Surgery and current management for cancer of the esophagus and cardia: Part II

SURGERY AND CURRENT MANAGEMENT FOR CANCER OF THE ESOPHAGUS AND CARDIA: PART II

SURGICAL THERAPY AND CARDIA HISTORY

OF SURGICAL

OF CARCINOMA

OF THE

ESOPHAGUS

THERAPY

Carcinoma of the thoracic esophagus was well described by the early 19th century, but the thought of a transthoracic operation for its removal was stifled for several reasons. First, battle injuries had repeatedly demonstrated the lethal effects that ensued when a gaping hole in the chest resulted in collapse of the lung. As a consequence, surgeons feared to enter the pleural cavity. It was not until the early part of the 20th century that this fear was dispelled by an understanding of how lung expansion could be maintained with an open chest.lo3 Second, surgeons observed that tugging or pinching the vagus nerve in the neck was promptly followed by slowing of the pulse and, in some situations, cardiac arrest. This gave rise to the fear that division of both vagi above the heart would cause instant death.‘04 The third observation was that patients who had escaped death from either injury to the vagi or the consequences of an open chest died from disruption of the esophageal anastomosis and subsequent infection of the pleural cavity. This gave rise to the concern that an intrathoracic anastomosis involving the esophagus was a potential source of great danger.‘“4 The first successful resection of a carcinoma of the thoracic esophagus was performed by Franz Torek in 1913. General anesthesia was administered by a new technique: the tracheal insuftlation of ether. The existing technique of a differential pressure chamber could not be used because the rubber cuff placed around the patient’s neck to separate the atmosphere about the head from that about the body would preclude the construction of a cervical esophagostomy. Torek avoided injury to the vagi and the possibility of sudden death by carefully dissecting them off the esophagus. Pleural infection from an esophageal leak was circumvented by closing the Cur-r

Probl

Surg.

August

1988

541

cardia and performing a cervical esophagostomy, thereby avoiding an intrathoracic anastomosis. Torek’s patient recovered and survived for another 13 years with continuity between the cervical esophagostomy and gastrostomy established via an external ‘rubber tube.” This allowed the patient to swallow all varieties of food provided it was well chewed into a semiliquid state. The successful establishment of normal alimentation via an esophagogastrostomy after an esophagectomy remained an unattainable goal until Ohsawa’sXo5 successful resection of eight patients with carcinoma of the lower esophagus and cardia reported in the Japanese literature in 1933. A similar procedure in one patient was reported by Marshall in the United States in 1937.‘06 No followup is available on Ohsawa’s patients. Marshall’s patient was reported to be plagued by persistent esophageal obstruction and esophagitis, which required repetitive dilatation. Adams and Phemister, from the University of Chicago, also realized the difficulty in constructing a dependable intrathoracic esophagogastric anastomosis and took the project to the laboratory. Only after a high degree of success was attained in dogs was a similar procedure applied to a patient with carcinoma of the thoracic esophagus. Their report, presented on April 5, 1938, before the Twenty-First Annual Meeting of the American Association for Thoracic Surgery in Atlanta, popularized the one-stage resection of thoracic esophageal cancer and intrathoracic esophagogastrostomy.“’ PREOPERATIVE MANAGEMENT

EVALUATION

AND PERIOPERATIVE

Proper preoperative evaluation and perioperative management of the patient with carcinoma of the esophagus is as important to the reduction of operative mortality as technical expertise. Careful selection of the candidate, judicious use of supportive measures, and a rational choice of the operative procedure can reduce mortality.1o8 Physiologic Assessment Prior to proceeding with surgical therapy for carcinoma of the esophagus, it is necessary to confirm that the patient is able to tolerate the operation. The physiologic status of the patient will affect the extent of the surgery. It is futile to select an operation that is aimed at increasing the long-term survival for a patient whose physiologic life expectancy is short. Carcinoma of the esophagus is predominantly a disease of men between the ages of 50 and 7O.l” As a result, the presence of additional chronic illnesses, such as chronic obstructive lung disease or ischemic heart disease, is the rule rather than the exception. It is 642

Curr

Probl

Surg,

August

1988

important that the patient have sufficient cardiopulmonary reserve to tolerate the operation. The respiratory function is best assessed with the FEV,, which should be 2 L or more. Any patient with an FEV, of less than 1 L is a poor surgical candidate for two reasons; first, because he is unlikely to survive the operation, and second, because if he does, his life expectancy is short due to his lung disease (Fig ll).“’ Clinical evaluation and electrocardiogram are not sufficient indicators of the cardiac reserve. The gated radionucleotide pool scan is noninvasive and provides accurate information on

l

FEVl ’ 1.25 liters

n

FEVl 2 0.75 but 5 1.25 liters

A Fell

80

<

0.75

bk?rs

4

survival

60

k

-r

0

4.0

8.0

.---~l

12.0

16.0

YEARS OF OBSERVATION FIG 11. Survival of patrent groups distinguished on the basts of their FEV, (From Dlener CF, Burrows B: Further observations on the course and prognosis of chronic obstructive lung disease Am Rev Resp/r DLS 1975 111. :I 9 724 Used by permlsston ) Curr

Probl

Surg,

August

1988

543

wall motion and ejection fraction. If the latter is below 40% or decreases on exercise, a coronary arteriogram and ventriculogram may be indicated. The use of the scan as a preoperative screening tool has resulted in a significant reduction of operative mortality in patients undergoing major vascular reconstructionsl” In this regard, it is interesting to note that the ejection fraction at rest remains relatively constant with advancing age.“’ Therefore, a resting ejection fraction of less than 40% is an ominous sign. We would not advocate an extensive en bloc resection in such a patient, regardless of how favorable his pathology appeared. A substantial number of esophagectomies are performed on elderly patients. It is therefore pertinent to assess the effect of age on surgical risk. Advanced age is associated with decreased overall performance, regardless of the presence or absence of disease. In a study of marathon runners, who obviously have a high cardiopulmonary reserve, Stones and Kozma found a rapidly decreasing performance after the age of 70.113 This decreased physical performance is manifested in increased operative mortality. Figure 12 is adopted from a study performed by Sikes and Detmer on 15,930 surgical cases, including both elective and emergency operations.“” The graph demonstrates the effect of age on procedure, adjusted mortal-

10 86-

O-64

70-74 65-69

80-84 75-79

85-89

AGE INTERVAL (years) FIG 12. The relatIonship between age and procedure-adjusted mortality Detmer DE: WLS Med J 1979, 78:27-30 Used by permission )

rate.

544

Probl

Cur-r

(From

Surg,

Sikes

August

ED Jr,

1988

ity. There is a steady increase in surgical mortality with advancing age and a precipitous rise in mortality over the age of 75. Increased risks may be justified if they are outweighed by the expected benefits. Thus, it is necessary to consider the overall life expectancy of this age group of patients. Since the turn of the century, the average life expectancy from birth has almost doubled, going from 47 years at 1900, to almost 75 years in the 1980s. Although these figures are impressive, they are largely the result of advances in the elimination of acute disease and infant mortality. The maximum life span has not changed.*15 There has been no increase in the number of centagenerians or the maximum age at which death occurs in the past 150 years. From actuarial data of the federal government, a maximum average life span of somewhat less than 85 years can be calculated. This number corresponds with the experimental results of Heyflick,“’ who calculated a theoretical maximum life span of less than 90 years based on the observation that human fibroblasts are capable of a finite number of divisions in tissue culture. Excluding trauma, suicide, and miscellaneous uncommon conditions, the majority of deaths over the age of 75 are due to cancer, stroke, or heart disease; and since man must die, reducing his chance of death from a cancer in the esophagus will only increase his chance of death from heart disease or stroke.‘17 In other words, curing a 75-year-old patient of cancer will only change the cause of death, but not the eventual outcome. As a result, the goal of surgical intervention at an advanced age is to palliate and “add life to years, not years to life.” On the basis of this analysis we have concluded that after the age of 75 an en bloc resection for cure of carcinoma of the esophagus is unwise because of the additional risk and reduced benefits. A palliative resection, however, besides having a small chance of cure, provides palliation with less surgery and is advocated for patients ovei 75, regardless how favorable their pathology appears.

Perioperative

Supportive

Measures

Supportive measures are performed to improve the ability of the patient to tolerate the operation and to sustain him in the postoperative period. Patients with mild congestive failure can be improved to some extent with vigorous medical management. Likewise, cessation of smoking, aggressive bronchopulmonary toilet, and bronchodilators may improve the FEV, of some patients. Patients with chronic lung disease do better if their operations are scheduled for the afternoon, thus allowing them to ambulate and cough up secretions that have accumulated in the lung overnight. Patients undergoing esophageal resection are prone to developing postoperative respiratory failure mainly from interstitial pulmonary edema. Following surgical removal of the mediastinal hmphatics Cur-r

Probl

SW-~

August

1988

54.5

and nodes, lymph clearance of both lungs is compromised.118 The lungs are supplied with a rich network of lyrnphatics that drain centrally toward the hilum. The direction of the flow is maintained by a series of strategically placed valves.‘1s The disruption of these lymphatic channels, as occurs when the middle mediastinal nodes are resected, leads to accumulation of interstitial lung water, which reduces alveolar volume and increases airway resistance. This phenomenon is manifested clinically by tachypnea, increased work of breathing, and eventually, respiratory failure. Rales may or may not be present, because the edema is mostly interstitial. Poor nutritional status may potentiate the problem. Guyton and Lindseyl” demonstrated experimentally that if the serum proteins are normal, the left atrial pressure has to exceed 24 mmHg before transudation into the alveoli develops. The critical left atrial pressure drops to 11 mmHg when the serum proteins are low. As a consequence, low left atria1 pressures (estimated by the pulmonary artery wedge pressure) must be maintained during the postoperative period. This goal is achieved by reducing the amount of parenteral fluid administered during the operation and in the postoperative period. If the serum albumin is low, colloids should be given to increase the critical left atria1 pressure at which transudation of fluid into the lung occurs. Since the predominant symptom of esophageal carcinoma is dysphagia, the nutritional status of the patient is of paramount importance in determining the outcome.lo” Low serum proteins have a deleterious effect on the cardiovascular system, and a poor nutritional status affects the host resistance to infection and the rate of anastomotic and wound healing.‘“’ The simplest way to assess the nutritional status of the patient is to measure the serum albumin prior to any hydration. A value below 3.4 gm/dl indicates poor caloric intake and an increased risk of surgical complications, including anastomotic breakdowns.‘Z2 Nutritional support can be provided in several ways. Oral intake is usually inadequate for the majority of esophageal carcinoma patients, and passage of a nasogastric tube can be difficult. The use of the gut for alimentation has several advantages over the intravenous route. These include better utilization of nutrients requiring a lower caloric intake”“; decreased incidence of metabolic, septic, and thrombotic complications, a tenfold decrease of cost per patientlz4; and ease in performing in outpatients. In our experience, a feeding jejunostomy tube provides the most reliable and safest method for nutritional support in patients with esophageal carcinoma who cannot consume an oral diet and who have a functionally normal small bowel. A gastrostomy is inadvisable for these patients because it may interfere with the use of the stomach for reconstruction. The jejunostomy permits nutritional support early in the postoperative pe646

Cur-r

Probl

Surg,

Au@&

1988

riod and minimizes the danger of regurgitation into the esophagus with possible aspiration when using a nasogastric feeding tube. The so-called “Witzel jejunostomy,” which employs a 1.2 mm tube placed through a serosal tunnel, was never very popular due to serious and frequent complications, most notably intraperitoneal leaks, kinking of the bowel, and intestinal obstruction. These complications were eliminated by the development of the intramural needle catheter technique described by Delaney et al.,lzS who used a 14-gauge needle and catheter from a central vein catheterization set. The only problem with this technique is the small diameter of the tube frequently leads to clogging and sluggish flow. Therefore, the choice of diet is restricted to a low viscosity elemental diet. We prefer a different commercial kit (Intestafix, Braun Melsungen AG, West Germany], which contains two breakaway needles and a flexible 12 French catheter. The larger lumen allows for the use of a more viscous formulae at a faster rate, and clogging is less frequent. The tube is somewhat stiffer, which enables easy replacement through the established tract should the tube become dislodged. Maintenance is simple and patients can easily take care of the catheter and the apparatus at home. In severely malnourished patients, the catheter is placed as a separate procedure to allow for preoperative nutritional support. Catheter feedings are continued while the patient is investigated, thus saving valuable time. In this case, the abdomen is entered through a small supraumbilical midline incision. Otherwise, the jejunostomy is placed at the time of the esophageal resection. The kit includes two breakaway needles. The shorter one is used to pass the catheter through the skin; the longer to create the intramural tunnel. The surgeon selects a loop of jejunum, about 25 cm from the ligament of Treitz, and places a purse-string suture on the antimesenteric side. To create the intramural antireflux tunnel, the serosa is pierced, the needle is held steady, and the wall of the bowel is secured over it. The tip of the needle should be visualized through the translucent serosa as the wall of the gut is pulled over the shaft. The length of the tunnel should be 12 to 15 cm, at which point the needle is angled toward the lumen to pierce the mucosa [Fig 131. The catheter is threaded through the needle into the lumen for a distance of 25 to 30 cm. The needle is split and removed and the purse-string is tied down We make it a point to verify the intraluminal position of the catheter by occluding the distal bowel and irrigating the catheter with saline. Next, the loop of jejunum is anchored to the parietal peritoneum and the transversalis fascia with four silk sutures placed circumferentially around the catheter. Finally, the catheter is secured to the skin with 3-O stainless steel wire (Fig 14). We prefer wire for this purpose because it is nonreacCur-r

Probl

Surf

Au@st

1988

547

FIG 13. The technique for signed breakaway

insertion needle.

of a large intramural Sets are commercially

jejunostomy available.

tube

using

a specially

de-

tive, and the sutures should remain for as long as the catheter is in place. At times when the commercial kit was not available, we have used a small gall bladder trocar to create the intramural tunnel. A 10 French infantile feeding tube can be easily passed through the lumen of the trocar. We found this an entirely satisfactory, if less elegant, alternative. Feeding is begun on the third postoperative day. We start with 5% dextrose in water, and gradually advance, using a continuous drip infusion technique, to full strength formula at a rate of 2,400 to 3,000 calories per day. Early in the postoperative period, elemental diet is used (Vital HN, Ross Laboratories, Inc.). As the patient resumes oral intake after surgery, the amount of nutritional support is tapered off. Patients who require nutritional support after discharge from the hospital are issued a portable pump (Ross Laboratories, Inc.) that can be carried on a shoulder strap while the patient goes about his daily activities (Fig 15). None of our patients have had any difficulty with the use of the pump at home over prolonged periods of time. Using this technique, we were able to avoid the use of total parenteral nutrition with its attendant mechanical, thrombotic, and septic complications.126 All our patients were able to gain or maintain their weight while receiving nutritional support. Excessive weight gain occurred in several patients and required reduction of the administration rate. We found that the intramural jejunostomy 54s

Cur-r

Probl

Surg,

August

1988

FIG 14. Method of securing skin of the abdominal

the feeding wall.

jelunostomy

catheter

to the parletal

peritoneum

and

the

described is a safe and effective method for providing nutritional support. It is particularly suitable for esophageal cancer patients because it bypasses the obstruction and avoids violating the stomach. Thus, the stomach remains available for reconstruction, if needed. While the standard needle catheter jejunostomy is acceptable, the larger tube we use is easier to maintain, and prolonged nutritional support at home is well accepted by the patients and their families. THE EFFECT OF TUMOR SURGICAL. PROCEDURE

LOC/4TION

ON

THE

CHOICE

OF

THE

The selection of surgical therapy for patients with carcinoma of the esophagus depends not only on the anatomical stage of the disease and swallowing capacity of the patient, but also on the location of the primary tumor. Tumors in the cervical part of the esophagus, particularly those in the postcricoid area, represent a separate pathological entity in that they are more common in females and the efferent lymphatics from the cervical esophagus drain differently from those of the thoracic esophagus.8X The former drain directly into the paratracheal and deep cervical or internal jugular lymph nodes with minimal flow in a longitudinal direction. Except in adCut-r

Pi-obl

Surg,

Au@st

1988

549

FIG 15. A patient portable ered.

at home after an en bloc esophagogastrectomy pump Partial nutritional support IS provided

with a feedlng jejunostomy until oral allmentation IS fully

and recov-

vanced disease, it is unusual for intrathoracic lymph nodes to be involved. For all practical purposes the tumor is managed as though it were a head and neck tumor. Low cervical lesions that reach the level of the thoracic inlet are usually unresectable due to early invasion of the great vessels and trachea. The length of the esophagus below the cricopharyngeus is insufficient to allow palliative intubation or construction of a proximal anastomosis for a bypass procedure. Palliation of this tumor is very difficult, and patients inflicted with disease at this location have a very poor prognosis. Upper airway obstruction or the development of tracheoesophageal fistulas in such tumors may demand surgical intervention on a palliation basis. Successful operative therapy of 560

