Malignant conditions involving the oesophagus, stomach, small intestine, gall bladder and bile duct

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CHAPTER 6 MALIGNANT CONDITIONS INVOLVING THE OESOPHAGUS, STOMACH, SMALL INTESTINE, GALL BLADDER AND BILE DUCT

KEYPOINTS

• In upper gastrointestinal tumours, accurate preoperative staging is important in determining appropriate management.
• Accurate staging includes clinical assessment and investigation of tumour and patient factors.
• Stage of disease directly correlates with outcome.
• Newer modalities of investigation include capsule endoscopy, endoscopic and laparoscopic ultrasound.
• Multidisciplinary care is now standard.
• Multimodality therapies are now common.

OESOPHAGOGASTRIC CANCERS

Gastric cancer incidence and mortality has fallen dramatically over the last 50 years in many regions, but probably remains the second most common cancer worldwide. The likely cause for this reduction is the disappearance of Helicobacter pylori and possibly greater consumption of fruit and vegetables, the reduced intake of salted, pickled and preserved foods, and improvements in refrigeration.

The incidence of gastric cancer varies worldwide, with the highest incidence being in Japan. Low rates can be expected in North America, India, Australia and New Zealand and northern Europe. The rates are also higher generally in lower socioeconomic groups and in males (male to female ratio 2:1). Gastric cancer is largely a disease of older age groups in most countries.

Despite a marked decline in fundal and distal tumours, there is a rising incidence of adenocarcinomas of the gastro-oesophageal junction and gastric cardia, particularly in Western nations, and predominantly in males. Comparatively high rates of this tumour are evident for the United Kingdom/Ireland, northern Europe, Australia and New Zealand, China and North America. The increase in incidence of cardia lesions has been associated with parallel increases for adenocarcinomas of the lower oesophagus, where hyperacidity, reflux oesophagitis, Barrett’s oesophagus and obesity have been proposed as likely risk factors. This may imply that there are, in fact, two diseases differing from each other in epidemiology, aetiology, pathology and clinical expression. It is important to distinguish cardia and lower-third oesophageal adenocarcinoma from gastric cancer invading the lower third of the oesophagus, as treatment options may vary.

Clinical

Common presenting symptoms include weight loss, abdominal pain, nausea, anorexia and dysphagia. Easy satiety, reflux symptoms and symptoms of anaemia may be present. Background history may include previous peptic ulcer, previous history of polyps (gastric or colonic) and should include assessment of risk factors. A careful history of factors that may increase operative morbidity and mortality should also be sought (cardiac, respiratory, other systemic illness, anticoagulants, etc).

Risk factors

Oesophageal

There is a strong association between smoking and alcohol consumption and oesophageal squamous cell cancer. Human papilloma virus may be an important causative agent for oesophageal (squamous cell) cancer. Other risk factors include achalasia, chemical strictures, diverticula, previous radiation therapy and post-cricoid webs. Barrett’s mucosa predisposes to oesophageal adenocarcinoma, as does smoking and obesity, while aspirin use may be protective.

Gastric

Precursors of gastric cancer include chronic gastritis (autoimmune and acquired), intestinal metaplasia/dysplasia, gastric polyps (adenomatous polyps, rare in hyperplastic polyps) previous gastrectomy (>15 y post resection), pernicious anaemia and, most importantly, Helicobacter pylori infection. Infection with H. pylori induces chronic gastritis. Whether treatment of H. pylori infection will diminish the risk of gastric cancer is currently under investigation.

Dietary factors are important. A high consumption of fruit and vegetables is negatively correlated with risk of gastric cancer. These food items are thought to have a protective antioxidant effect. A high intake of salted foods, and potentially of smoked, cured and pickled foods, is thought to be a risk factor. These foods may include elevated levels of N-nitroso compounds, which have been shown to be potent carcinogens in animal experiments. There is also additional preliminary evidence that high-nitrate and high-starch diets may be risk factors, whereas garlic, onions and green tea may have protective effects. Ionising radiation is an established cause, based on exposure to radiation from atomic bombs and radiation therapy in certain patient groups (ankylosing spondylitis). Consumption of alcohol is weakly associated with gastric cancer, and smokers have an increased risk generally. There is a small group of patients in whom hereditary factors are important.

