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Surgical management of esophageal carcinoma.

Although esophageal carcinoma is not the most common tumor--it accounts for only 5% of all gastrointestinal tumors and 1% of all new tumors--it has nearly a 1:1 mortality ratio: each year there are 14,000 new cases and 13,000 related deaths in the USA. Men have esophageal carcinoma 3 to 5 times more often than women, and black men are 3 times more likely than white men to have the disease. The mean age at diagnosis is 60 years.

BACKGROUND

Adenocarcinoma, typically in the distal third of the esophagus, and squamous cell carcinoma, typically in the proximal two thirds of the esophagus, each make up 49% of cases of esophageal cancer. The remaining cancers in this area include sarcoma (1%), lymphoma (0.5%), cylindroma (0.25%), and primary melanoma (0.25%) (1). The incidence of adenocarcinoma is clearly increasing; it will soon become the most prevalent type of cancer of the esophagus. No malignant tumor in the past 25 years has increased in incidence as much as adenocarcinoma of the esophagus. The primary risk of adenocarcinoma is related to the duration and severity of gastric-esophageal reflux and the progression of mucosal changes from Barrett's esophagus to dysplasia to adenocarcinoma. Early detection is the most important factor in determining survival. Most patients present with stage IIB to stage IV disease, and most disease occurs at the gastroesophageal junction.

Among patients with Barrett's esophagus, the risk of developing adenocarcinoma is 0.2% to 2.1% each year; 77% of patients with adenocarcinoma have had Barrett's esophagus. Endoscopy with systematic biopsy cannot reliably exclude the presence of occult adenocarcinoma, since it could miss adenocarcinoma located somewhere else in that region. Forty percent of patients with Barrett's esophagus and dysplasia have invasive carcinoma in the resected specimen.

The incidence of squamous cell carcinoma, which used to be the major cause of esophageal cancer, has significantly decreased. The decrease may be related to reductions in risk factors, which include smoking, excessive alcohol use, caustic lye injury or thermal injury, diet, obesity, achalasia, and tylosis.

Typical symptoms of esophageal cancer include difficulty swallowing, with a feeling of fullness, pressure, burning, or coughing; a feeling of both liquids and solids becoming stuck behind the sternum; indigestion; emesis; and weight loss. Many patients attribute their symptoms to heartburn and do not seek the medical care they need.

STAGING

The staging system for esophageal carcinoma and its tumor, nodal, and metastatic components appears in Table 1. While T stage has remained the same over time, N2 disease has been taken out of the system, and M1 has been divided into 2 subgroups based on the area affected.

Endoscopy and biopsy are essential for determining whether the tumor is squamous carcinoma, Barrett's esophagus, or adenocarcinoma. However, multiple staging modalities are available, from physical examination to computed tomography (CT), endoscopic ultrasound, magnetic resonance imaging (MRI), positron emission tomography (PET), thoracoscopy/laparoscopy, bone scan, laryngoscopy, and bronchoscopy.

CT scan is used most frequently in diagnosis. While it clearly shows the presence of tumor, it is only 49% to 60% accurate in staging the depth of the tumor, according to published reports (2-7). Endoscopic ultrasound is significantly better in determining T stage, with an accuracy ranging from 76% to 92% (3, 4, 6-9). While few studies have examined MRI's success in determining T stage, it appears to be very promising, with an accuracy rate of 96% to 100% (10).

For staging lymph nodes, CT has shown an accuracy rate of 39% to 74% (2, 4, 6-9); endoscopic ultrasound, 45% to 100% (4, 7, 9, 11-13); MRI, 56% (14) and 74% (15); and PET, 76% (11), 84% (16), and 87% (17). Endoscopic ultrasound has not only shown enlargement of nodes but also has characterized specific pathologic and histologic features of carcinoma in the lymph nodes. Krasna and Luketich recently proposed a new staging technique involving combined thoracoscopy/laparoscopy with a >90% accuracy rate for staging these cancers. Several other investigators have duplicated these results, which entails thorough and sequential nodal analysis via the thorascope around the first-and second-level lymph node basins (16, 18-20). A number of randomized studies have shown that about 50% of these cancers are upstaged when thoracoscopy or laparoscopy is performed after endoscopic ultrasound.

The value of accurate staging is controversial. Since many patients present with an obstructing neoplasm, the clinical approach at one time involved an aggressive attempt at resection for palliation even when advanced nodal disease or metastatic disease was encountered at surgery. The advent of local ablation and nonoperative palliative management may make accurate staging more important.