Cur-r

Probl

Surg,

August

1988

such tumors requires techniques from several allied specialties, such as thoracic surgery, otolaryngology, and plastic surgery. These tumors usually involve the high retrosternal trachea and larynx and necessitate the removal of both. The division of the trachea in such cases may preclude the possibility of a standard tracheostomy, since the remaining tracheal stump distal to the tumor will not reach the suprasternal notch. This is best managed by the removal of the medial heads of the clavicles and the manubrium down to the sternal angle of Louis. This provides excellent exposure and allows for the construction of a mediastinal tracheostomy. A musculocutaneous flap, consisting of the pectoralis muscle and its overlying skin, can be rotated to provide the extra tissue to bring the skin down to the tracheal stump. A circular incision in the flap can be used as a port through which the tracheal remnant is brought out to the skin.lz7 The close proximity of the upper and middle third of the thoracic esophagus to the trachea and aorta makes it impossible to carry out an en bloc dissection of a carcinoma located in this portion of the esophagus. A true en bloc dissection would require the removal of these vital structures. For this reason, resections of tumors in the upper and middle third of the thoracic esophagus are palliative and amount to little more than local excision of the primary tumor with separate excisions of the regional lymph nodes into which the tumor is likely to drain. Consequently, in this location, only tumors that have not penetrated through the esophageal wall and have not metastasized to the regional lymph nodes are potentially curable. Carcinomas of the lower third of the esophagus and cardia are amenable to an en bloc dissection, as discussed in Part I of this monograph. The regional lymph nodes can also be taken in continuity with a block dissection, making an operation designed according to the principles of surgical oncology applicable to this area of the esophagus. SURGKAL ESOPHAGUS

THERAPY

FOR

CARCINOMA

OF

THE

CERVICAL

It has been estimated that 7% to 10% of primary malignant tumors of the esophagus occur in the cervical portion.‘28 Czerny”29 reported the first successful resection of a carcinoma of the cervical esophagus in 1877. Initially, it was hoped that the prognosis for patients with this disease might be better than for those with carcinoma of the thoracic esophagus. Unfortunately, this has not been proved true. Early experience with resection of the cervical esophagus resulted in a high mortality rate, and reconstruction of the esophagus using neck flaps often required multiple operations.‘30 Because of these complexities and the generally disappointing results, radiotherapy frequently was chosen. Immediate mortality decreased, but Cur-r

Probl

SW&

August

1988

551

control of the tumor was not satisfactory.‘“’ The difference between the two forms of therapy is in the manner in which the disease recurs. Tumors treated initially with radiation therapy tend to recur locally, as well as systemically, and the local disease becomes unmanageable, with erosion into neck vessels and trachea, resulting in hemorrhage and dyspnea. Patients who undergo surgical therapy have few local recurrences provided total excision of the tumor was possible, but they succumb to metastatic disease. Colin13” reported a local failure rate of 80% after definitive radiation therapy; 20% of these patients required palliative surgery in order to control the local disease. Recent improvements in the techniques of immediate esophageal reconstruction have reduced the complications of the surgical treatment and have encouraged a more aggressive surgical approach.133 The data reported by ColinJ3’ suggests that an initial aggressive surgical resection yields longer suIvival than does radiation therapy (Fig 16). However, positive surgical margins, tracheal invasion that cannot be removed, and vocal cord paralysis correlate with a significantly shorter survival following surgery. His data also indicates that palliation was achieved better with esophagectomy

PC.005

,250 THERAPY 0.00

0

1 -----------d!R!!!

I I 12 24 36 48 60 72

I , I I I I I I I I 84 96 108 120 132 144 156 148 180 192 MONTHS

FIG 16. Survival curves or radiotherapy cal esophagus. 552

of patients with carcinoma of the cervical esophagus treated of 5,000 rads or more. (From Colin CF, Spiro RH: Carcinoma Am J Surg 1984; 148:460-466. Used by permission.) Cur-r

Pmbl

Surg,

by surgery of the cervi-

August

1988

and immediate gastric pull-up than with primary radiation therapy or chemotherapy (Fig 17). In general, lesions of the cervical esophagus that are not fixed to the spine, do not invade the vessels, and do not have fixed cervical lymph node metastasis should be resected. If non-fixed lymph node metastases are present, the resection should be considered palliative, since cure at this stage of disease is rare. The larynx is often invaded with microscopic tumor and, in 94% of such cases, a total laryngectomy in combination with esophagectomy is necessary.134 It is our opinion that the trachea should be removed even if gross tumor can not be visualized. A simultaneous en bloc bilateral neck lymph node dissection is performed, sparing the jugular veins on both sides. The thoracic esophagus is removed by blunt dissection

20I-1

SWALLOWING

SATISFACTORILY

m

SWALLOWING

WITH DIFFICULTY

m

UNABLE TO SWALLOW

181614-

1210-

8642-

PRIMARY RT (+ CHEMO)

SURGERY PLUS IMMEDIATE GASTRIC PULL UP

SURGERY PLUS IMMEDIATE LEFT COLON

SURGERY PLUS DELAYED RECONSTRUCTION

FIG 17. Swallowing ability esophagus. (From 1984; 148:460-466. Cur-r

Probl

of patients following Colin CF, Spiro RH. Used by permission.)

SW-~, August

1988

various Carcinoma

therapies for carcinoma of the cervical of the cervical esophagus. Am J Surg

553

through a cervical and upper abdominal incision, and the continuity of the gastrointestinal tract is reestablished by pulling the stomach up through the esophageal bed. A permanent tracheostomy stoma is constructed in the lower flap of the cervical incision. Cervical lesions that are totally unresectable are treated with radiation. If the patient has severe dysphagia, a colon bypass can be attempted with a proximal anastomosis made to the uninvolved piriform sinus and the pharynx. When extensive disease is present in the neck, or when there has been previous radiation therapy, the passage of the transplant through the thoracic inlet may be impossible and the subcutaneous route must be used.

Operative

Technique

The published works of Silver’35 and Akiyama et a1.13’jare excellent guides on the surgical approach to carcinoma of the cervical esophagus and our personal experience is based heavily on their observations. The patient is placed on the operating table in a manner that allows for simultaneous cervical, thoracic, and abdominal incisions (Fig 181. The right hand is placed under the right buttock, and the right arm and forearm are cradled in a sheet along the side of the operating table. The right chest is elevated about 20’ by placing a folded sheet under the right scapula. This position allows for a right anterior thoracotomy to be made should it be necessary. The left arm is positioned alongside the body, and a padded shoulder brace is placed against the left arm to prevent the patient from slipping sideways when the table is rotated to the left to perform a thoracotomy. The table is initially rotated 20“ to the right, placing the patient in a horizontal position. In this position, simultaneous cervical and abdominal incisions can be made for resection of the cervical esophageal carcinoma and blunt dissection of the thoracic esophagus. The cervical esophagus is exposed through a transverse neck incision, and the neck is explored to determine whether the tumor is resectable. The tumor is removed if it or the cervical nodes are not fixed to the prevertebral fascia or adjacent vascular structures, and if the trachea can be divided at a level that will give a tumor-free margin and still allow enough length for a permanent cervical tracheostomy. If this is not possible, a mediastinal tracheostomy should be considered.“’ The pharynx is divided below the level of the hyoid bone, and an appropriate lymph node dissection is done in combination with a laryngoesophagectomy. By performing an extramucosal dissection of the arytenoid cartilage, the mucosa of the larynx can be retained and closed in a manner that will funnel the pharynx down to the opening of the esophageal substitute. This will reduce the height at which the anterior half of the anastomosis must be performed. In preparation for the gastric pull-up, the gastrohepatic ligament 654

Curr

Probl

Surg,

August

1988

FIG 18. The position of the patient on the operating lesion. The position allows for an abdominal. be made wlthout repositioning and redraping

table for resectlon of a cervical esophageal anterolateral thoracic and cervical incision the patlent

to

and the gastrocolic omental mesentery are divided in a manner that preserves the right gastric artery on the lesser curve and the right gastric epiploic vascular arcade along the greater curvature of the stomach. The short gastric vessels are divided, if possible, near the splenic hilum leaving the branches so as to provide collateral circulation along the proximal border of the greater cunrature. The left gastric artery and its veins are divided near the celiac axis. The duodenum is mobilized by a Kocher maneuver (Fig 19). The esophageal hiatus is enlarged by an anterior midline incision up underneath the pericardium to allow the surgeon to place his hand into the posterior mediastinum. The dissection of the thoracic esophagus is done digitally from both the abdominal and cervical incision in the manner described in the section on transhiatal esophagectomy. In order to obtain adequate length of the stomach and prevent ischemia of the fundus, the cardia is encircled with a purse-string Cut-r

Probl

Surg,

August

1988

556

suture, ligated, and divided. The transected cardia is inverted into the stomach in a manner similar to inverting the stump of the appendix when performing an appendectomy. This maneuver preserves intragastric vascular anastomoses and maintains good vascularity to the very tip of the fundus. The prepared stomach can easily be brought into the neck by suturing the fundus into the funnel of an inverted Mousseau-Barbin tube. A bowel bag, which has been divided approximately 3 to 4 in from one end and cut so that one side and its bottom are open, is tied around the funnel so that the stomach is encased in the cellophane. The bag is lubricated with water, which greatly facilitates the movement of the stomach high into the neck without it becoming ensnared in mediastinal structures. Rior to moving the stomach, it is helpful to stretch the stomach wall by placing the muscular stomach under some tension. Care must be taken not to stretch the gastric vessels themselves. When this is done, the stomach usually reaches to the angle of mandible while lying on the anterior chest wall. After passing the stomach through the posterior mediastinum into the neck, a gastropharyngeal anastomosis is performed using a single layer of interrupted 4-O polypropylene sutures.

Gastroduodenal

A.

Lt. Gastroepiploic

Rt. Gastroeplploic

A!

A.

‘\

FIG 19. Preparation of the stomach for pull-up into the chest or neck showing ligation points of the left gastric, splenlc, branches of splenic, and branches of the right gastroepiploic arteries, and the incision for the Kocher maneuver. 666

Curr

Probl

Surg,

August

1988

If the stomach for some reason should not reach the pharynx, a helpful maneuver is to make a “smile” anterior gastric incision that when opened and reflected upward forms a flap to bridge the gap. The flap essentially extends the posterior wall of the stomach, and allows the central portion of the flap can be anastomosed with ease to the posterior pharyngeal tissue. The anterior portion of the anastomosis is completed by sewing the anterior walls of the stomach together along with the lateral portions of the flap, resulting in tubing of the fundus. For higher resections, the procedure can be reversed, giving more length on the anterior wall of the stomach and tacking the posterior wall to the prevertebral fascia. This leaves a raw area in the posterior pharynx that can be covered by pedicle flaps constructed in the mouth, and slid down into the stomach, or the use of local skin flaps. The main advantage of a transhiatal esophagectomy performed at the time of resecting a cervical esophageal tumor is that the entire esophagus is resected. This eliminates the possibility of tumor remaining in the distal esophageal stump, and removes any synchronous lesions in the thoracic esophagus. The completed procedure with a pharyngogastric anastomosis and permanent tracheostomy is shown in Figure 20. Analysis of Results We have performed 14 of these procedures, with one operative death.‘37 Although this procedure involves extensive surgery, it is tolerated better than a thoracic esophagectomy, particularly when associated with laryngectomy. This is probably due to the elimination of pulmonary complications that occur secondary to occult aspiration Nonlethal complications have included one avascular necrosis of the stomach, necessitating its removal, one anastomotic disruption, two tracheal tears, and one mediastinal hemorrhage secondary to injury to the azygos vein. The latter required a thoracotomy to control bleeding. The overall operative mortality reported by four authors is shown in Table 10. Out of a combined group of 84 patients who were TABLE

10.

Transhiatal for ‘Tumors

Esophagectomy of the Cervical

and Gastric Interposition Esophagus and Hypopharynx Operative

Author

No. uf Patients

DeMeester’.” B,&erl:% Kron’“” Kakegawa’.”

14 23

TOtal

Curr

Probl

Surs,

August

1988

Mortality no. ( % 1

17

1 Ii1 3 110) 1 ilii

2:1

1 14.31

84

ti

17) 557

FIG 20. Completed myotomy,

esophagolaryngectomy pharyngogastrostomy,

for and

cervical permanent

esophageal tracheostomy.

carcinoma

showing

pyloro-

treated with transhiatal esophagectomy and gastric interposition for tumors of the cervical esophagus and hypopharynx, the operative mortality was 7%. The most in-depth analysis of the procedure has been published by Kakegawa.‘38 He reported that total laryngectomy, combined with esophagectomy, is necessary in 94% of the patients and that 18% of the patients have intramural skip metastases, emphasizing the importance of total esophagectomy. He found that a transhiatal esophagectomy provided no particular advantage over a transthoracic one, except that the former could be done with the expectation of a lower operative mortality. His five-year survival of 23 patients resected with a concomitant transhiatal dissection was 22%, compared to 17% of 29 patients treated with a concomitant transthoracic esophagectomy.

668

Curr

Probl

Surg,

August

1988

SURGICAL ESOPHAGUS

THERAPY FOR AND CARDIA

CARCINOM4

OF

THE

THORACIC

The surgical therapeutic possibilities for a patient with a cancer of the thoracic esophagus include a curative resection, a palliative resection, or a bypass of an unresectable lesion causing dysphagia. A curative procedure is performed according to the principles of an en bloc resection in continuity with the regional lymph nodes. It is attempted in patients whose tumors are located in the lower third or cardia and do not extend grossly through the wall of the esophagus, when regional lymph nodes are grossly free of metastases, and when nodes at the margins of the resection, i.e., paratracheal, portal triad, or subpancreatic periaortic, are free of microscopic disease. Tumors that arise within the middle or upper third of the thoracic esophagus lie too close to the trachea and aorta to allow en bloc resection without removal of these vital structures. Consequently, tumors within this area of the thoracic esophagus are curable only if they do not extend histologically through the wall of the esophagus and have five or less regional 1”ymph node metastases. In essence, all procedures performed for tumors at this level are palliative and a cure is a chance phenomenon. However, this does not mean that efforts to remove the adjacent &mph nodes when resecting such tumors should be abandoned. To do so may leave inadvertently unrecognized metastatic disease behind and possibly hamper the patient’s overall survival. The use of a standard or en bloc esophagectomy for tumors located in the lower thoracic esophagus and cardia that are potentially curable varies according to surgeon preference. We prefer the en bloc resection in order to assure removal of all the disease in patients possessing the criteria of a high probability of cure. To proceed with an en bloc dissection, the regional nodes are examined and the tumor is inspected and palpated through the mediastinal pleura. No attempt is made to open the mediastinal pleura and dissect directly on the tumor. If both gross 1~ymph node metastases are present and the tumor grossly extends through the mediastinal pleura, resection for cure is abandoned and a resection for palliation is performed. For patients with lesions of questionable resectability, preoperative surgical evaluation should be done without a thoracotomy by cervical mediastinoscopy, pleuroscopy, and an upper midline laparotomy for exploration of the posterior mediastinum, celiac lymph nodes, and abdominal organs. Patients with clearly unresectable tumors or distant organ metastases have a poor prognosis. Their treatment should consist of insertion of an intraluminal jejunostomy tube for nutritional support and radiation therapy. Palliation by intubation should be done only when the objective assessment of swallowing function so indicates. Curr

Pmbl

Sur
1988

559

Standard Transthoracic Esophagogastrectomy The technique of standard esophagectomy has been influenced by the publications of Sweet,‘(’ Lewis,13” and Belsey.‘“’ Sweet advocated the left posterolateral thoracotomy approach for tumors of the lower esophagus, but this approach is not satisfactory if the malignancy extends cephalad and requires division of the esophagus above the aortic arch. In such situations, the esophagus must be dissected out from behind the aortic arch and subclavian artery, and an esophagogastric anastomosis performed in the apex of the left chest. The anastomosis is the most technically demanding part of the operation and every effort in planning should be made to give maximum exposure for its performance. Lewis performed the operation through separate upper midline abdominal and right thoracotomy incisions. This provides excellent visibility for both the abdominal and thoracic portion of the operation, and the best exposure for performing a high intrathoracic anastomosis. The approach requires two separate operations at the same sitting, with the closure of the abdominal incision and repositioning the patient prior to performing the thoracic portion. FisherI modified Lewis’ approach so that the abdominal and thoracic portions of the operation can be performed at the same time. The thoracic approach is through a right anterolateral incision in the third intercostal space, instead of the standard posterolateral incision. This approach allows for both a laparotomy and a thoracotomy to be performed without repositioning or excessive twisting of the patient. It gives good exposure for performing an anastomosis high within the chest, but makes dissection of the lower third of the esophagus somewhat difficult. Belsey’“’ reported on a technique by which the stomach is brought up through the esophageal hiatus from the right chest without using an abdominal incision. The gastric vessels are ligated sequentially as the stomach is pulled up through the hiatus. The drawback of this approach is that it does not allow for an adequate dissection of the abdominal lymph nodes. Operative Technique.-We prefer the Lewis’“’ or Fisher,141 approach in which the abdominal dissection is done initially through an upper midline incision and the esophagectomy through a right posterolateral or anterolateral thoracotomy. Gastrointestinal continuity is reestablished by pulling up the previously prepared stomach through the hiatus and anastomosing it to the esophagus high in the apex of the right chest. To do so, the right gastric and gastric epiploic arteries are preserved, and the stomach is freed from the greater omentum and spleen. The short gastric vessels are divided close to the splenic hilum, preserving, as much as possible, the anastomotic connections between the vessels along the upper third of the greater curvature of the stomach. Although a pulse may not be 860

Cur-r

Probl

Surg,

August

1988

felt in these vessels, they are important in maintaining gastric fundic blood supply. The left gastric artery is divided near its origin from the celiac axis so that the associated lymph nodes are removed with the surgical specimen. Akiyama*42 has shown that the incidence of metastases to nodes adjacent to the branches of the left gastric artery decreases with each successive branch along the lesser curve. To avoid transplanting involved nodes with the stomach into the thorax, the mesentery along the lesser curvature should be cleaned down to the level of the fourth branch (Fig 21). If this is not done, progression of nodal disease can interfere with an effective palliation by causing recurrent disease within the mediastinum, leading to painful infiltration of the spine, or external compression and obstruction of the esophagogastric anastomosis. In order to obtain adequate length of the stomach and prevent ischemia of the fundus, the stomach is divided just on the gastric side of the gastroesophageal junction. For this purpose, a gastrointestinal anastomotic stapler is used and the staple line is oversewn

FIG 21. The incidence of nodal metastases along the branches of the left gastric on Aklyama H. Curr Rob/ Surg 1980, 17.85 Used by permIssIon )

artery.

