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Holzheimer RG, Mannick JA, editors. Surgical Treatment: Evidence-Based and Problem-Oriented. Munich: Zuckschwerdt; 2001.
Introduction
When one thinks of cancer of the gastrointestinal (GI) tract, one's first thoughts go to cancers of the large intestine and stomach, rather than the small intestine, despite the fact that the small intestine contains 75% of the length of the alimentary tract, with 90% of its surface mucosal area. There are approximately 4800 new cases of small bowel cancer each year in the U.S., with 1200 deaths (1). It is the surprising rarity of small bowel cancer which makes this disease process particularly interesting since it may provide clues as to preventive strategies for the more common and fatal malignancies.
Relatively little has been published about the clinical features and management of small bowel cancer. While there are four major histologic subtypes of cancer of the small intestine (i.e., adenocarcinoma, malignant carcinoid, lymphoma, and leiomyosarcoma), this chapter focuses on adenocarcinoma of the jejunum and ileum (duodenal adenocarcinomas are discussed in chapter 57).
Incidence
Adenocarcinoma of the jejunum and ileum tends to be more common in Western industrialized countries than in other regions of the world (2, 3). This does not appear to be fully accounted for by differences in access to diagnostic technology or healthcare.
For Western countries, adenocarcinomas generally represent the largest fraction of these series, while lymphomas predominate in other countries (4–21). Population-based data from the Surveillance, Epidemiology and End-Results Program (SEER) of the U.S. National Cancer Institute for 1973–1982, which represents approximately 10% of the US population, indicate that 48.4% of adenocarcinomas of the small bowel are located in the duodenum, with 32.5% in the jejunum and 19.2% in the ileum (22). Our own group (23) updated this SEER analysis (1973–1990) and found a rate of 54% in the duodenum, with 28% in the jejunum and 18% in the ileum. The cause of this propensity for adenocarcinomas to occur in the duodenum in contrast to the jejunum/ileum is unknown. Lowenfels and others (24, 25), have ascribed this difference in risk to the higher concentration of bile and its metabolites in the duodenum, secondary to the presence of the ampulla of Vater.
In general, adenocarcinoma of the small bowel predominates in males as compared to females, with a male to female ratio of approximately 1.4 (22, 23). Our study indicates a higher incidence of adenocarcinoma in blacks than in whites (23). This racial distribution of small bowel adenocarcinoma was confirmed by a review of the Los Angeles County Cancer Surveillance Program (25).
Etiology
The strongest known risk factor for small bowel adenocarcinoma is prior Crohn's disease, initially reported by Ginsburg et al., in 1956 (26). The relative risk of adenocarcinoma of the small bowel for patients with Crohn's disease has been estimated at between 15 and > 100 (27–29). Lashner (27) suggested that the use of 6-mercaptopurine for treating Crohn's disease raised the risk of developing subsequent cancer, as did significant Crohn's disease in the jejunum. Crohn's-associated adenocarcinomas generally occur in the ileum, reflecting the subsite distribution of Crohn's disease. The risk of adenocarcinoma does not begin until at least 10 years after the onset of Crohn's disease and typically occurs more than 20 years afterward.
One study has suggested that animal fat intake was correlated with the incidence of small bowel carcinoma (30). Another study (31) suggested that the intake of red meat or salt cured or smoked food raised the risk of small bowel cancer. Other risk factors have also been suggested for adenocarcinoma of the small bowel, including cigarette smoking, alcohol consumption, prior peptic ulcer disease, familial adenomatous polyposis, prior colon cancer, celiac sprue, and cystic fibrosis (3). Bile may also be involved (24, 25) since prior cholecystectomy may be related to the incidence of adenocarcinoma (32).
Adenocarcinoma of the small and large bowel share many characteristics. The incidence rates of these two diseases have been shown to correlate in a linear fashion when compared between countries (33). Furthermore, there is an elevated risk for large bowel adenocarcinoma and small bowel adenocarcinomas to occur in the same individuals (34). Both types of cancer appear to develop from adenomatous polyps (35). In particular, familial adenomatous polyposis raises the risk for both malignancies since it is associated with diffuse small and large bowel polyps. Recent preliminary studies exploring molecular genetic changes in small bowel adenocarcinomas have suggested that they also parallel the molecular genetic changes which occur in colorectal carcinogenesis (36).