Examination

General physical examination may be unremarkable. However, nutritional assessment is important. Advanced disease may be identified by the presence of an epigastric mass, nodes in the left supraclavicular fossa, the presence of ascites, or a pelvic mass palpable on rectal examination as a result of peritoneal spread of tumour.

Investigations

Contrast studies

Seldom used in the diagnosis and investigation of oesophageal tumours, but barium swallow may be used in the investigation of a patient with dysphagia.

Computed tomography (CT) scanning

Of value in oesophageal cancer for the detection of distant metastases, particularly liver and pulmonary metastases. It can detect tracheal or bronchial invasion in up to 90% of cases, and the identification of pleural and pericardial involvement is similar. It is less accurate in the detection of nodal metastases (70% accuracy) and assessment of the cardio-oesophageal area, and the presence of diaphragmatic involvement is less secure with CT scanning. In gastric cancer, overall detection rates of the primary tumour approach 90%, but requires a high-resolution scanner, and distension of the stomach with water and contrast. CT has an accuracy of 70% in detection of nodal metastases, and the detection of distant metastases is similar to oesophageal cancer.

Magnetic resonance imaging (MRI)

Provides similar results to CT scanning.

Endoscopy

Along with accompanying biopsy, endoscopy is an important part of the investigation of a patient with suspected oesophageal or gastric cancer.

For oesophageal cancer, 100% of early cancers can be diagnosed. The number of biopsies increases diagnostic accuracy. Advanced cancers can appear polypoidal, ulcerative or diffusely infiltrative. Barrett’s mucosa can also be identified, and multiple biopsies should be performed to identify areas of high-grade dysplasia.

For gastric cancer, endoscopy can identify the site, the nature and the degree of involvement and the dimensions of the tumour. Biopsy can identify the tumour type, as the diffuse type of tumour (secreting mucin, and with no gland formation) has a worse prognosis than the intestinal tumour (which forms glandular structures). Chronic gastritis can also be identified.

Bronchoscopy

An important additional investigation in upper and middle-third oesophageal cancer to assess for evidence of invasion. Endoscopic ultrasound may be able to assess this.

Endoscopic ultrasound (EUS)

A useful tool in the preoperative staging of both oesophageal and gastric cancers, and its use provides superior results to CT in the local staging of these tumours. EUS can identify involved lymph nodes in up to 90% of cases, but is less accurate in early stage disease. EUS has a central role in the initial anatomic staging of oesophageal cancer because of its high accuracy in determining the extent of locoregional disease. EUS is inaccurate for staging after radiation therapy and chemotherapy, but can be useful in assessing treatment response. For initial anatomic staging, EUS results have consistently shown more than 80% accuracy compared with surgical pathology for depth of tumour invasion. Accuracy increases with higher stage, and is >90% for T3 cancer. EUS results have shown accuracy in the range of 75% for initial staging of regional lymph nodes. EUS has been invariably more accurate than computed tomography for tumour (T) and lymph node (N) staging. EUS is limited for staging distant metastases (M), and therefore EUS is usually performed after assessment for distant metastases by CT scanning or positron emission tomography. Pathologic staging can be achieved at EUS using fine-needle aspiration (FNA) to obtain cytology from suspect lymph nodes. FNA has had greatest efficacy in confirming coeliac axis lymph node metastases with more than 90% accuracy. EUS is inaccurate for staging after radiation and chemotherapy because of its inability to distinguish inflammation and fibrosis from residual cancer, but a decrease in tumour cross-sectional area or diameter of more than 50% has been found to correlate with treatment response. Stricture due to tumour precludes full assessment of tumour size and nodal status, and dilatation to allow passage of the probe results in a high perforation rate. EUS offers the best preoperative local gastric cancer staging, with accuracies in T and N staging of approximately 78% and 70%, respectively. Although EUS is not suitable for diagnosing distant metastases, it may be more useful in detecting ascites due to the close proximity to the peritoneum.

Laparoscopy

Can be performed as a separate procedure prior to final choice of therapy. Laparoscopy can identify occult peritoneal and hepatic disease in up to 25% of potentially resectable gastric cancers, thus allowing informed decision making in relation to a more significant abdominal operation. It also allows consideration of other palliative modalities.