(Based

with a continuous suture to prevent tearing of the closure when stretching the stomach to reach high in the neck, should that be necessary. This can be difficult for tumors of the lower esophagus and cardia since a sufficient margin must be taken to prevent recurrence, leaving enough viable stomach to reach high in the chest or up to the neck. An alternative method for tumors higher in the thoracic esophagus is to encircle the cardia with a purse-string suture and invert the transected cardia into the stomach in a manner similar to inverting the stump of an appendix when performing an appendectomy. This allows maximum stretching of the stomach for high anastomoses without the possibility of tearing the stapled closure or inadvertently extending the gastrotomy for the esophageal anastomosis into the suture line of the cardia closure. Surgeons vary as to whether they perform a pyloromyotomy to improve gastric emptying. For those who do not, the occasional experience of performing a pyloromyotomy for gastric stasis when the pylorus is located in the diaphragmatic hiatus will convince them of the merit of this recommendation. The esophagus usually is removed from the posterior mediastinum through a right posterolateral thoracotomy incision. This is started by dividing the azygos arch and entering the mediastinum through a longitudinal incision made anterior to the esophagus and parallel to the posterior margin of the trachea, hilum, and pericardium down to the diaphragm. The esophagus, along with as much mediastinal areolar tissue as is comfortable, is dissected out. The subcarinal nodes are also taken. The prepared stomach is brought up through the hiatus to the apex of the right chest or, if using the Fisher approach, into the neck, depending upon the level of esophageal transection necessary. To perform the anastomosis in the chest, the stomach is anchored by suturing the lesser curvature to the prevertebral fascia (Fig 221. Care is taken to avoid twisting the stomach clockwise in order to suture the lesser curve to the fascia. When mobilized properly, the stomach at the completion of the procedure will have been rotated 90’ counterclockwise, with the greater curvature moving from its original 3-o’clock position with respect to the hiatus to the l&o’clock position. It is only during the construction of the intrathoracic esophagogastric anastomosis that the stomach is temporarily rotated 180” in a counterclockwise direction. With the stomach in this position, a site for the esophagogastric anastomosis is selected on its original posterior wall. The gastric incision should be only 1.5 cm long and made perpendicular to the greater curvature (see Fig 221. It should not extend into or be parallel to the suture line used to close the cardia. The esophagus is divided obliquely, with the anterior wall cut more distal than the posterior wall. The anastomosis is done with interrupted single-layer 4-O Prolene sutures. The superior border of the anastomosis is performed 562

Cur-r

Pmbl

Surg,

August

1988

FIG 22. ReconstructIon of gastrolntestlnal contlnulty followlng a transthoraclc esophagectomy. The stomach IS suspended in the chest by suturing the lesser curvature to the right prevertebra1 fascia The broken line shows the position of the gastric tncislon and esophageal transection for the esophagogastrlc anastomosis

first, using the posterior wall of the esophagus IFig 23,A4). The anterior esophageal wall forms a small flap because of the oblique cut and is the last to be sutured. All sutures are tied within the lumen, with the exception of the last four where a modified Gambi stitch is used (Fig 23,BJ. Prior to completion of the anastomosis, a nasogastric tube is advanced into the stomach down to the level of the pylorus. When completed, the greater curvature of the stomach is rotated clockwise 90’ and sutured along the mediastinal pleura (Fig 241. This places the complete anastomosis within the mediastinum. If tumor is present in the cut margin of the esophagus on trozen section, the stomach is pulled up into the neck through a separate incision along the mediastinal border of the left sternocleidomastoid muscle and the anastomosis is performed at a higher esophageal level. The decision should be made prior to anchoring the stomach to the prevertebral fascia or making an incision in the stomach for

FIG 23. A, completion of the posterior portion of the esophagogastric anastomosis showing the flap formed by the oblique transection of the esophagus. B, completion of the esophagogastric anastomosis using three or four modified Gambi stitches to complete the anterior row. The previously placed sutures are tied with knots on the luminal surface.

Greater

Pleura

FIG 24. The stomach tlnal pleura, 564

is rotated 90” clockwise burying the anastomosls

and the greater curvature in the medlastinum. Cur-r

IS sutured

Probl

Surg,

to the medias-

August

1988

the esophageal anastomosis. The neck incision can be made without repositioning the patient if the operation has been performed through a right anterolateral thoracotomy, as recommended by Fisher. If performed through a standard posterolateral thoracotomy, the stomach should be secured in the thoracic inlet, the thoracotomy closed, the patient repositioned, and a neck incision made. The stomach is pulled up into the neck, anchored to the prevertebral cervical fascia, and the cervical esophagus anastomosed to its anterior wall. Analysis of Results.---The results of data on survival of transthoracic esophagogastrectomy for carcinoma of the esophagus are difficult to interpret because most reports do not identifjr whether the operation was done for cure or palliation, do not stratiQ their SUPviva1 data as to the esophageal level involved with tumor, and mix adenocarcinoma of the cardia and squamous cell carcinoma of the body in their survival data. Table 11 shows results from reports with sufficient patient detail from senior authors with extensive experience in the management of this disease. A curative operation was defined as one with no evidence of gross tumor remaining in the

chest or abdomen following the resection. The results indicate that operative mortality decreases as the position of the tumor descends down the esophagus, Five-year survival tends to be least at the extremes of the esophagus, where the extent of resection is limited proximally by the larynx and distally by the amount of stomach needed to reestablish gastrointestinal continuity. Transhiatal Esophagogastrectomy Transhiatal esophagectomy was introduced by Turner,‘4” a British surgeon, in 1927. Its use was short-lived after general endotracheal anesthesia became popular and a transthoracic esophagectomy was feasible.147 Akiyama’36 repopularized the operation in 1975 as a means of removing the thoracic esophagus in patients with pharyngeal or cervical esophageal carcinomas. Patients with upper or mid-thoracic esophageal tumors and bronchoscopic evidence of a tracheobronchial invasion are not candidates for a transhiatal esophagectomy. Similarly, if on exploration the tumor is fixed to the aorta, pericardium, or the tracheobronchial tree, it is unwise to proceed with a transhiatal esophagectomy. In performing the transhiatal esophagectomy, the surgeon must be prepared to open the thorax and to resect the esophagus if the transhiatal approach becomes too dangerous and is aborted, or if complications occur during the transhiatal dissection. Transhiatal esophagectomy was popularized in 1984 by Orringer”” for the resection of esophageal neoplasms. Based on his experience, there are at present few indications for opening the thorax in patients requiring an esophageal resection for malignant disease. Operative Technique.-The published work of Orringer14s is an excellent guide on the transhiatal resection, and our personal experience is heavily based on his work. The patient is placed on the operating table in the manner described for resection of a cervical esophageal cancer, i.e., the right chest is elevated 20” and the right hand placed under the right buttock in order to have access to the right chest through an anterolateral thoracotomy, should that be necessary (see Fig 18). A double lumen endotracheal tube is used so that should the chest need to be entered, one lung can be collapsed to facilitate the exposure in the chest. The abdomen is entered through the upper midline incision. The surgeon’s hand is inserted into the mediastinum through the diaphragmatic hiatus and grasps the tumor-containing portion of the esophagus to determine if it is fixed to the paravertebral fascia, pericardium, aorta, or tracheobronchial tree. Such fixation excludes resection by this route. Once it has been determined that the esophagus is mobile enough to be resected through the hiatus, the stomach is prepared as a substitute for the esophagus in the manner 566

Curr

Probi

Surg,

Au@wt

1988

described for the resection of cervical esophageal tumors. If the tumor is at the gastroesophageal junction, the surgeon should proceed with the resection only if he is satisfied that there is sufficient stomach available to allow an adequate margin distal to the tumor with enough greater curvature to reach the neck. After the stomach has been completely mobilized, the esophagogastric junction is encircled with a rubber drain. Downward traction on this drain by one hand tenses the esophagus as the other hand is inserted through the diaphragmatic hiatus and blunt gentle mobilization of the lower 10 cm of the esophagus from the mediastinum is carried out. When the esophageal tumor does not involve the distal esophagus, and after manual assessment of the tumorcontaining esophagus through the diaphragmatic hiatus reveals a resectable lesion, the esophagus, just above the esophagogastric junction, is divided with a GI stapler and the lower end of the esophagus is grasped with a serrated bronchial clamp. The clamp, rather than the stomach, is then used for subsequent traction on the esophagus to minimize trauma to the stomach that will subsequently be used to replace the esophagus. A purse-string suture is placed closely around the base of the cardia, and the gastroesophageal junction is suture-ligated and inverted into the stomach. After 10 cm of distal esophagus have been mobilized, attention is turned to the neck. A 7 cm incision is made along the anterior border of the left sternocleidomastoid muscle, starting at the suprasternal notch. The sternohyoid and sternothyroid muscles are identified and divided at their sternal origin. This gives excellent exposure into the base of the neck. The carotid sheath and its contents are retracted laterally, and the thyroid, larynx, and trachea are retracted medially. The recurrent laryngeal nerve is identified and protected. Care should be taken not to place a retractor directly on the nerve. The middle thyroid vein and inferior thyroid artery must also be divided. A small indentation can be seen between the trachea and the esophagus just below the left recurrent laryngeal nerve. The dissection is begun in this area, with the scissors directed between the esophagus and trachea in a caudal direction. This is done so that the tip of the scissors reaches a point approximately 3 cm to 4 cm lower on the right side than on the left of the esophagus. This is to avoid injury to the right recurrent nerve which lies lateral to the esophagus at this point. The cervical esophagus is mobilized in this plane circumferentially and encircled with a rubber drain. Upward traction is exerted on the drain and blunt dissection of the upper esophagus from the posterior surface of the trachea is carried out. A finger should be kept in the midline and placed against the esophagus at all times. The cervical esophagus is divided and a rubber

drain is sutured to the distal end of the divided esophagus with heavy silk and used for traction. The transhiatal dissection is then performed, both from the neck and abdomen. The abdominal dissection is facilitated by enlarging the hiatus with a 2 cm incision made in the diaphragm anteriorly under the pericardium. Downward traction on the caudal esophagus is maintained by grasping the bronchial clamp with one hand as the opposite hand is inserted behind the esophagus and progressively advanced into the chest, sweeping away the loose areolar and periesophageal tissues and developing the prevertebral space to the level of the carina. The dissection is continued in the neck by upward traction on the rubber drain sutured to the proximal end of the esophagus to be resected. The surgeon introduces his index and middle fingers through the neck incision along the paravertebral fascia and develops a paravertebral space. A clamp grasping a Kitner sponge dissector is inserted into the superior mediastinum through the cervical incision facilitates the dissection. The esophagus is swept away from the paravertebral fascia from above until the Kitner makes contact with the surgeon’s hand inserted from below through the diaphragmatic hiatus. This completes the mobilization of the posterior esophagus from the prevertebral fascia. Blood pressure should be monitored during this maneuver because intermittent hypotension can occur from cardiac compression by the surgeon’s abdominal hand. The anterior dissection is performed as a mirror image of the posterior mobilization. The caudal end of the esophagus is retracted downward, and the opposite hand is inserted palm down through the diaphragmatic hiatus. The esophagus is swept away from the mediastinal structures by applying posterior pressure. To avoid injury to the posterior membranous trachea, the fingers and then a Kitner sponge dissector are inserted through the cervical incision anterior to the esophagus and behind the trachea until contact is made with a hand inserted from below. Anterior mobilization of the esophagus is then completed, leaving only the lateral esophageal attachments undivided. Lateral mobilization of the upper 5 cm to 8 cm and the lower 8 cm to 10 cm of the intrathoracic esophagus can be achieved under direct vision through the cervical and abdominal incisions. To mobilize the remaining portion of the esophagus, the right hand is inserted through the diaphragmatic hiatus anterior to the esophagus and up into the superior mediastinum behind the trachea until the index and middle fingers can feel the circumferentially mobilized upper esophagus. The esophagus is trapped between the index and middle fingers, which are pressed posteriorly against the prevertebral fascia as a downward raking motion of the hand evulses any small remaining periesophageal attachments. 668

Curr

Probl

Surg,

Au@wt

1988

At times, dense fibrotic attachments in and around the carina can prevent complete dissection as described. In this situation, the entire intrathoracic esophagus can be mobilized, with the exception of a 1 cm to 2 cm segment in the subcarinal area. To complete the dissection, the mobilized upper esophagus and its attached rubber drain are delivered down into the abdomen through the diaphragmatic hiatus. The surgeon can then retract on both rubber drains, horseshoeing the esophagus. Usually this will expose the residual bands holding the midportion of the esophagus to allow them to be cut under direct vision. This maneuver, however, generally is not necessary. After complete mobilization, the intrathoracic esophagus is delivered out of the cervical or abdominal incision. If the stomach is to be used for the reconstruction, the tip of the fundus that reaches most cephalad is identified and sutured to the side of an inverted funnel of a Mosseau-Barbin tube. The stomach is then wrapped in a bowel bag that has been cut to size and lubricated with saline. The tube is passed through the posterior mediastinum and up into the neck, pulling the stomach behind it. Very little traction is required when using these aids. Traction is placed on the cellophane bowel bag rather than the stomach itself. Once in the neck, the gastric fundus is suspended to the prevertebral fascia with 3-O polypropylene sutures and the cervical esophagus is anastomosed to the anterior wall of the stomach in the manner described for the transthoracic esophagectomy. The edge of the diaphragmatic hiatus is sutured to the gastric wall in several locations to avoid subsequent intrathoracic herniation of abdominal viscera. Prior to pulling the stomach up into the neck, the limbs of two Jackson-Pratt catheters are drawn into the posterior mediastinum through the cervical incision and out the esophageal hiatus. With the stomach in place, the catheters are positioned so that a portion of the drains extends through the esophageal hiatus into the abdomen. They are brought out through a stab incision in the anterior abdominal wall and are used to drain the posterior mediastinum, subphrenic area, and chest cavity, should that be necessary. A nasogastric tube is used to decompress the intrathoracic stomach and is passed across the anastomosis at the time of its construction.

Analysis of Results.- Complications of transhiatal esophagectomy include pneumothorax, tracheal tear, hemorrhage, hoarseness from recurrent nerve injury, anastomotic disruption, chylothorax, and sympathetic pleural effusion. The most common intraoperative complication is entry into one or both pleural cavities during the mediastinal dissection. A tear of the posterior membranous trachea during the dissection can be disastrous, and management of this situation is greatly facilitated with the use of a double lumen tube. It is advisable to do an anterolateral right thoracotomy and repair Curr

Probl

Surg,

August

1988

569

the tear directly. Exposure of the tear through this incision is excellent if ventilation to the right lung can be interrupted. Major intraoperative bleeding is an exception rather than the rule; if excessive, it is usually due to damage to the azygos vein and requires a thoracotomy to control. Data on long-term survival of patients with carcinoma of the esophagus who have undergone transhiatal esophagectomy is not yet complete. Thus, no conclusions can be made by comparing the current data to that reported for standard or en bloc transthoracic esophagectomy. Even when the data is complete, comparison will be difficult because the indication for surgery in the transhiatal group is only palliation and cure, if achieved, is a chance phenomenon. Consequently, patients are not identified as having a curative operation, i.e., no evidence of gross tumor remaining in the chest or abdomen following the resection. Table 12 shows results from reports with sufficient patient detail from senior authors who have had significant experience with the procedure. The operative mortality, compared to that from a curative standard thoracic resection, is lower. This, however, has not been supported by retrospective comparative studies.77B 78 Some authors imply that an en bloc resection of carcinomas in the lower esophagus and cardia can be done through the transhiatal approach.14’ Whether this is so will require comparison of surgical specimens obtained by transhiatal and transthoracic approaches and the long-term survival achieved with the two techniques. It is unlikely that a randomized prospective study will be or could be done to answer the question. En Bloc Resection for Tumors of the Lower Esophagus and Cardia A standard esophagectomy consists of resecting the esophagus for upper or middle third tumors and a portion of the stomach, in adTABLE

12.