TREATMENT OPTIONS

Once the disease has been staged, numerous treatment options are available. Stage 0 or I disease is usually treated with surgery alone. Stage II and III disease is often treated with surgery, with or without neoadjuvant therapy. Stage IV disease is often treated nonsurgically, with stents, neoadjuvant therapy, photodynamic therapy, brachytherapy, or immunotherapy--modalities that might help downstage the tumor in some patients.

Many studies have compared neoadjuvant chemotherapy plus radiation with radiation therapy alone. Only one study with 113 patients showed a significant improvement in the 3-year survival rate in patients who underwent neoadjuvant chemotherapy with radiation (37%) compared with those who underwent surgery alone (26%) (P < 0.01). However, many other studies involving over 1500 patients have not shown a similar advantage for neoadjuvant chemoradiation (Table 2).

Innovative gene therapy strategies may open the range of treatment options for esophageal cancer. Investigators at Baylor have presented data involving an adenoviral vector containing the gene for tumor necrosis factor along with a promoter region that is triggered by radiation therapy.

According to the National Cancer Institute, 39 clinical trials are currently active in the USA evaluating treatment or prevention modalities for patients with esophageal carcinoma. Some trials focus on chemoprevention with cyclooxygenase-2 inhibitors or nonsteroidal antiinflammatory agents.

For resection, surgeons use several techniques: 1) the Ivor-Lewis, a thoracoabdominal approach; 2) the transhiatal, involving the abdomen and neck while avoiding the thoracic incision; 3) the transabdominal, used particularly for cancers of the lower gastroesophageal junction; and 4) the thoracoscopic/laparoscopic, a minimally invasive approach.

After removing the esophagus, surgeons usually use the stomach to create a neoesophagus. A colon interposition is sometimes used when the stomach is not suitable. Concerns with the colon include its tenuous blood supply and the possibility of intrinsic disease. A last resort is a jejunal interposition, usually as a free graft or augmented vascular supply. Techniques for anastomosis include the traditional 2-layer hand-sewn, a single-layer absorbable hand-sewn, a stapled end-to-end, and a robot-assisted end-to-end.

Beitler and Urschel's review of 4 randomized trials and 7 nonrandomized comparative studies showed that stapled and hand-sewn anastomoses have equivalent leak rates, but strictures are more common in stapled anastomoses (26). Strictures can be easily treated with serial dilation, whereas a leak can be a catastrophic complication. Another metaanalysis of 9 randomized trials showed that if surgeons didn't perform a pyloric drainage procedure, the incidence of gastric outlet obstruction was significantly increased (27). However, the article did not address the fact that pyloric drainage procedures increase the risk of bile reflux; most patients with esophageal carcinoma have reflux.

OUTCOMES

One of the most important factors in surgical success is clear margins. Roder et al showed that survival duration was dramatically decreased if there was residual tumor: for example, in stage I disease, survival duration decreased from 79 months to 23 months in patients with residual tumor, and in stage IIB disease, survival duration decreased from 30 months to 6 months (28).

With all techniques, the 5-year survival rate averages 18% to 38% (Table 3). A metaanalysis of all published literature in the English language on transthoracic, transhiatal, and thoracoscopic/ laparoscopic procedures revealed that intensive care unit stay and total hospital length of stay were lower in the group treated with the transhiatal approach (Table 4). Hulscher et al followed up on their metaanalysis of transthoracic and transhiatal procedures with a randomized trial, which also showed that transhiatal procedures resulted in a shorter intensive care unit stay, shorter hospital stay, and lower frequency of pulmonary complications (all P < 0.001) but did not have a statistically significant effect on survival (40). While the thoracoscopic/laparoscopic procedures seem to yield better short-term survival rates, most of the literature on this procedure consists of case reports. Randomized studies are needed to see whether the technique actually offers better results or the reports reflect a selection bias.

In the largest prospective outcomes cohort in the literature, Bailey et al documented a near 50% morbidity rate and 10% mortality rate after esophagectomy in 1700 patients of Veterans Affairs facilities. Multivariate analysis revealed that neoadjuvant chemotherapy was the risk factor that best predicted 30-day mortality. Other predictors of mortality included greater age, intraoperative transfusions, ascites, and diabetes (41).