Laparoscopic ultrasound

May combine the benefits of detection of occult metastases (laparoscopy) and nodal status (EUS). Resectability (up to 100%), TNM staging (82% accurate), nodal status (92%), T stage (96%), M stage (89%) are all significantly improved over laparoscopy alone for oesophagogastric tumours, and is as accurate as EUS. Laparoscopic ultrasound may be the optimal preoperative staging tool, and may have a complementary role to EUS in oesophageal cancer.

Management

Oesophageal cancer

The majority of cancers arising in the oesophagus are epithelial in origin (squamous or adenocarcinoma in the lower third).

Once preoperative staging has been completed, selection of primary treatment will depend on the results of staging, and the fitness of the individual patient. Radical treatment is not indicated in an infirm patient. Survival is directly correlated to stage of disease, and therefore accurate preoperative staging is important to determine whether radical treatment is indicated.

The management of oesophageal squamous cell cancer has evolved from surgery alone to definitive chemoradiation or preoperative chemotherapy or chemoradiation followed by surgery. Preoperative chemoradiation can result in a higher rate of complete resection (R0), but may result in a higher postoperative morbidity and mortality. Definitive chemoradiation has resulted in overall survival and local control rates that are comparable with those achieved with surgery alone and has been proven to be superior to radiation alone. Surgery remains the standard to which all other modalities are compared and is an acceptable option for patients with early-stage disease. For patients with locally advanced disease who are not surgical candidates, definitive chemoradiation with concurrent and adjuvant cisplatin/fluorouracil is the present standard of care.

Management of adenocarcinoma in this area is more difficult. Surgical management depends on the primary site. Oesophageal resection of lower-third adenosarcomas is the recommended surgical treatment. Radical gastric surgery is the recommended option for cardia tumours and proximal gastric cancers, with or without left thoraco-abdominal exposure. The use of neoadjuvant treatment of these tumours is evolving. Epirubicin, cisplatin and infused fluorouracil (ECF) shows significant benefit in advanced oesophagogastric cancer, particularly locally advanced disease.

Perioperative chemotherapy (pre- and postoperatively) significantly improves resectability, progression-free survival and overall survival in operable gastric and lower oesophageal cancer. Postoperative chemoradiation may be as beneficial as perioperative chemotherapy for cardia tumours.

Gastric cancer

While surgical resection remains the cornerstone of gastric cancer treatment, the optimum extent of nodal resection remains controversial, with randomised studies failing to show that the D2 (more extensive) procedure improves survival when compared with D1 dissection. This is despite data from Japan showing a survival advantage in Japanese patients. The use of neoadjuvant therapy may benefit selected patients, but may only be relevant to those patients who have a favourable response to treatment. The high rate of recurrence and poor survival following surgery provides a rationale for the early use of adjuvant treatment. Adjuvant chemotherapy or adjuvant radiotherapy used alone, do not improve survival following resection. In advanced gastric cancer, chemotherapy enhances quality of life and prolongs survival when compared with best supportive care.

Radiation can be employed for palliative treatment of bleeding gastric cancers with relief of symptoms in an acceptable number of patients.

GASTROINTESTINAL STROMAL TUMOURS (GIST)

These tumours, formerly known as leiomyomas and leiomyosarcomas, are now thought to be derived from undifferentiated stromal fibroblasts. Behaviour of these tumours correlates with the number of cells undergoing mitosis per high power field (<5 versus >5). They may be found on endoscopy, may present as a mass lesion, and can present as a result of upper gastrointestinal bleeding. Larger tumours tend to be at the malignant end of the spectrum. Recent addition of tyrosine kinase inhibitors has changed the management of these tumours. If resection is possible, gastric resection is performed. If resection is not possible, the addition of preoperative medical therapy can downstage these tumours to a resectable size. The addition of medical therapy post operatively is currently under investigation.

CARCINOMA OF GALL BLADDER

This tumour represents a small percentage (<2%) of all cancers but is the most common site of cancer in the biliary tract (80%–95% of cancers of the biliary tree). The incidence varies worldwide and the highest incidence occurs in the Andean area, in North American Indians and Mexican Americans. It is three times more common in women than in men in all populations. The highest rates in Europe are in Poland, the Czech Republic and Slovakia, and in Asia in northern and north-eastern India.