Transhiatal

Esophagectomy Operative

Level Upper

Author third

OrringeP

Patient

No.

Mortality, No. (W)

7

0 101

‘2%Actuarial

Survival

Middle

third

On-ingersz Baker133 Total

45 9 54

5(11) 0 (0) 5 191

17 (3~J

Lower and

third cardia

Or-ringers2 Finley’@ Bake?” Total

48 34 11 93

1 1 0 2

31 13yr1

570

La (31 101 (2) Cur-r

Probl

Suq,

August

1988

dition to the esophagus for lower third and cardiac tumors. The immediate adjacent lymph nodes are also removed. When all gross tumor has been removed, the procedure is considered to have been done for cure, and is associated with an overall 8% to 22% five-year survival rate (see Table 11). A criticism of the procedure and an explanation for such a poor survival in patients resected for cure is that the operation, as currently performed, does not apply the principles of en bloc resection for the removal of a neoplasm as is done elsewhere in the alimentary tract. The anatomical relationship of the upper and middle third of the esophagus to vital structures precludes an en bloc resection for tumors at these levels. Anatomically, it is applicable only to tumors in the lower third of the esophagus and cardia. In 1963 Logan15” reported his experience with en bloc resection for carcinoma of the cardia and lower third of the esophagus. He thought that to neglect the principles of an en bloc resection was a resignation to doing under direct vision the same operation Gre.y Turner had done blindly, namely transhiatal esophagectomy.146 In fact, if one rejected the principles of an en bloc resection of the lower esophagus and cardia, there is little argument for doing any other than a transhiatal resection. Employing the en bloc technique, Logan reported a 16% five-year survival, which was better than other results reported at that time. Logan’s operation was not widely adopted, partly because of the associated 21% operative mortality. Since that time, improvements have been made in the perioperative management of patients following major operations so that more reasonable operative mortality rates can be anticipated. Akiyamaa5 in 1981 and Skinners3 in 1983 revitalized interest in the en bloc resection for neoplasms of the esophagus and cardia. They were able to reduce the operative mortality to 1.4% and ll%, respectively, and Skinner reported a 33% three-year survival for carcinoma of the lower esophagus and cardia. Logan, Akiyama, and Skinner all used the stomach to reestablish gastrointestinal continuity. For carcinomas of the lower esophagus and cardia, this represented the closest margin to the tumor and a potential weakness of the en bloc resection. After gaining experience with the techniques of Logan, Akiyama, and Skinner, we made modifications that were thought to comply more faithfully with the principles of an en bloc resection while providing greater safety for the patient.73 The principles are: (1) an operative approach to the patient to maximize operative exposure while at the same time allowing intraoperative staging of the tumor so that the benefits of the curative resection were only applied to those who had favorable pathology, and (2) using the colon to reestablish gastrointestinal continuity in order to allow for a larger gastric resection. Cur-r

Pmbl

Sur5

August

1988

571

Operative Technique.-We perform the en bloc resection for carcinoma of the distal esophagus and cardia through three incisions and in the following order: right posterolateral thoracotomy, en bloc dissection of the distal esophagus and mobilization of the esophagus above the aortic arch, closure of the thoracotomy, repositioning of the patient in the recumbent position, upper midline abdominal incision, en bloc dissection of the stomach and associated lymph nodes, left neck incision, proximal division of the esophagus, transhiatal removal of the previous en bloc dissected distal esophagus and mobilized proximal esophagus, distal division of the stomach, and reestablishment of gastrointestinal continuity with a left colon interposition. The thoracic portion of the procedure entails an en bloc removal of the distal thoracic esophagus below the aortic arch with its surrounding areolar tissue containing the low paratracheal, tracheobronchial, subcarinal, paraesophageal, and parahiatal lymph nodes; the thoracic duct; the azygos vein down to where it passes into the abdomen on the lateral surface of the vertebra; and a collar of diaphragmatic muscle around the esophageal hiatus (see Fig 10~4 in Part I of this monograph). The block of tissue removed is limited anteriorly by the membranous trachea and pericardium, laterally by the right and left mediastinal pleura, and posteriorly by the intercostal arteries, aorta, and anterior vertebral ligaments. The abdominal portion of the procedure entails an en bloc removal of all the posterior peritoneal periaortic areolar tissue down to the celiac axis and the superior border of the common hepatic artery, the splenic artery and spleen, the greater omentum, and the proximal two thirds of the stomach (see Fig 10,B). The block of tissue includes lymph nodes along the left gastric artery, around the celiac axis, superior to and underneath the common hepatic artery, medial to the portal triad, in the greater omentum, and along the splenic artery down to the celiac axis. This extensive resection is done to incorporate in the surgical specimen all the potentially involved regional lymph nodes and submucosal lymphatics of the stomach and distal esophagus. The pancreas is not removed, but the splenic artery, along with its associated lymph nodes, is dissected off the superior border of the gland. The procedure is started in the right side of the chest with the division of the intercostal branches of the azygos vein from its arch down to where it passes into the abdomen on the lateral surface of the vertebra. The segments of the posterior pleura between the ligated intercostal veins are divided with an incision parallel to the long axis of the spine. The posterior dissection is extended in the direction of the left chest along the intercostal arteries to the aorta and over the anterior surface of the aorta, through the left mediastinal pleura, and into the left pleural cavity. To do so, the intact 672

Cur-r

Pmbl

Surg,

August

1988

azygos vein and its surrounding tissues are retracted anteriorly, which allows the hemiazygos vein(s) to be seen as it crosses over the spine underneath the aorta to join the azygos vein. The vein must be identified, ligated, and divided. The aorta becomes visible when the vein is divided and serves as a guide for the extension of the posterior incision into the left side of the chest. Early division of the azygos vein at its entry into the superior vena cava is avoided because it contributes to venous hypertension in the azygos system and excessive bleeding during the posterior mediastinal dissection. At the caudal end of the posterior pleural incision, where the azygos vein was ligated distally, the thoracic duct is identified, divided, and ligated. Anteriorly, the mediastinum is entered through a longitudinal pleural incision made parallel to the posterior margin of the trachea, hilum, and pericardium down to the diaphragm. The anterior dissection is extended across in the direction of the left chest along the posterior surface of the right main stem bronchus, trachea, left main stem bronchus, and the pericardium anterior to the subcarinal nodes. To do so requires division of the azygos vein at its entry into the superior vena cava. When both the anterior and posterior dissections of the posterior mediastinum are complete, the esophagus, encased in its periareolar tissues containing the paratracheal, subcarinal, paraesophageal, and parahiatal nodes, is pulled into the right thorax and freed by sharp division of a strip of left mediastinal pleura. Care must be taken to avoid damage to the left recurrent nerve near the aortic arch. The nerve can be identified as it comes underneath the aortic arch just above the left main stem bronchus. Its common course is to pass directly to the trachea without redundancy and to lie on the left posterolateral cartilaginous wall as it passes up into the neck. Identifying it underneath the aortic arch allows for mobilization of the proximal esophagus without damage to the nerve. Occasionally it follows the left lateral wall of the esophagus up into the neck. Inferiorly, a collar of diaphragmatic muscle is excised around the esophageal hiatus. Superiorly, the esophagus is bluntly dissected into the neck, but is not divided. No attempt is made to do an en bloc dissection above the level of the aortic arch. Suspicious nodes above the aortic arch are biopsied and, if positive, the en bloc dissection is abandoned for a palliative procedure. When the dissection is complete, the thoracotomy incision is closed with the specimen remaining in the chest, wrapped in a surgical sponge. Next, the patient is moved to the recumbent position. The previously inserted double-lumen endotracheal tube, used for selected deflation of the right lung, is removed and a single-lumen tube is inserted. The anterior neck, chest, and abdomen are prepared and draped, and an upper midline abdominal incision is made. Exposure for the abdominal dissection is facilitated b.v a Weinberg retracCurr

Probl

Surg,

August

1988

573

tor that has been welded to a Balfour handle and attached to an over-arm bar. The abdominal dissection begins with the removal of the greater omentum from the transverse mesocolon and mobilization of the spleen to the midline. This allows access to the left retroperitoneal periaortic areolar tissue that lies just anterior to the aorta. The abdominal dissection begins along the left crus, where the thoracic dissection was discontinued. The excision of a collar of diaphragmatic muscle is continued down the margin of the left crus to the celiac axis. The pancreas is identified, and the splenic artery, along with its vein and associated lymph nodes, is dissected off the superior border of the tail of the gland. The splenic vein is ligated approximately midway down the pancreas, where it turns inferiorly and leaves the artery. Removal of the splenic artery, along with its associated lymph nodes, is continued down to the celiac axis, using the palpation of the pulse as a guide to the dissection. At its origin from the celiac axis, the splenic artery is divided, which allows for the identification of left gastric artery. On the right side, the gastrohepatic ligament is divided along the liver margin up to the esophageal hiatus. Care must be taken not to interrupt the hepatic artery that might be lying in this mesentery. The posterior peritoneal tissue underneath and along the superior border of the common hepatic artery, and the areolar tissue containing lymph nodes along the medial border of the portal triad, are swept toward the celiac axis. Dissection of a collar of diaphragmatic muscle around the esophageal hiatus, which was begun during the thoracic portion of the operation, is continued down the right crus. The dissection of the hiatus is completed with the division of the left gastric artery at its origin from the celiac artery. The esophagus is exposed and divided in the neck through an incision made along the anterior border of the left sternocleidomastoid muscle. Care is taken to identify and protect the left recurrent laryngeal nerve. The surgical specimen is removed from the posterior mediastinum transabdominally, trailed by a long suture tied to the esophageal end of the specimen. Gastrointestinal continuity is reestablished between the proximal esophagus in the neck and the remaining gastric antrum in the abdomen with an isoperistaltic left colon transplant based on the left colic artery and the inferior mesenteric vein (Fig 25). The retention of the antrum and the pyloric valve improves postoperative gastrointestinal function sufficiently to merit salvage. The colon transplant is pulled up through the posterior mediastinum with the aid of an upside-down Mousseau-Barbin tube encased in a trimmed cellophane bowel bag, and using the above mentioned suture as a guide. Of importance is that if the operation has lasted too long, if the patient is unstable, or if the arterial supply or venous drainage of the colon is not satisfactory, then the colon is not divided, the antral 574

Cum

Probl

Surg,

August

1988

FIG 25. ReconstructIon of gastrolntestlnal tract Distal anastomosis IS made to antral esophagus tn neck. (From De Meester peutlc approach to cancer of the lower 1988; 95:43--49 Used by permIssIon )

with left colon InterposItIon after,en bloc resection portton of stomach and proximal anastomosls to TR. Zanlnotto C, Johansson K-E. Selective theraesophagus and cardla J Thorac Cardlovasc Surg

opening of the stomach is closed, an intramural jejunostomy tube is inserted, and a cervical esophagostomy is constructed. The proximal marginal and midcolic artery and vein are divided to increase the vascular@ of the subsequent colon transplant and to avoid the necessity of dissecting the base of the midcolic artery and vein at a later date. The transverse mesocolon should be opened wide and the entire small bowel brought through the opening so that the Cur-r

Prohl

Sorg,

August

1988

575

transverse colon lies under the small bowel low in the abdomen. The transvere colon is sutured to the low anterior abdominal wall to prevent its migration into the upper quadrant and adherence of the transverse mesocolon to the denuded splenic bed. The patient is discharged on jejunostomy tube feedings, and returns in 60 to 90 days for reestablishment of gastrointestinal continuity with the previously delayed isoperistaltic left colon graft through the substernal route. The one-stage operation is preferred because postoperative adhesions and scarring of the transverse mesocolon can limit the length of the colon transplant; but, the reconstruction phase should not be done unless everything is satisfactory. Analysis of Results.--In our opinion, an en bloc dissection of the esophagus is anatomically applicable only to the lower esophagus and cardia, and we have limited the use of the technique to tumors that arise within this location. Patients whose extent of disease does not definitely preclude an attempt at a curative resection and who are physiologically fit are candidates for an en bloc resection. During the thoracic and abdominal dissection, intraoperative staging is done according to the algorithm in Figure 8 in Part I of this monograph. If distant organ metastases are discovered, or obvious tumor extension through the esophageal wall and multiple gross lymph node involvement is present, the en bloc dissection is abandoned and a palliative resection performed, using the stomach to reestablish gastrointestinal continuity. Table 13 shows our experience with this approach in 52 patients with carcinoma of the lower esophagus or cardia. Nineteen patients had advanced or unresectable disease at the time of referral and received only palliative treatment. Six of

TABLE Selected

13. Surgical

Therapy’

Therapy Palliation only No operation Exploration &pass Palliative lesection Standard esophagectonyt Transhiatal esophagectomv Repeat esophagogastrectorny Curative resection by radical Total

No. of Patients 19

9 4

6 19 10 5 4 t?sophago~astlectornv

14

52

‘From De Mmster ‘I‘H. Zanirmtta C;, Johanson K-E: Selective therapeutic appmach to cancer ot the lower esophagus and mdia. J ~kx-nc ~ardiovasc .surs 1988; 95:434Y. Used by Permission t’l’wo patients switched fmm a arative rasr[?ion because of operative findings

576

Cur-r

Probl

Surg,

August

1988

these 19 had dysphagia relieved with a bypass operation, one had an esophageal stint, and the other twelve received radiation treatment or chemotherapy. Palliative resection was performed on another 19 patients: 4 because of recurrent tumor at the anastomosis after a previous esophagogastrectomy for adenocarcinoma of the cardia; 8 who were treated with preoperative chemotherapy because of clear evidence of W2 N2 disease; 3 because of marginal physiological reserve; 2 because they were older than 75 years; and two who had initially been candidates for a curative resection until more extensive disease was discovered during an attempted curative en bloc dissection. Figure 26 shows the actuarial survival curves for the various groups: palliation only, palliative resection, and curative en bloc resection. The 30-day hospital mortality for the group that had en bloc curative resection was 7%. Table 14 shows the postoperative staging classifications of the 14 patients undergoing curative en bloc resections. Only 14% (21141 who were preoperatively and intraoperatively considered to have favorable esophageal disease were judged

0 Curative

n

Resection

Palliative Resection

l 40

N=14

.. \ 1 \

20

-

= L, I.. ‘, : N=19

0

V

1

u---*-----m-g--~ I

I

I

I

2

3

4

5

Years FIG 26. A&anal survival following various selected therapies based on preoperative and Intraoperatlve staging of patients with carclnorna of the lower esophagus and cardia. (From De Meester TR, Zanlnotto C, Johansson K-E. Selective therapeutic approach to cancer of the lower esophagus and cardla J Thorac Cardiovasc Surg 1988: 95.43-49. Used by permlsslon ) Curr

Probl

Surg,

August

t988

577

TABLE

14.

