This is a remarkable idea. I have used your technique on oneoccasion and found it everything you claim it to be: simple, bloodless, and logical. I mustadmit to a moment of trepidation as I first tugged on that mucosal sleeve. What would I do if it snapped offin the middle? It yielded only withpersistent tugging before giving way, much as a belt around the waist does
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5 0 Saidi et al.
when pulled through all the loops at once. The muscle sleeve stretched easily to accommodate the gastric tube, just as you said. Now I must share some concerns. Is it right to do this operation for a notoriously multicentric disease such as esophageal cancer? Is there the possibility of further compromising venous return at the thoracic inlet? Does the muscle sleeve retain its peristaltic commitment, and if so, does it aid or hinder swallowing? Dr. Saidi. I can simply answer Dr. Hiebert's philosophic concern by saying that the EEPT is a method of reconstruction after resection. I hope I have made it clear that no limitations or restrictions are placed on the surgeon's decision regarding the extent of the resection. If the aim is curative, so be it; if palliation is the principal purpose, this is not changed in any way. Survival depends primarily on the biologic nature and behavior of the tumor and therefore is not affected by the mode of reconstruction used. We have been pleased to establish for most patients-and unfortunately we have too many of them-the ability to eat comfortably as much food of any variety as they desire. The 7.6% with "poor" swallowing ability consists of four patients who could not swallow solids all the time, three of them having had anastomotic stricture. Dilation or revision of their stricture did overcome the problem. Yes, islands of mucosa can be left behind if the mucosal stripping is done in a hurried manner. On two occasions when the mucosal sleeve was pulled out too forcefully and did not come out in one piece we were able to extract the remaining mucosal shreds without much difficulty. The operations were done by the attending and resident surgical staff, and we did not have staplers available. We have not had a reason or need to switch to the transhiatal extraesophageal approach. I can assure you that with good surgical sense and gentleness it is a rather simple and straightforward operation. The postmortem specimen from a I3-year-old boy with cancer of the cervical esophagus, who was not part of the series of patients presented and who died of the tracheostomy tube eroding the innominate artery, showed that the esophageal muscular tunnel wraps itself around the contained colon loop. It makes one wonder if the venous circulation of the transplanted organ is not being compressed. Lacking manometric studies, I must rely on the functional results obtained in saying that the esophageal substitute within the muscular tunnel functions as a satisfactory swallowing gullet. I too was worried that our initially high rate of cervical anastomotic leakage might be due to a constriction of the muscular tunnel, as there were four leaks in the first 10 patients with cancer of the cardia and lower esophagus. However, greater care in the technical execution of the anastomosis resulted in only four more leaks in the next 58 cases. Dr. Mark B. Orringer (Ann Arbor, Mich.). This innovative technique relies on the unusual fat content of the esophageal submucosa, which allows more mobility of the overlying mucosa than in any other portion of the alimentary tract. This technique is a refinement of the mucosa-stripping inversion technique described by Akiyama! and our Chinese colleagues' I am concerned about leaving in a portion of the esophagus being resected for cancer, but that concern may be as unfounded as the concern about doing a transhiatal esophagectomy and leaving in some of the mediastinal lymph nodes contiguous with the organ. I have several questions. First, is there any real advantage of
this technique in terms of blood loss? As experience with transhiatal esophagectomy is gained, more of the operation is done through the hiatus under direct vision, and blood lossdiminishes. In our last 18 transhiatal esophagectomies, one patient received 1 unit of blood; none of the others required transfusions. Because Dr. Saidi's technique does not achieve as high a margin above tumor as with a standard transhiatal esophagectomy and a portion of the muscular wall of the esophagus near the tumor is left behind, is there any difference in local tumor control or recurrence involving the unresected native esophagus? Third, is any difficulty encountered in pulling the mobilized colon graft up through the narrow muscular tunnel? That is, would not injury to the vascular pedicle be more likely with this approach? Finally, my greatest concern in performing a cervical esophagogastric anastomosis is protection of the proximal remaining esophagus. Once you have circumcised the esophageal muscle in the neck and begun traction and upward pulling, trauma to the proximal end of esophagus above the myotomy may occur, perhaps explaining the 14% prevalence of anastomotic leakage, which certainly is a higher figure than we would accept. REFERENCES I. Akiyama H. Esophagectomy without thoracotomy. In: Stipa S, Belsey RH, Moraldi A, eds. Medical and surgical problems of the esophagus. Serono Symposia. Vol: 43. London: Academic Press, 1981:339-44. 2. WU TQ, Jiang XM. Treatment of carcinoma of the gastric cardia by inversion esophagectomy and without thoracotomy (in Chinese). Chin Med J 1979;59:358-60. (Referenced in: Huang GJ, K'ai WY, eds. Carcinoma of the esophagus and gastric cardia. Berlin: Springer-Verlag, 1984:320-1.) Dr. Saidi. Thank you, Dr. Orringer; I will answer your questions in the reverse order asked. The proximal end of the cervical esophagus, once esophageal circumcision in the neck is completed, is kept aside until anastomosis and is not traumatized in any way. We have not had any difficulty in pulling the colon loop to the neck, because it goes through a channel of predetermined length and width, which incidentally, is also the shortest possibleanatomic route between the abdomen and the neck. Opening the hiatal gateway wide, which includes cutting the two crura, brings the inferior mediastinum into full view,allowing ready access to the esophagus at least 12 to 15 cm above the gastroesophageal junction. The mucosal stripping can be started at a satisfactory level above the tumor for cancers of the lower esophagus and cardia, verifying absence of tumor by frozen section at the transection line. If mucosal stripping cannot be started under direct vision some 7 to 10 em proximal to the tumor, resection is performed through the chest after the stomach is mobilized in the abdomen. There is essentially no bleeding during the reconstruction phase of the operation, as we have had no postoperative or excessive intraoperative bleeding. As you quite rightly pointed out, the whole concept of the operation is based on known anatomic features of the normal esophagus. The muscular layer of the esophagus, in particular, has the beautiful characteristic of being able to expand enormously and remain expanded.