Aetiology and risk factors

Up to 85% of patients with gall bladder cancer have gallstones. This appears to be relevant if the stones are symptomatic over a long period of time. Other risk factors include obesity, chronic infections of the gall bladder (Salmonella typhi) and environmental exposure to chemicals (occupations in oil, paper, chemical, shoe, textile and cellulose acetate fibre manufacturing industries). The incidence is increased 14-fold 20 years after surgery for gastric ulcer. There is an association with porcelain gall bladder (calcification of the gall bladder wall), familial adenomatous polyposis (FAP)/Gardner’s syndrome. There is a high incidence of anomalous bile duct–pancreatic duct junction (pancreatic duct joins bile duct) in patients with gall bladder cancer.

Clinical presentation

The peak age incidence is over 70 years. Gall bladder cancer may be asymptomatic and is identified either on ultrasound before laparoscopic cholecystectomy, or histologically after resection for symptomatic gallstones. Less than 30% of patients are diagnosed preoperatively, and usually only those with advanced disease. The majority of these patients will present with jaundice, due to direct invasion of the hilum by the cancer.

Presentation of more advanced cancers include biliary obstruction (biochemically or clinical jaundice), acute cholecystitis or empyema.

Investigation

Biochemistry may confirm cholestasis and jaundice. Coagulation profile is important in jaundiced patients. Plain abdominal X-ray may show gall bladder calcification. Ultrasound may show a mass. CT can confirm this, and may show contrast enhancement of the suspected cancer. EUS can be helpful in preoperative staging.

Management

Surgical therapy is appropriate for disease that is localised and resectable. Laparotomy should be considered if gall bladder cancer is suspected preoperatively. Laparoscopy may be helpful in staging these patients, and may avoid laparotomy if disease is advanced. If gall bladder cancer is not suspected preoperatively, but is suspected intraoperatively, operative management ranges from completion of laparoscopic cholecystectomy, with removal of the gall bladder in a bag to avoid contamination of the port site, to laparotomy and extended resection of the gall bladder bed and regional hepato-duodenal lymph nodes. The choice will depend on operative findings and the comorbidities of the individual patient. Postoperative chemoradiotherapy may benefit selected patients. There is evidence that implantation of tumour cells may occur in port sites after laparoscopic cholecystectomy, and the biological aggressiveness of the tumour is the most likely explanation for this phenomenon as opposed to poor operative technique.

Prognosis

Most large studies of gall bladder cancer demonstrate 5%–15% overall 5-year survival. Pathologic stage remains the best prognostic factor. Most gall bladder cancers are adenocarcinomas, with a small percentage represented by adenosquamous cancer and other rare types. Early stage disease has a better prognosis, and resected disease has a better prognosis than non-resected disease (52% versus 19% for stage IV disease, respectively).

CHOLANGIOCARCINOMA

Carcinoma of the bile duct is an uncommon tumour. The overall number of cases curable by surgery is approximately 10%. Prognosis is related to anatomical location, which, in turn, determines the resectability.

Pathogenesis

There is a strong association with primary sclerosing cholangitis (PSC) and with inflammatory bowel disease. Chemical carcinogens implicated in aetiology include aflatoxin, methylene chloride and vinyl chloride monomer, with industrial exposure in factory workers. There is an increase in risk for choledochal cysts, which probably relates to an anomaly of the pancreaticobiliary junction, resulting in a common channel of variable length (bile duct joins pancreatic duct).

Pathology

The tumours are usually mucus-secreting adenocarcinomas, arising from the epithelium of any part of the biliary tract. These tumours can be multifocal. Tumours in the middle third of the bile duct are usually nodular in appearance. Lower-third tumours are generally papillary, and hilar tumours tend to be stenosing and sclerotic. Perineural invasion is a negative prognostic factor. The tumour can invade adjacent structures, including the liver, and adjacent blood vessels, including the hepatic artery and the portal vein.

Clinical

Cholestatic jaundice is the usual presentation, with or without preexisting cholestasis without jaundice. The disease may be extensive by the time jaundice develops. Systemic features of malignancy may be present, including weight loss and anorexia. Fever may be present owing to coexistent cholangitis. A history of inflammatory bowel disease should be looked for. Nutritional assessment is important, as is the assessment of medical comorbidities in relation to operative risk.