Postouerative

Classification

After

Curative

Favorable

No. of Patients

Less

Favorable

WO NO WI NO

2 1

WO WO Wl Wl

Nl NZ Nl N2

W2 NO W2 Nl Total ‘Intraoperative

3 staging

12/14 correct

Resection* No. of Patients

No. of Patients

Unfavorable

3 1 1

W2 N2

2

1 3 Y

2

186”~ I

unfavorable postoperatively, i.e., the tumor had penetrated through the wall of the esophagus and five lymph nodes or more were involved. As mentioned previously, 2 other patients were discovered to have advanced disease during the operation, and the resection for cure was abandoned. Thus, 4 of 16 patients initially thought to be candidates for curative en bloc resection had unfavorable pathologic conditions, 2 discovered at operation and 2 discovered after histologic examination of the surgical specimen. Overall, preoperative staging had an accuracy of 75%, and the combination of preoperative and intraoperative staging had an accuracy of 86%. Figure 27 shows the relationship of tumor size to the presence of favorable, less favorable, or unfavorable pathologic conditions in the 14 patients having resection for cure. All tumors less than 3 cm in length were classified as favorable. The tumors were 4 cm or less in 93% of the patients undergoing resection for cure. A total of 599 lymph nodes, or 42.7 * 14.2 nodes per patient, were removed by curative resection. Table 8 (in Part 1 of this monograph) shows the prevalence of metastases to the different @mph node groups. Four of the 14 patients who had a curative resection did not have lymph node metastases. Three are currently alive and 1 died of a cause other than cancer. It is our conclusion that this approach allows for the identification of patients with early disease for whom a curative en bloc resection can be performed with low operative mortality and an increased probability of survival.‘” Table 15 shows operative mortality and survival data after en bloc resections performed by other authors. Both Logan and Skinner have attempted to apply the technique of en bloc resection to tumors in the middle third, as well as the lower third and cardia. As previously mentioned, we believe that an en bloc resection is not applicable to tumors in this location because of the close anatomical relationship of the esophagus to vital structures at this level. Tumors in the middle and upper thirds are curable only if they do not extend through 578

Curr

Probl

Surg,

Au,@st

1988

O/O

Favorable

010 Unfavorable

Number of Patients

5 3 1 I

y /

cm FIG 27. Relationshrp of tumor srze to favorable (WO-1 NO), less favorable (WO-1 Nl-2 or W2 NO-l), and unfavorable (W2 N2) pathology In patrents having en bloc resection of carcrnoma of the distal esophagus or cardra (see Table 7 in Part I for stagrng definition) (From De Meester TR, Zaninotto C, Johansson K-E: Selective therapeutrc approach to cancer of the lower esophagus and cardra. J Thorac Cardiovasc Surg 1988; 9543-49. Used by permission )

the wall of the esophagus and involve less than five lymph nodes. Removal of the esophagus at these levels is essentially done by stripping the esophagus out of the mediastinum and removing as many adjacent lymph nodes as is conveniently possible. Under these circumstances, cure is a chance phenomenon and similar to that acTABLE Curative

15. En Bloc

Esophagectomy Operative

L&T

I

Curr

Patient

Authm

Probl

Surg.

August

1988

.No.

Mortality, No.

I% I

% Actuarial

Survival

579

complished by a standard resection elsewhere in the esophagus. In support of this opinion, the survival of patients following an attempted en bloc resection of the middle third of the esophagus is no better than that achieved with a standard resection (see results in Table 11 vs. those in Table 15). This is not so for carcinomas of the lower third and cardia, for which an en bloc dissection appears to give better results. Logan, who was the first to introduce the en bloc concept to esophageal surgery, operated on unselected patients and had a prohibitively high operative mortality rate of 21%. Since that time, improvements have been made in operative management, intensive care, postoperative treatment following major operations, and selection criteria of operative candidates so that a more reasonable mortality rate can be achieved. Indeed, our results and those of Skinner have shown that this operative mortality rate can be reduced by at least one half with a subsequent increase in patient survival. PALLIATIVE ESOPHAGUS

THERAPY FOR AND CAFKDIA

ADVANCED

CARCINOMA

OF THE

The most successful means of palliating an esophageal carcinoma is by resection, since removal of the primary tumor results in fewer problems with dysphagia, hemorrhage, perforation, fistula formation, and pain. Unfortunately, 60% of patients are unsuitable for resection either because of the advanced nature of the tumor or because of general debilitation41 Palliation should be provided for these patients when dysphagia is such that a semi-soft diet cannot be taken (Grade III or greater dysplagia; see Table 6 in Part I of this monograph) or when a respiratory tract fistula develops. The objective should be to provide adequate symptomatic relief with the lowest mortality and shortest hospital stay possible. A variety of therapeutic options exist that can be used alone or in combination. BOUGIENAGE Dysphagia occurs when the esophageal lumen is reduced to less than 12 mm in diameter.151 Simple dilatation of the stricture to 50 French has been shown to provide relief of dysphagia in 92% of patients.15’ Maloney-type rubber, mercury-filled dilators are the safest and easiest to use, but the initial dilatation, especially when the stricture is tight, is best performed using an endoscopically placed guide wire over which a dilator of similar shape, but with a central orifice (Savary), is passed. Fluoroscopy should be used to check the position of the wire prior to dilatation. Several studies have shown that dilatation of malignant strictures 580

Cum

Probl

Surg,

August

1988

is a safe procedure, even in association with a respiratory tract fistula or during radiotherapy. Cassidy et al.‘“” had only three deaths in 154 patients in whom a total of 3,160 dilators were passed before, during, and after radiation therapy. The proximal stomachs of two patients were perforated by guide wires and the third died from bleeding following dilatation of a severe postradiation stricture. Unfortunately, relief of dysphagia is usually short and repeated dilatations are necessary. In one study of 26 patients undergoing radiotherapy, 616 dilatations were necessary to maintain satisfactory relief of dysphagia during a mean survival time of only six months.‘“”

INTUBATION Intubation of malignant esophageal strictures has been used as a means of avoiding repeated bougienage. It was first attempted by the French surgeon Leroy d’Etoilles in 1845. Initially the tubes were passed blindly until 1924, when Souttar developed a tube that could be positioned using a rigid esophagoscope. Subsequent developments by Mousseau and Barbin in 1956 and Celestin in 1959 required that the tube be placed by a traction technique via a gastrotomy.‘54 Recently, there has been a resurgence of interest in endoscopically placed tubes, and in 1977 the Nottingham introducer, which facilitates the peroral passage of tubes, became commercially available .155 Many types of tubes are now commonly used, most being made of polyvinvl with an internal diameter of 10 mm to 12 mm. The proximal end -is funnel-shaped to prevent caudal displacement and to direct food into it, while some also have a distal flange to retard proximal dislodgement. Intubation can be performed either by the pulsion or traction techniques,ls4 and failure to successfully intubate a stricture is comparatively rare. tising a pulsion technique for thoracic tumors and a traction technique for lower esophageal tumors, Angorn failed to successfully insert a tube in only 28 of 1,135 patients.‘“” However, both methods are associated with an appreciable incidence of complications, including bolus obstruction of the tube, perforation of the esophagus, reflux of gastric contents through the tube, obstruction of the tube from distal tumor overgrowth, and, when the traction method is used, complications related to the laparotomy. Displacement of the tube may also be a problem, particularly when the tube is placed prior to irradiation. In general, intubation is not applicable to tumors in the upper third of the esophagus because of the lack of room to seat the funnel below the cricopharyngeus, and may be difficult for strictures of the cardia because of angulation of the lumen. Intubation has been advocated for palliation of respiratory tract fistulae, but the need to Cur-r

/‘rob1

SW-~, Au@st

19X8

581

place the tube in the proximal esophagus close to the upper sphincter often results in poor palliation and a failure to close the fistula. A new tube is available with a cuff specifically designed to occlude a fistula. Hegarty et a1.157 reported postoperative mortality rates of 64.3% for traction intubation and 25% for pulsion intubation when there was an associated fistula. Despite these problems, intubation is a widely used method of palliation and, although there is a 10% incidence of perforation with the endoscopic method,‘58 this technique is favored over the traction technique because of the lowei hospital mortality and shorter hospital stay.‘“’ Nearly all who survive intubation are improved, but only 60% to 95% can manage a semisolid diet and none enjoy totally normal deglutition (Table 16). In many instances, this is explained by the severe anorexia that occurs with advanced disease, as opposed to the inadequacy of the procedure SURGICAL

BYPASS

For many surgeons the results of intubation are inadequate, since they consider that the only acceptable form of palliation in patients who have an appetite is the restoration of the ability to eat and drink normally. In this respect, a surgical bypass is clearly superior to intubation. It is also particularly applicable for those occasional patients in whom a resection was abandoned because of local tumor invasion or who have a malignant fistula, when the disease is locally confined.‘63 In such a situation, an occasional prolonged survival can be achieved with irradiation, during which the patient is able to eat exceptionally well.‘“’ Historically, relief of obstruction was achieved using a cervical stoma and a feeding gastrostomy, but this should be condemned as it provides totally ineffective palliation. A feeding enterostomy, in conjunction with surgical bypass, is often a useful means of supplementing the oral diet, for even though surgery may restore the ability to swallow normally, the patient may eventually lose his appetite and reduce his caloric intake below that required to remain active. In patients who have suffered several complications following attempted resection for cure or palliation, which precludes the thought of further surgery, an extracorporeal tube, which connects a cervical esophagostomy to a gastrostomy, may provide very beneficial palliation.‘“5 Table 17 shows the results of a variety of surgical bypass techniques available using either the colon, jejunum, or stomach via the subcutaneous, substernal, or transpleural routes. The substernal route is preferred as it is farther from the tumor site and less apt to become obstructed from tumor extention. Use of the whole stomach reduces the number of anastomoses needed and, thereby, reduces 582

Curr

Probl

Surg,

August

1988

t&k

=

Angorn’B” Diamentes’“” Lishmanl” LJnruh’62 Watson””

‘T

tnlullation’

‘I‘ P

No. of Patients

YO 1,045 228 98 28 16 49 39 49 32 traction; P = pulsion. to eat semi-solid diet upon discharge

‘Traction

Author

16.

Vs. P&ion

TABLE

20 25 45 23 41

‘1

16 31 25 14 16

P

Mortality

frum hospital

Hospital

I% /

4 3 0

T

Perforation

6 19 8 Y

P

Rate I?+, /

83 96

87 85

80

73 61

P

1% It T

Palliation

17.

gastric Kirschner

Procedure

bypass

of Bypass

Procedures

Reversed gastric bypass Intrathoracic gastric bypass lsoperistaltic gastric tube Substernal colon b,ypass

Substernal Modified

Bypass

A Comparison

TABLE

Orringer’ss Akiyamal” Ongl”’ WonglM Giraud’“” Lam”’ Yamagishi”’ Burdette’7L

Author 37 11 18 142 29 8 15 28

No. 35 18 33 13 17 0 0 0

“43 BTI

24 0 22 42 1’7 38 0 16

w Operative Mortality

100 94 96

25 100 ti4 69

?c suIvi\~ors Able to Eat Normally

the operation time. Gastric tube procedures are prone to complications due to the extensive suture line. Alternatively, jejunum and colon bypasses do not have the reflux problems associated with a gastric bypass, and there is no evidence that the incidence of anastomotic leakage and the overall mortality rate are higher for the coionic bypass. Belsey’73 reported a 1% incidence of significant anastomotic fistulae in a series of 360 left colon reconstructions. Ong’74 also showed that of 167 bypass operations, the anastomotic leakage rate was lowest for the colonic compared to either gastric or jejunal technique. Whichever method is used, it is essential to provide decompression of the esophagus, since it has been demonstrated that motor function persists in the excluded segment.‘7” When the stomach is used, this can be achieved with an external catheter brought out through the neck or by internal drainage in which a cuff of proximal stomach is anastomosed to the jejunum. The use of the reverse whole stomach bypass is a unique technique that retains the integrity of both vagus nerves, and the cardioesophageal junction to drain the excluded esophagus. The procedure is to transsect the duodenum immediately beyond the pylorus, pass the mobilized stomach substernally, and anastomose the prepyloric area to the cervical esophagus.“jgS 1fi9a The reported mortality rate for each procedure varies greatly and is probably related more to the nutritional state of the patient than to the operative procedure. This is supported by the observation that bypass does not seem to carry a higher mortality than surgical intubation, while obtaining a similar rate of effective palliation (see data in Table 16 vs data in Table 171. RALIIOTHERAPY Palliative irradiation can be used either solely or in combination with any of the above methods. Although there is no definition for palliative radiotherapy, it is generally accepted that 4,500 to 4,800 cGy in 20 divided fractions over four weeks is needed to achieve an improvement in swallowing. Wara et a1.176reported that of 103 patients completing a course of irradiation, 11% achieved no palliation, while 66% had an improvement in symptoms which lasted longer than two months. Although some patients will remain euphagic until they die of distant metastases, many will continue to have problems with swallowing. Beatty et al.13* reported that only one third of patients treated with full courses of irradiation did not develop symptoms or clinical signs of recurrent stricture of the esophagus. In nearly all patients who developed dysphagia following irradiation, the cause was recurrent tumor. Although radiotherapy does not have the immediate mortality of intubation or bypass surgery, the lengthy course of the treatment is Cur-r Ptwbl

Surg,

August

1988

686

difficult to justify for those with a limited life expectancy. Consequently, there is a reluctance by many to accept patients with advanced disease. Beatty concludes that patients who present with metastatic disease or a respiratory tract fistula receive minimal benefit from irradiation of the primary lesion. LASER THERAPY In the last ten years medical lasers have received much attention, first for controlling gastrointestinal hemorrhage and, more recently, for the relief of tumor obstruction of the gastrointestinal tract. The neodymium yttrium-aluminum-garnet (Nd-YAG) laser has largely replaced the argon laser, although both can be efficiently delivered down flexible quartz light guides and applied via fiberoptic endos-

COPY.

The procedure is usually performed under intravenous sedation. Fleischer and Kessler17’ originally described a method whereby 1 cm to 2 cm of tumor were treated per session, starting at the proximal tumor margin, with a session being repeated every 48 hours until the full length of the tumor had been covered. In their experience, the mean number of sessions required to alleviate symptoms was 2.8 applied over 5.7 days. More recently there has been a move to use a single session method. The stricture is dilated prior to laser therapy, which begins at the distal margin. Unfortunately, edema commonly limits the amount of tissue that can be treated at one sitting so that often a second treatment session is required.‘78 Experience has shown that however tight the stricture, most patients can be helped by laser therapy, and the procedure is of benefit in controlling a rare hemorrhage from esophageal tumors. The lumen can typically be increased from 2 mm to 4 mm to 13 mm to 16 mm in two treatment sessions. In one series, 84% of patients had the diameter of the lumen increased to at least 12 mrn1.17’ The most successful results are achieved with tumors that are exophytic rather than submucosal, distal as opposed to proximal, and short rather than long.‘6o Some studies have shown that an adenocarcinoma responds better than a squamous lesion, although this has been refuted by others and may reflect a tendency for adenocarcinomas to be distally sited and exophytic. All report that laser therapy is a safe procedure with good patient tolerance. In most series all patients were able to take a normal diet at the completion of therapy. Despite the universal technical success, swallowing was only subjectively improved in about 80% of the patients and was unchanged in 20% .17’ Results were most favorable in those who had a good pretreatment appetite. Laser therapy also has good long-term results. Swallowing was judged to be improved two months after treatment, without further ss6

Curr

Probl

Surg,

August

1988

therapy, in 88% of patients who reported early benefit. Less than half the patients treated will require retreatment, usually at an interval of eight to ten weeks. Although there is some suggestion that concurrent use of irradiation may prevent the need for retreatment, this has not been substantiated. It has been suggested that the lasting response is due to a layer of fibrosis that forms on laser treated surfaces, acting as a biological stent and impeding luminal ingrowth of tumor. There are few prospective trials comparing the benefit of laser therapy with other forms of palliation. In one series the duration of palliation of dysphagia was significantly greater than that obtained in historical controls treated with radiation therapy.l” In another study that compared the results of 20 patients randomized to receive either laser recanalization or intubation, superior palliation of dysphagia, fewer complications, and longer survival were reported in the laser treated group.‘8z Future developments in laser design, including the use of lateral-aiming laser fibers and smaller endoscopes, will allow better access to tumors and improve the technical aspects of the procedure. ELECTRICAL.

COAGULATION

1’HERAPY

A BICAP heater probe is an electrical coagulation device with a self-contained grounding electrode that produces thermal destruction of much larger areas of tumor than the laser. It is currently being clinically evaluated, and those who have used it claim the procedure is quicker and as effective as laser therapy.ln3 COMBINATION THERAPY FOR ESOPHAGUS AND CARDIA

CARCINOMA

OF THE

Despite advances, the results obtained with either surgery or radiation therapy alone remain undeniably disappointing. Consequently, many feel that the treatment of carcinoma of the esophagus is entering a new era. As for carcinoma of the breast, it may be that cytoreduction, or debulking of tumors by surgery in combination with irradiation and chemotherapy, offers the most promising future hope for long-term survival. PREOPERATIVE

RADIATION

THERAPY

The use of preoperative irradiation has aroused considerable timism since Clifton’s first report in 1953.1s4 The rationale is that sectability rates may be increased and the risk of tumor spread surgical manipulation reduced. There are many published series Cm-r

Probl

Sur&~ August

1988

opreby re587

porting the use of preoperative radiation therapy, but only those of Launois,lti H~ang,‘~ and the EORTC studyls6 are both randomized and prospective (Table 18). The following issues refer to the series reported in Table 18. What Preoperative Radiation Protocol Should Be Used?-The most commonly used radiation protocol is 40 Gy applied in divided fractions over a four-week period, with surgery to follow in four to six weeks when the acute vascular response has subsided and before tissue fibrosis occurs. Variations in radiation dosage, fractionation, and the interval between therapy and surgery have been tried. There has generally been a move away from using large doses of radiation because of increased toxicity, and a longer period between the onset of therapy and resection during which fibrosis and metastases occur. In the Stanford experience, a high dose of radiation resulted in a 50% cancellation of surgery because of toxicity. The operative mortality was high and an additional 12.5% mortality occurred due to fatal radiation injury to the heart and lungs.lg3 A more intensive course of irradiation has been encouraged by evidence in animal tumor models that larger fractions of radiation have a greater effect .lg5 This prompted Launois’@ and Nakayama”” to use an intensive course of radiotherapy, which was followed soon after by surgery. There is concern, however, over the possible long-term sequelae of such a regimen. Kelsen”’ tried both a short high-dose and a traditional dose protocol and found the short course to be as effective as the latter. Despite this, the traditional radiation protocol of 40 Gy over a four-week period, with surgery following four to six weeks later, is still favored by most oncologists. What is the Eflect of Irradiation on &se&ability?-Resectability depends both on the local extent of the tumor and the patient’s condition. Clifton,ls7 reporting early experience from the Memorial Hospital, showed an increase in the resection rate from 58% without radiation to 79% with preoperative radiation. A similar finding was reported by Akakura.*” The validity of these observations is, however, difficult to judge since most comparisons are unfortunately made using historical controls. In contrast, Launois,‘44 in his prospective series, found no difference in the resection rates for either middle or lower third tumors. Wilson”’ claimed that surgery two to three days after irradiation resulted in easier dissection with less blood loss. This surprising finding has not been substantiated. Many authors believe the advantage of a four-week waiting period prior to surgery is that it allows for further assessment of the patient and for nutritional support. In Marks’ series,1g2 195 patients out of 332 managed in this way were found to be unsuitable for surgery. The pity is that these patients were subjected to preoperative irradiation for several weeks without receiving any palliation. 5sl3

Curr

ProbI

Surg,

AUgUSt

1988

18.