Overall, the 5-year survival rate is about 50% for stage I disease but drops precipitously for patients with higher-stage disease (28, 29, 42, 43). Similarly, having even 1 lymph node positive for disease decreases survival rates by 25% to 40%, and having 4 or more positive nodes is associated with a survival rate of [less than or equal to]5% (28, 44, 45). The 4 predictors of the worst 30-day survival rate after surgery were positive lymph nodes, higher-stage disease, blood transfusion of [greater than or equal to]3 units, and incomplete tumor resection (46).

DISTAL ESOPHAGECTOMY EXPERIENCE AT BAYLOR

Between 1992 and 2000, surgeons at Baylor treated 61 patients with cancer of the gastroesophageal junction. The mean age of the patients was 56 years (range 33-77); 53 of the 61 patients were men. Forty-eight had adenocarcinoma, 10 had squamous cell carcinoma, 1 had squamous cell carcinoma plus adenoma, and 2 had carcinosarcoma. Most patients had early stage disease and were thus good surgical candidates: 3 (5%) had stage 0 disease; 21 (34%), stage I; 15 (26%), stage IIA; 7 (11%), stage IIB; 8 (13%), stage III; and 7 (11%), stage IV.

Twenty-eight patients (46%) received neoadjuvant therapy, consisting of a combination of cisplatin, 5-fluorouracil, and 45 Gy of radiation. After this therapy, 5 patients--all with squamous cell carcinoma--had a complete response in their primary tumor. One of 3 procedures was used, depending on surgeon preference and patient needs (curative or palliative): 21 patients underwent the Ivor Lewis procedure; 38, the transhiatal procedure; and 2, the transabdominal procedure. The transhiatal approach was used more in the later years as its superiority in decreasing morbidity was recognized. A gastric conduit was used in 58 patients and a colon interposition in 3 patients. The complications of vocal cord paralysis and stricture were all associated with transhiatal esophagectomies. The complications of anastomotic leak and respiratory failure occurred with the Ivor-Lewis procedure. Two patients died within 30 days of this operation; both were severely ill (Table 5).

After follow-up intervals ranging from 3 months to 8 years (mean 5 years), the 5-year age-matched expected survival rate was 87%. Our actual observed survival rates were 66% for carcinoma and 100% for dysplasia/high-grade Barrett's esophagus.

SUMMARY AND PROPOSED TREATMENT ALGORITHM

Some summary points from the review are as follows:

* In tumor staging, endoscopic ultrasound and/or MRI are both more accurate than CT scan.

* In nodal staging, the thoracoscopic/laparoscopic approach has been found to be more accurate than endoscopic ultrasound, which is better than PET scan, MRI, and CT scan.

* Neoadjuvant therapy is still investigational. While it may have a role in downstaging--several studies showed a 30% to 40% downstaging success rate--it has increased morbidity rates both intraoperatively and postoperatively and causes patient dropout from protocol due to the toxicities of the therapy.

* The hand-sewn anastomosis technique leads to more leaks, while stapled anastomosis leads to more strictures.

* If pyloric drainage is not performed, there is a significant risk of gastric outlet obstruction, which is counteracted by the risk of having chronic bile reflux.

* There is no difference in survival rates between the transthoracic and transhiatal approaches. Thoracoscopy/laparoscopy appears to yield better survival statistics, but more study is required.

[FIGURE 1 OMITTED]

Based on the analysis and our data, a standardization of therapy is proposed (Figure). Upon diagnosis with esophagogastroduodenoscopy with biopsy, the patient would undergo a CT scan, mainly to look for distant metastases. If the CT scan showed that the cancer was stage I through III, the patient would undergo endoscopic ultrasound with fine-needle aspiration. Any time stage IV disease was diagnosed, the patient would receive nonoperative therapy. PET scans and thoracoscopic/laparoscopic staging would be used to further determine if tumor necrosis factor gene therapy or neoadjuvant therapy were needed to downstage the tumor before proceeding to surgery for a curative or palliative operation.

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AMIT N. PATEL, MD, MS, JOHN T. PRESKITT, MD, JOSEPH A. KUHN, MD, ROBERT F. HEBELER, MD, RICHARD E. WOOD, MD, AND HAROLD C. URSCHEL, JR., MD

From the Departments of General Surgery (Patel, Preskitt, Kuhn) and Cardiothoracic Surgery (Hebeler, Wood, Urschel), Baylor University Medical Center, Dallas, Texas.

Presented at surgical grand rounds, Baylor University Medical Center, Dallas, Texas, January 2003.