Investigations

Liver function tests will confirm the cholestatic nature of the jaundice and the level of bilirubin. Coagulation studies should be performed especially international normalised ratio (INR), particularly if endoscopic or surgical intervention is contemplated. Carcinoembryonic antigen (CEA) is expressed in the cells of cholangiocarcinomas and may be elevated in the serum. Cancer antigen 19-9 (CA 19-9) may also be elevated, but modest levels of this marker can also be found in inflammatory and infective bile duct pathology. Chronic anaemia may also be present, and a raised white cell count may suggest associated biliary sepsis. Nutritional assessment is also important.

Imaging

Ultrasound

Can identify the level of obstruction in most cases, and can identify gallstones in the gall bladder. Ultrasound may identify a tumour mass and suggestion of vascular invasion may be raised. Liver secondaries may also be identified.

CT scanning

Using three phase scanning, may show a mass lesion with or without local extension or lymphadenopathy. Lobar or segmental atrophy may also be identified (due to gradual, progressive bile duct obstruction, especially in tumours arising primarily in left or right main bile ducts in the hilum).

Cholangiography

Is important to develop a road map of duct obstruction, especially if surgery is contemplated. Endoscopic retrograde cholangiography (ERC) can outline the level of obstruction from below, and cytology may be positive with brushings. Placement of a stent (either temporary or permanent) can also be accomplished. Percutaneous transhepatic cholangiography (PTC) can delineate the proximal ducts, and is especially important in more proximal-based tumours. Communication between the right and left bile ducts can also be outlined, and this may be important in the planning of surgical decompression.

Endoscopic ultrasound (EUS)

May also be used to delineate bile duct anatomy, presence or absence of nodal metastases, and cytological diagnosis may be possible. This may be useful if surgical resection is not contemplated by virtue of stage of disease or because of patient comorbidity. With respect to accuracy of EUS, the sensitivity, specificity, positive predictive value, negative predictive value and accuracy can be as high as 86%, 100%, 100%, 57% and 88%, respectively. EUS-FNA can have a positive impact on patient management in up to 84% of patients: preventing surgery for tissue diagnosis in patients with inoperable disease, facilitating surgery in patients with unidentifiable cancer by other modalities and avoiding surgery in benign disease. Given the apparent accuracy and safety of EUS with FNA for imaging bile duct mass lesions and for obtaining a tissue diagnosis in patients with suspected cholangiocarcinoma, EUS may represent a new approach to diagnosis, especially when CT and endoscopic retrograde cholangiopancreatography (ERCP) fail. The ability to obtain a definite diagnosis has a significant impact on patient management in a significant proportion of patients.

Selective angiography

May identify hepatic arterial and portal venous involvement prior to surgery. If the main portal vein is involved, resection may be difficult or impossible. If a left bile duct hilar cholangiocarcinoma involves the right portal vein or hepatic artery, curative resection is not possible as preservation of the opposite lobe blood supply is required (and similarly for a right hilar cholangiocarcinoma).

Management

The aims of treatment are to:

• resect the primary tumour, if possible
• relieve jaundice
• treat and/or prevent cholangitis.

As a minority have surgically resectable disease, the majority of patients require biliary drainage. The options for drainage include operative drainage, endoscopic drainage and stenting, percutaneous drainage, or combined percutaneous and endoscopic approaches.

Other modalities of treatment include radiation therapy using iridium-192 with additional external beam radiation. There is some evidence that this regimen can increase 2-year and median survival for combined doses >55 Gy. Photodynamic therapy has also been used to delay biliary occlusion in unresectable cases. The place of chemotherapy for this group of patients is in evolution, with newer agents (gemcitabine, capecitabine and platin-based regimens) showing some promise in phase II trials.

The survival of patients with bile duct cancer will depend on how advanced it is. Statistically, overall only about 21% of patients with extrahepatic bile duct cancer survive 5 years, because most patients are diagnosed late.

Both stage III and stage IV are considered unresectable, indicating that the cancer cannot be completely removed surgically.

SMALL INTESTINAL TUMOURS

The small intestine, which is about 3 m in length and comprises over 60% of the mucosal area of the gastrointestinal tract, is the major site for nutritional absorption, and is relatively resistant to carcinogenesis. Small intestine carcinoma is rare compared with other parts of the gastrointestinal tract and accounts for approximately 2% of gastrointestinal malignancies, compared with 10% oesophageal, 10% stomach, and 70% from the colon and rectum. Adenocarcinoma accounts for 40%–60% of small intestine malignancies. The remainder include carcinoid tumours, lymphomas, gastrointestinal stromal tumours (GIST), sarcomas and metastases from breast, melanoma, lung and renal cell cancers.