Control 25-3014 Control

57 104 63

1981

1986

1985

1970

L,aunois’”

Sugimachi”

Wilson’BX

Ak&Ui-~lxy

1976 1976 1970 M’

332 138 42

1981 1979 4513.5 w 45/3-4 w 50-60/S-7

Control 40-60/4-6 w 40-6014 w

229 76t 133

M’

4.214 w Control 50-6016-S

\\

d

26 25 117

‘d = days;\v - weeks. 1 Gy : 100 rads. t19 had a shorter course of 20 Gv over five davs

Parke?“’ Dogget?

KelsenlY” Van Andel’“’ Marks’=

Control 4018-12

83 77 67

1986

Hua&R5

33112 d Control 40/28 d

102 106

1987

Dose, Gy/d or w

Studies

EORTC””

No.

Radiotherapy

Year

of Preoperative

Author

Results

TABLE

%

w

21.2 5.8 4.8 13.0 10.0 20.8 13.2 12.1 21.0 18.0 31.7 31 .o

Xl.2 100 100 80.8 80.0 82.1 39.7 53.9 61.9 30.4 87.2 57.0

82.5 100

100 100 86.8 41.3 34.1 69.0

100 88.5 100

3.8 4.3 27.6

25.3 19.5

W Operative Mortality

95.2 89.6 75.8

77.3 82.1

Resectable

100 100 92.5

95.1 100

surgq

13.9 22.0 4.7

13.6 5.0 21 .o

31.0 (2 yl‘l 12.0 I2 y”I 25.0

1 1 .5 16.7 21.4

45.5 25.0 9.5

16.0 10.0

% 5vr. SW&al

Does Preoperative Irradiation Result in “Downstaging?‘-The available data suggest that an esophageal tumor response to radiation increases with increasing dosage, but that the normal tissue tolerance is surpassed before there is the likelihood of attaining local tumor control. Those series using high doses have, as expected, reported tumor “sterilization.” Akakura”’ found that his curative resection rate was increased from 25.8% to 65.1% by preoperative high dose radiation therapy. More than half the specimens either had no residual tumor cells or showed destruction of cancer cell nuclei. With irradiation, the number of surgical specimens with tumor present at the resection margins fell from 24% to 6.2%. It is difficult to determine to what extent this was due to a change in surgical policy. An unacceptably high rate of residual tumor, especially in the nonirradiated group, could be viewed as a failure of surgical decisionmaking. Doggettlg4 and Parkerls3 both report patients (7 out of 23 and 5 out of 40) with complete tumor eradication following irradiation. Sugimachi”’ showed that the five-year survival of those in which there was no residual cancer present in the resection specimen was 45.1%. Apart from the few patients with tumor eradication, disagreement exists regarding the effect radiation therapy has on the incidence of lymph node metastases and on the degree of tumor penetration. The EORTC series”’ showed no difference, but two studies have suggested that there is an increase in the number of distant lymph node metastases. AkakuralsY showed that, although the total proportion of involved nodes was similar in both treatment groups, there was a shift to involve distal nodes with irradiation. A similar finding was reported by Maetals8 when he compared the surgical specimens from those patients treated by preoperative radiotherapy and resection with those from patients treated by resection alone. In the irradiated group, 11% had intrathoracic nodal involvement and no abdominal node metastases and 30% had intra-abdominal nodal involvement and no thoracic node metastases. In the surgery only group, the proportion was reversed, i.e., 30% had intrathoracic nodal involvement and no abdominal node metastases and 10% had intraabdominal nodal involvement with no thoracic node metastases. There was a delay of five to six weeks in both series between radiotherapy and surgery, which may have accounted for this observation. What is the Eflect of Irradiation on Operative Mortality?-Preoperative irradiation at the standard dose and fractionation does not seem to affect operative mortality significantly. The slight increase in mortality associated with irradiation in all studies, except Huang’s,185 does not have statistical significance.

590

Cur-r

ProblSur~

August1988

What is the Effect of Irradiation on Treatment Morbidity?-The side effects of radiotherapy include fibrosis, pneumonitis, pericarditis, bone marrow depression, and fistula formation. The incidence of these complications are dose-dependent and are variably reported. Launois““’ The EORTC study’86 reported no difference in morbidity. found the incidence of pulmonary complications to be similar, and neither he nor Huang”’ reported an increased risk of anastomotic leakage following irradiation. Sugimachi,‘s’ however, reported a significant increase in pulmonary complications in the irradiated group 140.4% vs. 27.0% J, as did the OESO group7” (Table 19). Does Preoperative Irradiation Improve Survival?-There is no evidence that preoperative irradiation has anything but a slight beneficial effect on survival. Akakura”” reported increased survival in his retrospective series using historical controls, but his results may have been influenced by selection and changes in technique. Wilson’s prospective but nonrandomized trial “’ showed an increased survival at 12 months, but this was not significant at 24 months. In the three prospective series only Huang’“” reported increased survival. Launois’44 reported no improved survival, and the EORT(: study”’ showed that, although radiation therap.y delayed the appearance of local recurrence, there was no benefit in terms of increased survival. Both the EOKTC study and Launois’ series had above average operative mortalit?, rates, which may have obscured any potential survival advantage fol% irradiation. In summary, local therapy has its limitations be it surge’y, radiotherapy, or the two combined, for a condition in which there is a high prevalence of disseminated disease. Pearson”)R has suggested that local therapy, even if it can totally eradicate tumor, only influences the outcome in approximately one third of all patients, because the other two thirds will fail within two years of intercurrent disease, age, malnutrition, or distant metastases.

TABLE Preouerative

Curr

Probl

Surg,

19. Radiotheratw

Au,qst

1988

and

Postrwerative

ComtAications’

591

POSTOPERATIVE

RADIATION

THERAPY

Postoperative irradiation is attractive because it can be selectively given to those who need it and can be targeted to a particular area in light of the knowledge gained at operation. However, the beneficial effect may be very little because of the large areas that need to be treated and the limited radiosensitivity of the tissues remaining after a surgical resection. Furthermore, dosage must be modified because of the limited radiation tolerance of the gastric or colonic reconstruction. In one of the few studies that addressed this question, Kasia et al.“” used 60 Gy in a T-shaped field over six weeks postoperatively in 111 patients. This was designed to prevent the neck and mediastinal recurrence observed in 14 of 18 of his patients prior to the use of postoperative irradiation. He found a marked decrease in the incidence of neck and mediastinal recurrences in those irradiated (2 of 14). This control of local disease did not improve survival, except in those who did not have node metastases. The five-year survival for patients with normal nodes treated with postoperative irradiation was 35%, compared to 16% for those with uninvolved nodes treated with surgery alone. This would seem to suggest that high dose postoperative irradiation can eradicate microscopic disease in the neck and mediastinum that is not in the nodes. CHEMOTHERAPY

AND

RESECTION

Physicians have long considered esophageal cancer to be resistant to chemotherapy, even though use of chemotherapy in a disease with a high degree of distal dissemination is obviously appealing. Response to chemotherapy can be judged either by improvement in the patient’s symptoms, barium esophagogram, endoscopy, or the absence of tumor at surgery. Symptomatic improvement is the least reliable indicator. To date, ten drugs have been adequately studied relative to epidermoid cancer of the esophagus, nine of which have had moderate (lC;%,i activity. A complete remission to single agents does occur rarely, but response durations are brief.“’ Combination chemotherapy has been more promising. Most regimens involve cisplatin in combination with one or more drugs. Response rates are about 40% to 50%, with a duration of seven months. Unfortunately, a response is usually seen in patients with a Karnofsky score higher than 50, while a response was poor and toxicity increased in those with a score lower than 50. A comparison of performance status grade according to the AJCCS scale, ECOG scale and Karnofsky score is shown in Table 20. Combined chemotherapy prior to surgery has been used successfully for testicular and ovarian cancer, and this approach is now 592

C’urr

Probl

Surg,

August

1988

_..----_

l_-

DeMeester Ckrdiovasc Surg tUCCS. Amrricar~

‘From

assistance

G. Johansson K-E Srlertiw therapeutic approach lY88; 95:X349. l&d by permission. Joint Committee for Cancer Staging. LCOG. Eastern Cooperative

TR, Zanmotto

~\wn~al activitv 5yrnptwnatic but arnbulatoi~; cams tar sell Ainbulatorl\i nlore than 50% of time, occasionally needs Antbulatory 50% UI‘ less of time, nursing care needed Bedridden; n~ay need hospitalization

Perfotmance

TABLE 20. Performance status*t -

HO Hl HZ H3 H4

Scaic: ECOG

Oncologv

Group.

to cancer of the lww

AJJcc:s

.--..

asophagus

4

0 1 2 3

Scale

90-100 70-80 50-60 3030 la-20 and cardra. J

Thorac

Karnofsky Score l%J

being evaluated for esophageal cancer. Early trials used single agents, but recently, combinations of cisplatin, bleomycin, and vindesine have been tested. In one study, 34 patients with local-regional disease were given a single course of cisplatin and bleomycin infusion three weeks prior to surgery.1so Twenty percent of patients had a 50% or greater reduction in tumor mass, as measured by the repeat barium swallow immediately before surgery. For those patients with resectable disease, surgery was followed by further chemotherapy and radiation. The authors conclude that chemotherapy had no effect on operative mortality and morbidity, resectability, or longterm survival. In a second study, vindesine was added to the cisplatin bleomycin combination.20” Two cycles were given preoperatively, as this had been shown to produce maximum response in those with metastastic disease. Thirty-four patients were treated with this regimen, and 28 were subsequently resected eight weeks later. Chemotherapy had produced sufficient tumor shrinkage in ten patients to downstage the primary tumor from Tl-2 to TO-l on radiologic and histologic review. In three patients, no residual disease was found in the resected specimen. A disappointment was that the complication rate was increased and there has been no obvious improvement in survival. The theoretical advantage of combining chemotherapy and radiation is that the drugs may act as radiation sensitizers. Several trials are currently underway and some early results are available. There appears to be some hope that combined modality therapy may increase survival. In Austin’s series,‘03 36% of those treated with chemotherapy, radiation, and surgery were alive at 2.5 years, compared with 25% of a historical group, with similar tumor staging, treated by surgery alone. The use of chemotherapy is associated with an increased morbidity and there is concern that this may be potentiated by concurrent radiotherapy. Wolfezo4 reported no hospital mortality for 29 patients treated with chemotherapy, radiation, and surgery. On the other hand, the Wayne State University experience is of a 27% to 30% treatment-related mortality for the combined therapy.‘05 To date, the most impressive conclusion is that concurrent radiation and chemotherapy increases the number of patients who achieve a complete response prior to surgery, i.e., no microscopic evidence of tumor in the resected specimen. In contrast, Hilgenberg et a1.,205awho used preoperative chemotherapy and selective postoperative irradiation, reported that only one resected specimen was completely free of tumor although another contained only necrotic tumor (Table 21). However, the significance of this is not clear with regard to survival. LeichmanZo5 found that all those who had residual tumor at the time of surgery died of their cancer, while 92% of those with complete response to preoperative therapy had a median dis694

Curr

Probl

Surg,

August

1988

TABLE The

21.

Incidence

of Complete

Responses

Author

Chemotherapy

Leichmanz””

to Combination

Therapy

Radiation

No.

Complete

Response

5-FU + cisplatin 5-FU + mitimycin-C

30 G.v

42

Austin”’ WolfeLoJ

5-FU + cisplatin VP16 + cisplatin

30 Gy 45 Gy

11

36

29

34

Hilgenberp

5-FU + cisplatin

27

4

(%)

26

ease-free survival of 3.5 years or died from a noncancer-related cause. They suggested that surgery might not be a necessary part of the curative regimen for patients with squamous cell carcinoma of the esophagus. This conflicts with Austin’s findings that the survival of those with and without residual tumor was not significantly different .‘03 Chemotherapy and radiation has been advocated for those who refuse surgery or are unfit for it. In such patients, Kolaric et al.“” reported a significant improvement in survival of patients receiving combined radiation and chemotherapy, compared to chemotherapy alone. One hundred and three patients with unresectable esophageal cancer were entered into three prospective studies to compare bleomycin and radiation, Adriamycin and radiation, and a combination of bleomycin, Adriamycin, and radiation. Patients receiving both radiation and chemotherapy did better than those receiving radiation alone. Unfortunately, the combination of bleomycin and Adriamycin produced severe toxicity. The Eastern Cooperative Oncology Group”’ reported the results of a randomized trial of radiation versus radiation plus bleomycin in patients who were thought to have an unresectable tumor. The results for the 77 patients evaluated were poor, with no difference in survival or palliation between the two treatment arms. Once again, the use of bleomycin was associated with additional toxicity. Wolfe”04 has reported excellent palliative results for 34 patients with inoperable tumors treated with cisplatin, VP16, and 60 Gy and irradiation. Treatment was well tolerated by most patients, although there was one chemotherapy-related death. None of the remainder required any additional palliation or supportive alimentation. At the time of reporting, 16 patients had died 2 to 16 months post-therapy, while the longest survivor was free of recurrence 16 months after completing treatment. The results of combination therapy, although exciting in isolated patients, are not sufficiently predictable to be considered standard therapy. Morn work needs to be focused on the selection of those most apt to receive benefit. Cur-r

Pmbl

Surg,

Au@st

1988

595

RETJMENCES

1. Dunham IJ, Bailar JC: World maps of cancer mortality rates and frequency ratios. J Nat1 Cancer Inst 1968; 41:15.5-203. 2. Wynder EL, Brass II: A study of etiological factors in cancers of the esophagus. Cancer 1961; 14:389-413. 3. Tuyns AJ, Pequignot G, Jensen OM: Le cancer de l’oesophage en Ille-etVilaine en fonction des niveaux de consommation d’alcool et de tubac. Des risques qui se multiplient. Bull Cancer (Paris) 1977; 64:45-60. 4. Tuyns AJ, Pequignot G, Abbatucci JS: Oesophageal cancer and alcohol consumption: Importance of type of beverage. Znt J Cancer 1979; 23:443-447. 5. Hirayama T: Diet and cancer. Nutr Cancer 1979; 1:67-81. 6. Schottenfeld D: Alcohol as a cofactor in the etiology of cancer. Cancer 1979; 43:1962-1966. 7. Jussawalla DJ: Epidemiological assessment of aetiology of esophageal cancer in Greater Bombay. Monograph No. 1 International Sem on Epidemiology ofEsophageal Cancer, Bangalore, India, 1971, 20-30. 8. Kmet J: Opium and oesophageal cancer in Iran. Lancet 1978, 2:1371-1372. 9. Hewer T, Rose E, Ghadirian P, et al: Ingested mutagens from opium and tobacco pyrolysis products and cancer of the oesophagus. Lancet 1978; 2:494496. 10. Yang CS: Research on esophageal cancer in China: A review. Cancer Res 1980; 40:2633-2644. 11. Berenblum I, Haran N: The influence of croton oil and of polyethylene glycol-400 on carcinogenesis in the forestomach of the mouse. Cancer Res 1955; 15:510-516. 12. Miao C, Guo FC, Zhang JZ, et al: The relationship between fungi and nitrosamines and their precursors. The action of fungi isolated from grains in Linxian. Med Ref 1978; 2:46-53. 13. Miller RW: Cancer epidemics in the People’s Republic of China. J Nat2 Cancer Inst 1978; 60:1195-1203. 14. Fong LYY, Newberne PM: Zinc deficiency and methylbenzylnitrosamineinduced esophageal cancer in rats. J Nat1 Cancer Inst 1978; 61:145-150. 15. Harper PS, Harper RMJ, Howel-Evans AW: Carcinoma of the esophagus with tylosis. Q J Med 1970; 39:317-333. 16. Wychulis AR, Woola GL, Anderson HA, et al: Achalasia and carcinoma of the esophagus. JAMA 1971; .X5:1638-1641. 17. Appelquist P, Salmo M: Lye corrosion carcinoma of the esophagus. A review of 63 cases. Cancer 1980; 45:2655-2658. 18. Holmes GKT, Stokes PL, Sorahan TM, et al: Coeliac disease, gluten free diet and malignancy. Gut 1976; 17:612-619. 19. Stokes PL, Prior P, Sorahan TM, et al: Malignancy in relatives of patients with coelic disease. Br J Prevent Sot Med 1976; 30:17-21. 20. Cahan WG, Castro EB, Rosen PB, et al: Separate primary carcinomas of the esophagus and head and neck region in the same patient. Cancer 1976; 37:85-89. 21. Raphael HA, Ellis FM, Docker MB: Primary adenocarcinoma of the esophagus: Id-year review and review of the literature. Ann Surg 1966; 164:785796. 22. Turnbull ADM, Goodner JI: Primary adenocarcinoma of the esophagus. Cancer 1968; 22:915-918. 23. Cederquist C, Nielsen J, Berthelsen A, et al: Adenocarcinoma of the oesophagus. Acta Chir Stand 1980; 146:4114X. 596