This raises the question of the relative incidence of both diseases. Colorectal cancer represents one of the most common cancers in the United States, while small bowel adenocarcinoma is one fiftieth as common (1, 3). The reason for this disparity is not known, but potential explanations include the extremely rapid turnover of small intestinal mucosal cells (37), which would tend to eliminate partially transformed intestinal cells prior to their reaching full carcinogenic development; the relative absence of bacteria in the small bowel, which may be protective (38); the rapid transit of small bowel contents, reducing the contact time between potential carcinogens and the small bowel mucosa (33); and/or its alkaline environment (39).
Clinical presentation and diagnosis
In its early stages, adenocarcinoma of the jejunum and ileum is usually asymptomatic. Diagnostic delays range from months to years, averaging approximately 6–8 months (17, 40, 43), with many patients misdiagnosed as neurotic (41) or as having irritable bowel syndrome (42). Most patients present during the 6th and 7th decades of life with > 90% of patients becoming symptomatic (8, 40, 44). The most common presenting symptoms are listed in table I (17, 40–49). Rarely, patients may present with multiple lesions within the small and large bowel (45–47). In addition, patients with other malignancies including ovary, appendix, colon, lung and kidney may present with intraperitoneal or hematogenous metastatic disease to the small intestine (48).
Table I
Frequency of symptoms at presentation of small bowel adenocarcinoma.
Unlike gastric and colonic cancer, which are amenable to endoscopic biopsy, small intestinal cancer distal to the duodenum is relatively inaccessible. This difficulty in assessment has led to definitive preoperative diagnoses in only 35–72% of reported series (49–51). A high index of suspicion is required due to the non-specific nature of the symptoms.
Plain radiographs may reveal evidence of obstruction, but their sensitivity is low. In contrast to the duodenum, which may be routinely visualized by barium contrast studies and/or endoscopy, Bauer found that routine UGI series with small intestinal follow-through was diagnostic in only 36% and 20% of jejunal and ileal lesions, respectively (43). Enteroclysis increases the sensitivity of small intestinal barium studies (42), and pushtype jejunal endoscopy (52) enhances the diagnostic accuracy of jejunal lesions with its capability of visualizing the jejunum to a level of 40–100 cm past the ligament of Treitz (53).
CT scanning is a useful adjunctive study to assess the extent of local and/or metastatic disease (50). CT characteristics of adenocarcinoma may include “annular narrowing with abrupt concentric or irregular ‘overhanging edges’, a discrete tumor mass, or an ulcerative lesion” (54). Buckley and Fishman (55) studied the accuracy of CT staging of small bowel adenocarcinomas in their retrospective analysis of 15 patients (duodenal lesions = 7, jejunal = 6, ileal = 1, not specified = 1) using 3–5 mm sections at 4–15 mm intervals, and comparing CT findings with final operative pathology reports. They found that the overall CT staging accuracy was 45%, with sensitivities of 0, 0, 50 and 58%, and specificities of 100, 94, 63, and 63% for stage I, II, III, and IV, respectively. In addition, CT scanning was 88% sensitive in the detection of mesenteric infiltration, and 75% sensitive for lymphadenopathy. Other laboratory tests, including assessment of hepatic function, are useful if biliary obstruction or hepatic metastases are present.
Stage/grade distributions
Staging systems for jejunal and ileal adenocarcinoma have been varied. Frost (56) used the American Joint Committee on Cancer (AJCC) staging system, while Ouriel (49) utilized a modified Astler-Coller Duke's system (see table II). Approximately 20% of patients present with early disease while 22–43% present with distant metastases (49, 56).
Table II
Staging of small bowel carcinoma.
The grading system for small bowel adenocarcinoma is as follows: I = well differentiated (0–42% of tumors), II = moderately differentiated (24–45%), and III = poorly differentiated (34–42%) (43, 56).