Small intestine cancers occur most frequently in the sixth and seventh decades, and are slightly more common in men. Adenocarcinomas occur in decreasing frequency from duodenum to ileum. Other primary tumours occur in increasing frequency from proximal to distal small intestine. There is an association with coeliac disease and small intestinal lymphoma, and adenocarcinoma is associated with hereditary colorectal cancer syndromes, particularly duodenal tumours in familial adenomatous polyposis (FAP), hereditary non-polyposis colorectal cancer and Peutz-Jeghers syndrome. Small intestine adenocarcinomas are also more common in patients with Crohn’s disease affecting the small intestine.

The 5-year relative survival is low for adenocarcinomas (20%–40%). Reasons for this are not clear, but these outcomes may relate to the relatively uncommon nature of the tumour, and diagnostic delays which occur as a result of the anatomical site.

Clinical

Clinically, most patients with small bowel adenocarcinoma have nonspecific signs and symptoms. The more frequent symptoms include abdominal pain and postprandial fullness (experienced by 50% of patients). Anaemia (up to 70%) and signs and symptoms of intestinal obstruction (50%) are common presentations. Up to 20% of patients may present acutely with either bleeding or obstruction, and require more urgent intervention. Other symptoms include weight loss, anorexia and fatigue. Perforation with accompanying peritonitis is an uncommon presentation.

Investigations

Endoscopy is useful for the diagnosis of duodenal adenocarcinoma, but has limited application in the investigation of more distal lesions. Push enteroscopy and double-balloon enteroscopy may be useful, usually in concert with capsule endoscopy, which employs wireless technology. These latter techniques may provide preoperative confirmation of tumours, but are not yet widely available.

CT is important in the assessment of the abdominal cavity and staging, but has variable detection rates—50% rising to 80% for detection of metastatic disease in some series.

The barium contrast study is another useful diagnostic tool, but has limited sensitivity. Small intestine enema is more sensitive than a small bowel follow-through series.

If all investigations are negative, and the index of suspicion is high, surgical intervention, either laparoscopic or open, may be indicated.

Management

Surgical resection is the gold standard of care for adenocarcinoma. Earlier stage tumours tend to occur more proximally, and this may relate to the earlier development of symptoms, and earlier detection.

Early tumour stage (stage 1 and 2) and curative resection are the only independent factors for better prognosis and long overall survival time. Lymph node metastasis is an independent predictor of disease-free survival, and probably accounts for the differences in outcome by stage. Patterns of failure post resection include peritoneal recurrence, wound recurrence, liver metastases and metastases in more distant sites, including the lungs. The role of adjuvant systemic therapy in higher risk patients is unknown.

Other tumours of the small intestine include carcinoid tumours, lymphomas, and GIST. Most small intestine carcinoids are clinically silent, and may present with local complications requiring emergent surgery, or present as metastatic disease. The rate of lymph node involvement and the prognosis of carcinoid tumours depend on their site and size. Lymph node metastases are most commonly found with small bowel carcinoids (20%–45%), providing the rationale for extended resection including the adjacent lymph node drainage area. More aggressive treatment is reserved for younger and fitter patients.

Management of GIST is similar to gastric GIST. Lymphoma may require resection if perforation, obstruction or bleeding occur. Chemotherapeutic regimens will depend on haematological advice.

FURTHER READING

American Society of Clinical Oncology website: www.asco.org. This site provides access to journal articles related to cancer topics.

Garden OJ. A companion to specialist surgical practice. Hepatobiliary and pancreatic surgery. Edinburgh: Elsevier; 2005.

Griffin SM, Raimes SA. A companion to specialist surgical practice. Upper gastrointestinal surgery. Edinburgh: Elsevier; 1997.

National Cancer Institute website: www.cancer.gov. The US National Institute of Health provides a good overview of current treatment of various cancers, including supporting level of evidence where available.

Pearson FG, Cooper JD, Deslauriers J, et al. Esophageal surgery. Philadelphia: Elsevier; 2002.

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