Curr

Probl

SW5

August 1988

24. Collis JL: Surgical treatment of carcinoma of the esophagus and cardia. Br .I Surg lY71; 58:801-804. 25. Scicchitano LP, Comishion RC: Primary adenocarcinoma of the esophagus. Am J Surg 1962; 104:531-533. 26. Bosch A, Frias 2, Caldwell WI. .4denocarcinorna of the esophagus. Cancer 1979; 43:1557-1561. 27. Cutler SJ, Young JL Jr teds): Third National Cancer Survey: Incidence data, in &drew PMS: National Cancer Institute Monograph. Besthesda, MD, WCI41, 1975. 28. Earlam R: The clinical relevance of epidemiology of oesophageal cancer, in Watson A, Celestin R (edsi: Disorders of the Oesophagus: Advances and Controversies. London, Pitman Publishing Ltd., 1984, pp 15616ti. 29. Sarr MG, Hamilton SR, Marrone GC, et al: Barrett’s esophagus: Its prevalence and association with adenocarcinoma in patients with s?/mptoms of gastroesophageal reflux. Am .I Surg 1985; 149:187-193. 30. Haggitt RC, Tryzelaar J. Ellis PH. et al: Adenocarcinoma complicating columnar epithelium-lined IBarrett’si esophagus. Am .I C/in Path01 lY78; 70:15. 31. Siewert R, Weiser HF, Lepsien G, et al: Endobrachyoesophagus und adenocarcinom der speisetihre. Chirurg 1979; 50:675-680. 32. Spechler SJ, Robbins AH, Kubins HB, et al: Adenocarcinoma and Barrett’s esophagus. An overrated risk: GastroenteroloLgv 1984; 87:927-933. 33. Cameron AJ, Ott BJ, Payne WS: The incidence of adenocarcinoma in columnar-lined (Barrett’s) esophagus. iV Engi J Med 1985: 313:857-859. 34. Naef AP, Savary M, Ozzello L: Columnar-lined lower esophagus: An acquired lesion with malignant predisposition. J ‘I’horac Cardiovasc Surg 1975; 70:826-835. 35. Skinner DB, Walther BC. Riddell KH, et al: Barrett’s esophagus. Comparison of benign and malignant cases. Ann Surg 1983; lY8:554-566. 36. Spechler SJ: Endoscopic surveillance for patients with Barrett’s esophagus: Does the cancer risk justify the practice? Ann Intern Med 1987; 106:902-904. 37. Reid BJ, Weinstein WM, Lewin KJ, et al: Endoscopic biopsy can detect highgrade dysplasia or early adenocarcinoma in Barrett’s esophagus without grossly recognizable neoplastic, lesions. Gastroenterology 1988; 94:X1-90. 38. McKeown KC: Clinical presentation of carcinoma of the oesophagus. .I H Co11 Surg Edinb 1986; 31:1YY-206. 3Y. Kesano JH: Treatment of cancer of the esophagus. Bull Sor Int Chir lY.57; 6:311-314. 40. Orringer MB, Skinner DB: 1J1~1sual presentations of primary and secondar?/ esophageal malignancies. Ann 7’horac Surg 1971; 11:305-314. 41. Earlam R, Cunha-Melo JR: Oesophageal squamous cell carcinoma: 1. A critical review of surgery. Br J Surg lY80; 67:381-390. 42. Coordinating Groups for Research on Oesophageal Cancer: Early diagnosis and surgical treatment of oesophageal cancer’ under rural conditions. Chin Med J lY76; 2113-116. 43. Lightdale CJ, Winawer SJ: Screening diagnosis and staging of esophageal cancer. Semin Oncol 1984; 11:10-112. 44. Shu YJ: Cytopathology of the esophagus. An overview of esophageal c.ytopathology in China. Acta Cvtor 1983; 27:7-16. 45. Munoz N, Crespi M: Studies in the aetiology of oesophageal carcinoma, in Watson A, Celestin LR iedsi: Disorders qf the Oesophagus: Advances and Controversies. London, Pitman Publishing Ltd., 1984, pp 147-154. Cur-r

Probl

Surg.

Au,+st

1988

597

46. Edwards DAW, Lobello R: Radiographic discrimination of benign and malignant oesophageal strictures. Gut 1982; 23A453. 47. Winawer SJ, Melamed M, Sherlock P: Potential of endoscopy, biopsy and cytology in the diagnosis and management of patients with cancer. Clin Gastroenterol 1976; 5:575-595. 48. Graham DY, Schwartz JT, Cain GD, et al: Prospective evaluation of biopsy number in the diagnosis of esophageal and gastric carcinoma. Gastroenterology1982; 83:228-231. 49. Guanrei Y, He H, Sungliang Q et al: Endoscopic diagnosis of 115 cases of early esophageal carcinoma. Endoscopy 1982; 14:X7-161. 50. Mandard AM, Tourneaux J, Gignous M, et al: In situ carcinoma of the esophagus: Macroscopic study with particular reference to the Lug01 test. Endoscop-v 1980;12:51-57. 51. Jass JR, Morson BC: Epithelial dysplasia in the gastrointestinal tract, in Sherlock P, Jerzy-Glass G (eds): Progress in Gastroenterologv, vol 4. New York, Grune & Stratton, Inc, 1983, pp 345-371. 52. Ming SC: Tumors of the esophagus and stomach. Atlas of Tumor Pathology. Armed Forces Institute of Pathology, 1973, series 2, section 2, fascicle 7, pp 27-79. 53. Minielly JA, Harrison EG, Fontana RS, et al: Verrucous squamous cell carcinoma of the esophagus. Cancer 1967; 20:207&2087. 54. DeMeester TR, Skinner DB: Polypoid sarcoma of the esophagus. A rare but potentially curable neoplasm. Ann Thorac Surg 1975; 20:405-417. 55. Osamura RY, Shinamura K, Hatu J, et al: Pot-ypoid carcinoma of the esophagus. A unifying term for “carcinosarcoma” and “pseudosarcoma.” Am J Surg Path01 1978; 2:201-208. 56. Garlock JH: Radical surgical treatment for carcinoma of the cardiac end of the stomach. Surg Gynecol Obstet 1942; 74:555-560. 57. Smithers DW: Adenocarcinoma of the esophagus. Thorax 1956; 11:257-267. 58. Troncoso P, Riddell RM: Pathology of esophageal carcinoma, in DeMeester TR, Levin B teds): Carcinoma of the Esophagus. New York, Grune & Stratton, Inc., 1985, pp 89-118. 59. American Joint Committee on Cancer: Manual for Staging qf Cancer. Philadelphia, JB Lippincott Co, 1983. 60. Fleming JAC: Carcinoma of thoracic esophagus: Some notes on its pathology and spread in relation to treatment. Br J Radio1 1943; 16:212-214. 61. Rosenberg JC, Franklin R, Steiger Z: Squamous cell carcinoma of the thoracic esophagus: An interdisciplinary approach. Curr Probl Cancer 1981; 5:1-52. 62. Akiyama H, Kogwe T, Itai Y: The esophageal axis and its relationship to the resectability of carcinoma of the esophagus. Ann Surg 1971; 176:3&36. 63. Klinkhamer AC: Esophagography in Anomalies qf Aortic Arch System. Amsterdam, Excerpta Medica Foundation, 1969. 64. Halvorsen RA, Thompson WA: Computed tomography of the gastroesophageal junction, CRC Crit Rev Diagn lmag 1985; 21:183-228. 65. Picus D, Balfe DM, Koehler RE, et al: Computed tomography in the staging of esophageal carcinoma. Radiology 1983; 146:433-438. 66. Quint LE, Glazer GM, Orringer MB, et al: Esophageal carcinoma: CT findings Radiology 1985;155:171-175. 67. Duignan JP, McEntee GP, O’Connell DJ, et al: The role of CT in the management of carcinoma of the oesophagus and cardia. Ann R Co11 Surg Engl 1987; 69:286-288. 598

Cur-r

ProblSurg,

August1988

68. Quint LE, Glazer GM, Orringer MB: Esophageal imaging by MR and CT: Study of normal anatomy and neoplasms. Radiology 1985; 156:727-731. 69. Little AG, DeMeester TR, Kirchner PI’, et al: Guided biopsies of abnormalities on nuclear bone scan. Techniques and indications. J Thorac Caardiovast Surg 1983; 85:396403. 70. King RM, Pairolero PC, Trastek VF, et al: Ivar Lewis esophagogastrectomy for carcinoma of the esophagus: Early and late functional results. Ann Thorac Surg 1987; 44:119-122. 71. Skinner DB, Dowlatashy KD. DeMeester TR: Potentially curable cancer of the esophagus. Cancer 1982; 502571-2575. 7.2. Skinner DB, Ferguson MK, Soriano A, et al: Selection of operation for esophageal cancer based on staging. Ann Surg 1986; 204:391-401. 73. DeMeester TR, Zaninotto G, Johansson K-E: Selective therapeutic approach to cancer of the lower esophagus and cardia. J Thorac Cardiovasc Surg 1988; 95:42-54. 73a. Becker CD, Barbier PA, Terrier F, et al: Patterns of recurrence of esophageal carcinoma after transhiatal esophagectomy and gastric interposition. RIB 1987; 48273-277. 74. Pearson JG: Radiotherapy of carcinoma of the oesophagus and postcricoid region in Southeast Scotland. Clin Radio1 1966; 17:242-257. 7.5. Newaishy GA, Read GA, Duncan W, et al: Results of radical radiotherapy of squamous cell carcinoma of the esophagus. Clin Radio1 1982; 33:347-352. 76. Earlam R, Cunha-Melo JR: Oesophageal squamous cell carcinoma: It. A critical review of radiotherapy. Br J Surg 1980; 67:457461. 77. Garvin PJ, Kaminski DL: Extrathoracic esophagectomy in the treatment of esophageal cancer. Am J Surg 1980; 140:772-781. 78. Shahian DM, Neptune WB, Ellis FH, et al: Transthoracic versus extrathoratic esophagectomy: Mortality, morbidity and long-term survival. Ann Thorac Surg 1986; 41237-246. 79. Giuli R, Sancho-Garnier H: Diagnostic, therapeutic and prognostic features of cancers of the esophagus: Results of the international prospective study conducted by the OESO group 1790 patients). Surgery 1986; 99:614-622. 80. Sweet RH: Late results of surgical treatment of carcinoma of the esophagus. JAMA 1954; 155:422425. 81. Wong J: Transhiatal oesophagectomy for carcinoma of the thoracic oesophagus. Br J Surg 1986; 73:89-90. 82. Orringer MB: Transhiatal esophagectomy without thoracotomy for carcinoma of the thoracic esophagus. Ann Surg 1984; 200:282-288. 83. Skinner DB: En bloc resection for neoplasms of the esophagus and cardia. J Thorac Cardiovasc Surg 1983: 85:59-71. 84. Morson BC: The spread of carcinoma of the oesophagus, in Tanner NC. Smithers W feds): Tumors of the Oesophagus. Monographs on Neoplastic Disease at Various Sites, Vol 4. Edinburgh, E &. S Livingstone, 1961, pp 136 145. 85. Akiyama H, Tsurumaru M, Kawamura ‘I‘, et al: Principles of surgical treatment for carcinoma of the esophagus: Analysis of l.ymph node involvoment Ann Surg 1981; 194:438446. 86. Castrini G, Pappalardo G: Carcinoma of the cardia: I‘actical problems. .I Thorac Cardiovasc Surg 1981; X2:190-193. 87. Sous HU, Borchard F: Cancer of the distal esophagus and cardia: Incidence, tumorous infiltration and metastatic spread. Ann SUFg 1986; 203:188-195. 88. DeMeester TR: Surgical anatomy of the esophagus, in Shields TW (edi: GenCurr Probl Surg, August 1988

599

era1 Thoracic Surgery, ed 2. Philadelphia, Lee & Febiger, 1983, pp 82-91. 89. Giuli R: Surgical complications and reasons for failure in DeMeester TR, Levin B teds): Cancer of the Esophagus. Orlando, Grune & Stratton 1985, pp 198-208. 90. Tam PC, Cheung HC, Ma L, et al: Local recurrences after subtotal esophagectomy for squamous cell carcinoma. Ann Surg 1987; 205:189-194. 90a. Wong J: Esophageal resection for cancer: The rationale of current practice. Ann J Surg 1987; 153:18-24. 91. Papachristou DN, Former JG: Adenocarcinoma of the gastric cardia: The choice of gastrectomy. Ann Surg 1980; 192SS--64. 92. Miller C: Carcinoma of the thoracic oesophagus and cardia. A review of 405 cases. Br J Surg 1962; 49507622. 93. Nicks R, Green D, McClatchie G: A clinicopathological study of some factors influencing survival in cancer of the oesophagus. A survey of ten years experience. Aust NZ J Surg 1973; 43:3-13. 94. Thompson JC: The stomach and duodenum, in Sabiston DC, Jr (ed): DavisChristopher Textbook of Surgery, ed 11. London, Saunders, 1977, p 899. 95. Goldsmith HS, Akiyama H: A comparative study of Japanese and American gastric dimensions. Ann Surg 1979; 190:690-693. 96. Holscher AH, Voit H, Buttermann G, et al: Function of the intrathoracic stomach as esophageal replacement. World J Surg, in press. 97. Orringer MB, Stirling MC: Cervical esophagogastric anastomosis for benign disease: Functional results. Presented at the American Association for Thoracic Surgery, April 1988. J Thorac Cardiovasc Surg; in press. 98. Isolauri J, Markkula H, Autio V: Colon interposition in the treatment of carcinoma of the esophagus and gastric cardia. Ann Thorac Surg 1987; 43~420424. 98a. DeMeester TR, Johansson K-E, Franze I, et al: Indications, surgical techniques, and long-term functional results of colon interposition or bypass. Ann Surg; in press. 99. Hinder RA: The effect of posture on the emptying of the intrathoracic vagotomized stomach. Br J Surg 1976; 63:581-584. 100. Moreno-Osset E, Tomas-Ridocci M, Paris F, et al: Motor activity of esophageal substitute (stomach, jejunal and colon segments). Ann Thorac Surg 1986; 41:515-519. 101. Cheung HC, Siu KF, Wong J: Is pyloroplasty necessary in esophageal replacement by stomach? A prospective, randomized controlled trial. Surgery 1987;102:19-24. 102. Belsey R: Reconstruction of the oesophagus. Ann R Co11 Surg Engl 1983; 65:360-364. 103. DeMeester TR, Lafontaine E: The pleura, in Sabiston DC, Spencer FC teds): Gibbons’s Surgery of the Chest, ed 4, vol 1. Philadelphia, WB Saunders Company, 1983, pp 361-406. 104. Torek F: The first successful case of resection of the thoracic portion of the esophagus for carcinoma. Surg Gynecol Obstet 1913; 16:614-617. 105. Ohsawa T: The surgery of the oesophagus. Arch Jpn Chir 1933; 10:605. 106. Marshall SF: Carcinoma of the esophagus: Successful resection lower end of esophagus with reestablishment of esophageal gastric continuity. Surg C/in NAm 1938; 181643-648. 107. Adams W, Phemister DB: Carcinoma of the lower thoracic esophagus. Report of a successful resection and esophagastrostomy. J Thorac Surg 1938; 7:621-632. 600

CurrProblSurg,

August 1988

108. Nishi M, Hiramatsu Y, Hioki K, et al: Risk factors in relation to postoperative complications in patients undergoing esophagectomy or gastrectomy for cancer. Ann Surg 1988;207:148-154. 109. Garfmkel L, Poindexter CE, Silverberg E: Cancer in black Americans. Cancer 1980; 30:39-43. 110. Diener CF, Burrows B: Further observations on the course and prognosis of chronic obstructive lung disease. Am Rev Respir Dis 1975; 111:719-724. 111. Boucher CA, Brewster DC, Darling RC, et al: Determination of cardiac risk by dipyridamole-thallium imaging before peripheral vascular surgery. N Engl J Med 1985; 312:389-394. 112. Port S, Cobb FR, Coleman E, et al: Effect of age on the response of the left ventricular ejection fraction to exercise. N Engl J Med 1980; 303:1133-1137. 113. Stones MJ, Kozma A: Adult age trends in record running performances. Ew Aging Res 1980; 6:407416. 114. Sikes Ed Jr, Detmer DE: Aging and surgical risk in older citizens of Wisconsin. Wis MedJ 1979;7827-30. 115. Fries JF: Aging, natural death and the compression of senescence. N Engl JMed1980; 303:130-135. 116. Heyflick L: Aging under glass. E,xp Gerontol 1970; 5:291-303. 117. Maloney JV: The limits of medicine. Ann Surg 1981; 194:247-255. 118. Thomas PA: Physiologic sufficiency of regenerated lung lymphatics. Ann Surg1980; 192:162-168. 119. Trapnell DH: The peripheral l-ymphatics of the lungs. Br J Radial 1963; 361660-672. 120.