Corresponding author: Amit N. Patel, MD, MS, Department of Surgery, Baylor University Medical Center, 101 N. Brookside Drive, Suite 102, Dallas, Texas 75214 (e-mail: anpatel72@hotmail.com).
Table 1. Staging of esophageal carcinoma *

Stage Grouping

Stage 0 Tis N0 M0
Stage I T1 N0 M0
Stage IIA T2 N0 M0
 T3 N0 M0
Stage IIB T1 N1 M0
 T2 N1 M0
Stage III T3 N1 M0
 T4 Any N M0
Stage IV Any T Any N M1
Stage IVA Any T Any N M1a
Stage IVB Any T Any N M1b

Definition of TNM

Primary Tumor (T)

TX Primary tumor cannot be assessed
T0 No evidence of primary tumor
Tis Carcinoma in situ
T1 Tumor invades lamina propria or submucosa
T2 Tumor invades muscularis propria
T3 Tumor invades adventitia
T4 Tumor invades adjacent structures

Regional Lymph Nodes (N)

NX Regional lymph nodes cannot be assessed
N0 No regional lymph node metastasis
N1 Regional lymph node metastasis

Distant Metastasis (M)

MX Distant metastasis cannot be assessed
M0 No distant metastasis
M1 Distant metastasis

 Tumors of the lower thoracic esophagus:

 M1a Metastasis in celiac lymph nodes
 M1b Other distant metastasis

 Tumors of the midthoracic esophagus:

 M1a Not applicable
 M1b Nonregional lymph nodes and/or other distant metastasis

 Tumors of the upper thoracic esophagus:

 M1a Metastasis in cervical nodes
 M1b Other distant metastasis

* Used with the permission of the American Joint Committee on Cancer
(AJCC), Chicago, Illinois. The original source for this material is the
AJCC Cancer Staging Manual, Sixth Edition (2002) published by
Springer-Verlag New York, www.springer-ny.com.

Table 2. Median survival duration and 3-year survival rate with and
without neoadjuvant therapy for esophageal carcinoma

 Median survival 3-year survival
 (months) rate (%)

 Neo Neo
Trial N Surgery + surg Surgery + surg P value

Walsh (21) 113 11 16 26 37 <0.01
Law (22) 147 13 16.8 31 44 NS
Kelsen (23) 467 16.1 14.9 37 35 NS
Clark (24) 802 13.3 17.2 34 43 NS
Ancona (25) 96 24 25 41 44 NS

Table 3. Results of esophagectomy

 5-year
 Mortality Morbidity survival
Study Type N rate (%) rate (%) rate (%)

Skinner (29) En bloc 80 11 52 18
Altorki (30) En bloc 78 5 58 33
Altorki (31) En bloc 111 5 49 37
Orringer (32) THE 100 12 38 15
Orringer (33) THE 1085 4 26 32
Rao (34) THE 411 11 27 38
Mannell (35) Total 93 12 45 13
King (36) RT 100 3 27 15
Lozac'h (37) RT 264 2 23 27

THE indicates transhiatal esophagectomy; RT, right thoracotomy.

Table 4. Metaanalysis comparing types of operation for
esophageal carcinoma

 THLA
 Transthoracic * Transhiatal * ([dagger])
 (n = 4591) (n = 3383) (n = 274)

ICU stay (days) 11.2 9.1 3.6
Hospital stay (days) 21.0 17.8 11.2
In-hospital 9.2 5.7 2.7
 mortality (%)
Wound infection (%) 7.7 4.3 1
Vocal cord 3.5 9.5 0
 paralysis (%)
3-year survival (%) 27 25 58 (double
 dagger])
5-year survival (%) 35.2 24.9 --

* From reference 38.

([dagger]) From reference 39 and other sources.

(double dagger]) Value represents 30-month survival rate rather than
3-year survival rate. ICU indicates intensive care unit; THLA,
thoracoscopy/laparoscopy.

Table 5. Operative mortality and morbidity rates for 61 esophageal
cancer patients at Baylor University Medical Center

Complication n %

Death 2 3
Anastomotic leak 4 7
Respiratory failure 3 5
Vocal cord paresis 3 7
Psychosis 2 3
Deep vein thrombosis 1 2
Atrial fibrillation 2 3
Myocardial infarction 1 2
Anastomotic stricture 7 11
Major wound infection 0 0
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Author:Patel, Amit N.; Preskitt, John T.; Kuhn, Joseph A.; Hebeler, Robert F.; Wood, Richard E.; Urschel, H
Publication:Baylor University Medical Center Proceedings
Article Type:Disease/Disorder overview
Geographic Code:1U7TX
Date:Jul 1, 2003
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