Treatment
Surgery
Surgical intervention provides the only hope of cure for patients with this disease. Most studies report that curative resection is possible in approximately 40–65% of cases (43, 49). Tumors are unresectable when there is extensive local disease or metastases to multiple regional/distant lymph nodes and/or the liver/peritoneal surface. For tumors of the jejunum and proximal ileum, wide local excision (WLE) with lymphadenectomy is the procedure of choice (43, 49, 56), with ileocolectomy required for distal ileal lesions. In Bauer's 21-year review of small intestinal adenocarcinoma (43), 55% of patients underwent curative resection. Patients who are considered incurable may undergo palliative resections or bypass procedures (20–30%).
Radiotherapy
Small bowel adenocarcinoma is generally considered radioresistant (39). Furthermore, the sensitivity of the small bowel to radiation injury is limited. As a result, the role of radiotherapy has generally been restricted to palliation. Very few patients receive radiotherapy as part of their primary treatment (56–63). Japanese investigators have explored the use of radiotherapy in the intraoperative setting, where a single dose of radiation can be given to a tumor bed with residual microscopic or macroscopic disease while shielding nearby organs (64).
Chemotherapy
We reviewed the literature from 1984 to the present and found 57 patients reported who were treated with chemotherapy for stage C or D adenocarcinoma, including duodenum (43, 49, 56, 59–63). 5-fluorouracil was the most common agent used, either as a single agent or in combination with other agents, including doxorubicin, Cisplatin, levamisole, and Mitomycin. Only three patients survived longer than 2 years.
We have previously mentioned multiple parallels between large bowel and small bowel adenocarcinoma. The similarities have been recognized by clinicians, as well as epidemiologists and molecular geneticists, and have led to the adoption of similar therapeutic strategies. The rarity of small bowel adenocarcinoma makes randomized trials, or even large case series, very difficult and unfeasible. This is particularly true for locally advanced disease, where most oncologists currently utilize similar adjuvant chemotherapy regimens as would be administered in the context of colorectal cancer. Furthermore, newer agents for colorectal cancer, such as CPT-11, which is utilized in 5FU-refractory colon cancer, may also be considered for this disease.
Survival
The five-year survival rates from selected recent series for adenocarcinoma of the small bowel are shown in table III with overall survival rates of 15–30% (8–10, 17, 19, 40, 43, 49, 56, 65, 66). If unresectable the prognosis is dismal with no chance of long term survival. For resectable lesions, studies have reported 5-year survival rates of 40–60%.
Table III
Survival at 5 years for patients with small bowel adenocarcinoma (from selected series).
In Frost's 30year review (56), all patients with ileal adenocarcinoma succumbed to their disease, while 83% of patients with jejunal lesions died. Ouriel (49) had better results with 5-year survival of 46% and 20% for jejunal and ileal lesions, respectively. Bauer (43) found no survival difference based on age, duration of symptoms, tumor location within the small intestine, type of recurrence (local or distant), or grade in 38 patients. However, approximately 50% of patients with jejunal disease had node positive tumors, while 80% of patients with ileal disease had positive lymph nodes. When patients recurred, most had developed distant metastatic disease, most commonly to the liver, with approximately 20% recurring locally. Overall, the five year survival was 0% and 25% for jejunal and ileal lesions, respectively (43).
Conclusions
Adenocarcinoma of the jejunum and ileum is a rare clinical entity with a non-specific presentation. A high index of suspicion is required to prevent prolonged diagnostic delays. Improvements in endoscopic and radiological procedures should lead to earlier diagnosis and better outcomes. High-risk groups, such as patients with a genetic predisposition or obstructive symptoms in older patients, should be pursued with aggressive diagnostic techniques. Unfortunately, the rarity of this lesion precludes the performance of properly designed clinical trials of adjuvant therapies. At this time, the only successful therapy is aggressive surgical resection. A national database may be the only option that will allow for standardization of reporting, diagnosis, treatment, and follow-up.
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