121. 122. 123. 124. 125. 126. 127. 128. 129.

Guyton AC, Lindsey AW: Effect of elevated left atrial pressure and decreased plasma protein concentration on the development of pulmonary edema. Circulation Res 1959; 7:649-657. Heatly RV, Lewis MH, Williams RHP: Preoperative intravenous feeding: A controlled trial. Postgrad Med J 1979; 55:541-545. Piccone VA, Ahmed N, Crossberg S, et al: Esophagogastrectomy for carcinoma of the esophagus. Ann Thorac Surg 1979; 28:369-377. Allardyce D, Groves A: A comparison of nutritional responses from intravenous and enteral feedings. Surg Gynecol O&et 1974; 139:179-184. Lim STK, Choa RG, Lam KH, et al: Total parenteral nutrition versus gasttostomy in preoperative preparation of patients with cancer of the esophagus. JSurg 1981;68:69-72. Delaney HM, Carnevale N, Garvey JW: Jejunostomy by a needle catheter technique. Surgery 1973; 73:786-790. Ryan JA, Abel RM, Abbott WM, et al: Catheter complications in total parenteral nutrition: A prospective study in 200 consecutive patients. N Engl J Med 1974;280:757-761. Gomes MN, Km11 S, Spear SL: Mediastinal tracheostomy. Ann Thorac Surg 1987; 43539-543. Silverberg E: Cancer statistics 1983. CA 1983; 16:33. Ravitch M: A Century ofsurgery. Philadelphia, JB Lippincott Co, 1981, pp 56.

Watson WL, Pool L: Cancer of the cervical esophagus. Surgery 1948; 23:893905. 131. Beatty JD, DeBoer G, Rider WD: Carcinoma of the esophagus: Pretreatment assessment, correlation of radiation treatment parameters with survival, and identification and management of radiation treatment failure, Cancer 1979; 432254-2267. 130.

Cur-r Pmbl Surg, August

1988

601

132. Colin CF, Spiro RH: Carcinoma of the cervical esophagus. Changing therapeutic trends. Am J Surg 1984; 148:460466. 133. Baker JW Jr, Schechter GL: Management of paraesophageal cancer by blunt resection without thoracotomy and reconstruction with stomach. Ann Surg 1986; 203:491499. 134. Kron IL, Joob AW, Levine PA, et al: Blunt esophagectomy and gastric interposition for tumors of the cervical esophagus and hypopharynx. Am Surg 1986; 52:140-141. 135. Silver CE: Surgical management of neoplasms of the larynx, hypopharynx and cervical esophagus. Curr Probl Surg 1977; 14:2-69. 136. Akiyama H, Hiyama M, Miyazono H: Total esophageal reconstruction after extraction of the esophagus. Ann Surg 1975; 182:547-552. 137. DeMeester TR, Lafontaine ER: Surgical therapy, in DeMeester TR, Levin B teds): Cancer of the Esophagus. Orlando, Grune & Stratton, Inc, 1985, pp 141-197. 138. Kakegawa T, Yamana H, Ando N: Analysis of surgical treatment for carcinoma situated in the cervical esophagus. Surgery 1985; 97:150-156. 139. Lewis I: The surgical treatment of carcinoma of the oesophagus with special reference to a new operation for the growths of the middle third. Br J Surg 1946; 34:18-31. 140. Belsey RH, Hiebert CA: An exclusive right thoracic approach for cancer of the middle third of the oesophagus. Ann Thorac Surg 1974; 18:1-15. 141. Fisher DR, Brawley RK, Kiefer RF: Esophagogastrostomy in the treatment of carcinoma of the distal two-thirds of the esophagus. Ann Thorac Surg 1972; 14:658-670. 142. Akiyama H: Surgery for carcinoma of the esophagus. Curr Probl Surg 1980; 17:1-20. 143. Lu YK, Li YM, Gu YZ: Cancer of esophagus and esophagogastric junction: Analysis of results of 1,025 resections after 5 to 20 years. Ann Thorac Surg 1987; 43:176-187. 144. Launois B, Delarue D, Campion JP, et al: Preoperative radiotherapy for carcinoma of the esophagus. Surg Gynecol Obstet 1981; 153:690-692. 145. Molina JE, Lawton BR, Myers WO, et al: Esophagogastrectomy for adenocarcinoma of the cardia. Ten years experience and current approach. Ann Surg 1982; 195:146-151. 146. Turner GG: Carcinoma of the oesophagus. The question of its treatment by surgery. Lancer 1936:67-72, 130-134. 147. Tanner NC: The present position of carcinoma of the oesophagus. Postgrad Med J 1947; 23:109-139. 148. Orringer MB: Transhiatal esophagectomy without thoracotomy for carcinoma of the esophagus. Adv Surg 1986; 19:149. 149. Finley RJ, Grace M, Duff JH: Esophagogastrectomy without thoracotomy for carcinoma of the cardia and lower part of the esophagus. Surg Gynecol Obstet 1985; 160:49-56. 150. Logan A: The surgical treatment of carcinoma of the esophagus and cardia. J Thoracic Cardiovasc Surg 1963; 46:150-161. 151. Wolf BS: Roentgenologv of the esophagogastric junction, in Margulis AR, Burhenne HJ teds): Alimentary Tract Roentgenology. St Louis, CV Mosby Co, 1967, pp 371422. 152. Heit HA, Johnson LF, Siegel SR, et al: Palliative dilation for dysphagia in esophageal carcinoma. Ann Intern Med 1978; 89:629-631. 153. Cassidy DE, Nord HS, Boyce HW Jr: Management of malignant esophageal 602

Curr

Probl

Surg,

August

1988

Role of esophageal dilatation and peroral prosthesis. Am J Gas1981; 76:173. 1.54. Earlam R, Cunha-Melo JR: Malignant oesophageal strictures: A review of techniques for palliative intubation. Br J Surg 1982; 69:61-68. 15.5. Atkinson M, Ferguson R, Parker GC: Tube introducer and modified Celestin tube for use in palliative intubation of oesophagogastric neoplasms at fiberoptic endoscopy. Gut 1978; 19:669-671. 156. Angorn IB: Intubation in the treatment of carcinoma of the esophagus. world J Surg 1981; 5:535-541. 157. Hegarty MM, Angorn IB, Bryer JV, et al: Palliation of malignant esophagorespiratory fistulae by permanent indwelling tube. Ann Surg 1977; 185:8891. 158. Ogilvie AL, Dronfield MW, Ferguson R, et al: Palliative intubation of oesophagogastric neoplasms at fiberoptic endoscopy. Gut 1982; 23:1060-1067. 159. Watson A: A study of the quality and duration of survival following resection, endoscopic intubation and surgical intubation in oesophageal carcinoma. L3r J Surg 1982; 69:585-5X8. 160. Diamantes T, Mannell A: Oesophageal intubation for advanced oesophageal cancer: The Baragwarath experience 1977-1981. Rr J Sorg 1983; 70:555-5.57. 161. Lishman AH, Dellipiani AW, Devlin HB: The insertion of oesophagogastric tubes in malignant oesophagoal strictures: Kndosc0p.v or surgery? Br .I Surg 1980; 67:2.57-259. 162. Unruh HW, Pagliem KM: Pulsion intubation versus traction intubation for obstructing carcinomas of the esophagus. Ann ‘I’horac Surg 1985; 40:337342. 163. Little AG, Ferguson MK, DeMeester TR, et al: Esophageal carcinoma with respiratory tract fistula. Cancer 1984; 53:1322-1328. 164. Wong .I, Lam KH, Wei WI, et al: Results of the Kirschner operation. World .I Surg 1981; 5:547-552. 165. Skinner DB, DeMeester TR: Permanent extracorporeal esophagogastric tube for esophageal replacement. Ann ‘l’horac Surg 1976; 22:107-111. 166. Orringer MB: Substernal gastric b.vpass of the excluded esophagus: Results of an ill-advised operation. Surgery 1984; 96:467-470. 167. Akiyama H, Hiyama M: A simple esophageal I~~ypass operation by lhf. high gastric division. Surgery 19’74; 75:674-681. 168. Ong GB: The Kirschner operation: A forgotten procedure. Br .I Surg 1973: 60:221-227. 169. Giraud RMA, Berzin S: The reversed gastric esophagoplasty in palliation oi carcinoma of the esophagus. Surg G.vnecol Ohstet 1987; 165:115. 169a. Charbit L, Brun JG, Celerier M: Oesophagoplastie par retournenment tit: l’estomac entier vers le cou. Nouv Presse Med 1982; 11:669-671. 170. Lam KH, Wong J, Lim STK, et al: Intrathoracic gastric bypass for carcinoma of oesophagus found unresectablc at exploration. Br J Surg 1982; 69:71-7X 171. Yamagishi M, Tkede N, Yonemoto ‘I‘: An isoperistaltic gastric tube. New method of esophageal r-eplacenlent. Arch Surg 1970; 100:689-692. 172. Burdette WJ: Palliative operation for carcinoma of cervical and thoracic esophagus. Ann Surg 1971; 173:714-732. 173. Belsev RHR: Palliative managetnenl of esophageal czancer‘. Am J .Sur# 1980: 139:789-794. 174. Ong GB: IJnresectable carcinoma of the oesophagus. Ann R Co/l Sur:r: ping/ 1975; 56%14. 17.5. Duranceau ACH, Lafonlaint: b:R, Arcbambault SC el al: Motor limc:lion in strictures:

troenterol

Currt’robl

Surg,

Au~ust1988

603

176. 177.

the excluded esophagus and its implications in the management of patients with unresectable carcinoma of the esophagus. Ann Surg 1987; 206:787-790. Wara WM, Mauch PM, Thomas AN, et al: Palliation for carcinoma of the esophagus. Radiology 1976; 121:717-720. Fleischer D, Kessler F: Endoscopic Nd:YAG laser therapy for carcinoma of the esophagus: A new form of palliative treatment. Gastroenterology 1983; 85:600-606.

178.

179. 180.

181.

182.

183. 184. 185.

186.

187. 188.

189. 190. 191. 192. 193. 194.

195. 196. 197.

604

Pietrafitta JJ, Dwyer PM: Endoscopic laser therapy of malignant esophageal obstruction. Arch Surg 1986; 121:395-400. Ahlquist DA, Gostout CJ, Viggiano TR, et al: Endoscopic laser palliation of malignant dysphagia: A prospective study. Mayo Clin Proc 1987; 62:867-874. Fleischer D, Sivak MV Jr: Endoscopic Nd:YAG laser therapy as palliation for esophagogastric cancer. Gastroenterology 1985; 89:827-831. Mellow MH, Pinkas H: Endoscopic therapy for esophageal carcinoma with Nd:YAG laser: prospective evaluation of efficacy, complications and survival. Gastrointest Endosc 1984; 30:334-339. Carter R, Smith J: Oesophageal carcinoma: A comparative study of laser recanalization versus intubation in the palliation of gastro-oesophageal carcinoma. Lasers Med Sci 1986; 1:245-251. Hamilton J: Personal communication, 1987. Clifton EE, Blansfield HN: The treatment of carcinoma of the esophagus by radiation therapy and surgery. Surgery 1953; 33:748. Huang GJ, Gu XZ, Wang LJ, et al: Experience with combined preoperative irradiation and surgery for carcinoma of the esophagus. Gann Monograph on Cancer Research 1986; 31:159-164. Gignoux M, Roussel A. Paillot B, et al: The value of preoperative radiotherapy in esophageal cancer: Results of a study of the E.O.R.T.C. World J. Surg 1987; 11:426-432. Sugimachi K, Matsufuji H, Kai H, et al: Preoperative irradiation for carcinoma of the esophagus. Surg Gynecol Obstet 1986; 162:174-176. Wilson SE, Hiatt JR, Stabile BE, et al: Cancer of the distal esophagus and cardia: Preoperative irradiation prolongs survival. Am J Surg 1985; 1.50:114121. Akakura I, Nakamura Y, Kakegawa T, et al: Surgery of carcinoma of the esophagus with preoperative radiation. Chest 1970; 57:47-57. Kelsen DP, Ahuja R, Hopfan S, et al: Combined modality therapy of esophageal carcinoma. Cancer 1981; 48:31-37. van Andel JG, Dees J, Dijkhuis CM, et al: Carcinoma of the esophagus: Results of treatment. Ann Surg 1979; 190:684-689. Marks RD Jr, Scruggs HJ, Wallace KM: Preoperative radiation therapy for carcinoma of the esophagus. Cancer 1976; 38:84-89. Parker EF, Gregorie HB: Carcinoma of the esophagus. Long term results. JAMA 1976; 235:1018-1020. Doggett RLS, Guernsey JM, Bagshaw MA: Combined radiation and surgical treatment of carcinoma of the thoracic esophagus. Front Radiat Ther Oncol 1970; 5:147-154. Hall E: Radiobiologv for the Radiologist. Hagerstown Harper and Row, 1978, p. 81. Nakayama K, Kinoshita Y: Surgical treatment combined with preoperative concentrated irradiation. .IAh4A 1974; 227:178-181. Clifton EE, Goodner JT, Brunstein E: Preoperative irradiation for cancer of the esophagus. Cancer lY60; 13:37-45. CUrr

Probl

Surg,

August

1988

198. Maeta M, Koga S, Andachi H, et al: Preoperative radiotherapy and intraabdominal metastasis of the lymph node in the surgical treatment of carcinoma of the thoracic esophagus. Surg Gvynecol Obstet 1987; 165:235-238. 199. Pearson JG: The value of radiotherapy in the management of esophageal cancer. AJR 1969; 105300-513. 200. Kasai M, Mori S, Watanabe T: Follow-up results after resection of thoracic esophageal carcinoma. World J Surg 1978; 2:543-551. 201. Kelsen D: Chemotherapy of esophageal cancer. Semin Oncol 1984; 11:159168. 202. Bains M, Kelsen DP, Beattie EJ, et al: Treatment of esophageal carcinoma by combined preoperative chemotherap.v. Ann Thorac Surg 1982; 34:521528. 203. Austin JC, Postier RG, Elkins KC: Treatment of esophageal cancer: The continual need for surgical resection. Am J Surg 1986; 152:592-596. 204. Wolfe WG, Burton GV, Seigler HF, et al: Early results with combined modality therapy for carcinoma of the esophagus. Ann Surg 1987; 205:563-571. 205. Leichman L, Steiger Z, Seydel HI;, et al: Combined preoperative chemotherapy and radiation therapy for cancer of the esophagus: The Wayne State University Southwest Oncology Group and Radiation Therap?/ Oncology Group Experience. Semin Oncoi 1984; 11:178-185. 205a. Hilgenberg AD, Carey RW, Wiikens EW, et al: Preoperative chemotherapy, surgical resection and selective postoperative therapy for squamous cell carcinoma of the esophagus. Ann Thorac Surg 1988; 45:357-363. 206. Kolaric K, Maricic Z, Roth A, et al: Combination of bleomycin and Adriamycin with and without radiation in the treatment of inoperable esophageal cancer. Cancer 1980; 45:2265-2273. 207. Earle JD, Gelber RD, Moertel CG, et al: A controlled evaluation of combined radiation and bleomycin therapy for squamous cell carcinoma of the esophagus. Int J Radiat Oncol Rio1 Phys 1980; 6:X21-826.

Curr

Probl

Surg,

August 1988

606