Early-Stage Small-Bowel Adenocarcinoma: A Review of Local Endoscopic Therapy

• Introduction
• Small-Intestinal Adenocarcinoma
• Early-Stage Carcinoma in the Gastrointestinal Tract
• Early Duodenal Carcinoma
• Endoscopic Resection
• Outlook
• References

Early adenocarcinomas in the small intestine are a rare entity. Most adenocarcinomas in the small intestine are diagnosed at a more advanced stage. After surgical resection, only 3 - 10 % are found in stage T1 and 0 - 3 % in stage Tis (high-grade intraepithelial neoplasia), resulting in an overall 3 - 13 % rate of early-stage small-intestinal adenocarcinomas. The diagnosis of early small-intestinal carcinoma by endoscopy is still very rare, although it will propably improve with the development of new endoscopic techniques.

At present there have been only two studies and a few case reports on the treatment of early duodenal carcinoma by endoscopic resection. No major complications such as massive bleeding or perforation occurred in the studies and case reports, which show that endoscopic resection is a safe and effective treatment for early duodenal cancers that have not invaded the submucosa. Endoscopic resection can be carried out with reduced costs and lower morbidity and mortality rates in comparison with surgery.

Introduction

Small-bowel tumors often present insidiously, with nonspecific symptoms. The most common complaints reported by patients with advanced small-bowel cancer are abdominal pain, nausea, vomiting, weight loss, bleeding, and intermittent obstruction [1] [2] [3] [4] [5]. Proximally located carcinomas can be easily diagnosed by barium contrast studies and esophagogastroduodenoscopy; distally located carcinomas require enteroclysis, enteroscopy, capsule endoscopy, computed tomography, or intraoperative endoscopy [6] [7] [8]. Despite the development of new techniques and equipment, such as capsule endoscopy, push enteroscopy, and double-balloon enteroscopy, it is still difficult to diagnose primary small-intestinal cancer [9], and the diagnosis is commonly delayed [1] [4] [5] [6].

Small-Intestinal Adenocarcinoma

Cancer of the small intestine is relatively rare, representing 1 - 5 % of malignant tumors in the gastrointestinal tract [1] [5] [10] [11]. Primary adenocarcinomas are the most common malignant cancers in the small intestine, accounting for 27 - 58 % of cases [1] [4] [5] [6] [9] [12] [13] [14]. Reports on the distribution of adenocarcinomas in the small intestine vary, with 47 - 55 % found in the duodenum, 18 - 29 % in the jejunum, 14 - 24 % in the ileum, and 14 % in sites not specified [1] [4] [6] [15]. Little is known about the pathogenesis of small-intestinal adenocarcinoma. Risk factors include Crohn’s disease and preexisting adenoma, either single or multiple, in association with one of the multiple polyposis syndromes - particularly familial adenomatous polyposis, Peutz-Jeghers syndrome, and hereditary juvenile polyposis [5] [6] [16] [17] [18] [19]. An association with celiac sprue, neurofibromatosis, cystic fibrosis, peptic ulcer disease, and urinary diversion procedures such as ileal conduit has been reported [5] [14], as well as a correlation with colorectal carcinoma [5] [14] [20] [21]. Potential dietary risk factors such as red meat and smoked and salted food have been suggested [22]. In addition, a direct relationship with consumption of bread, pasta, sugar and rice and an inverse relationship with coffee, fruit, and vegetables has been postulated [23].

The treatment of choice for adenocarcinoma of the small intestine is surgical resection. In adenocarcinomas of the jejunum, resection of the tumor along with the adjacent mesentery and lymph nodes, with a wide margin of normal bowel on either side, is commonly carried out. Adenocarcinomas of the terminal ileum are treated as cecal tumors, with terminal ileal resection and right hemicolectomy. Adenocarcinomas of the duodenum require pancreaticoduodenectomy (Whipple procedure). Local resection of pedunculated polyps with a clear resection margin has been reported in some cases [15] [24].

Curative surgical resection is possible in 40 - 65 % of patients, with 5-year survival rates varying from 36 % to 81 % for resected tumors and from 12 % to 30 % for unresected tumors [1] [4] [5] [6] [25] [26] [27] [28] [29]. Factors associated with significant differences in survival are the depth of cancer invasion, presence of lymph-node metastases, tumor differentiation, surgical margin status, extramural venous spread, and a history of Crohn’s disease [1] [4] [30].

Small-intestinal adenocarcinomas are staged in accordance with the extent of bowel-wall invasion, the presence or absence of invasion into adjacent structures, and the presence or absence of lymph-node or distant metastases (using the TNM classification) (Table [1]) [31].

Five-year survival rates of 81 - 90 % have been reported for patients with T1/T2 cancer, while the reported 5-year survival rates in those with T3/T4 cancer are 40 - 58 % [1] [4] [6].

Early-Stage Carcinoma in the Gastrointestinal Tract

Early carcinomas in the gastrointestinal tract have been reported in the esophagus, stomach, and large intestine. They are defined as adenocarcinomas confined to the mucosa or submucosa, regardless of any regional lymph-node metastases [32] [33] [34]. In Japan, around 34 % of esophageal cancers [35], more than 50 % of gastric cancers [36], and approximately 20 % of colonic cancers [37] [38] are detected at an early stage and have 5-year survival rates of 83 %, 90 %, and 97 %, respectively [39] [40] [41] [42]. The rate of detection of early carcinomas in the West is much lower [43].

According to the above definition of early carcinoma, early carcinomas in the small intestine consist of lesions staged Tis (high-grade intraepithelial neoplasia) and T1. Most small-intestinal adenocarcinomas are discovered at a more advanced stage [6] [44]. Only 3 - 10 % are found in stage T1 [4] [6] [45] and 0 - 3 % in stage Tis [4] [20] [45], resulting in an overall 3 - 13 % rate of early small-intestinal adenocarcinomas. In the reported cases, the staging was carried out after surgical resection of the tumor.

Endoscopic diagnosis of early small-intestinal carcinoma is still very rare, and endoscopic resection has only been reported for early duodenal carcinoma. This review therefore focuses on early duodenal carcinoma.

Early Duodenal Carcinoma

Since 47 - 55 % of small-intestinal cancers are found in the duodenum, which is easily reached and examined by endoscopy, early duodenal carcinomas are best detected using upper endoscopy [1] [4] [6]. The classification of early duodenal carcinoma is analogous to the classification of early gastric cancer by the Japanese Gastroenterological Endoscopy Society (Figure [1]) [24] [46]. An analysis of the literature on early duodenal carcinoma found lymph-node metastasis in 0 % of intramucosal carcinomas and 5 % of submucosal carcinomas. No differentiation was made with regard to the submucosal invasion depth (sm1 to sm3) [47].

Previously, early duodenal carcinomas were treated surgically by pancreaticoduodenectomy or pancreas-sparing duodenectomy [44], with a morbidity rate of 30 - 40 %, a mortality rate of 1 - 2 %, and 9 - 10 days of hospitalization [48] [49]. Advances in endoscopic techniques have now made it possible to treat early duodenal carcinoma endoscopically, with the expected lower morbidity and mortality rates [50] [51].

Endoscopic Resection

Endoscopic resection has been accepted as a radical treatment for early esophageal, gastric, and colorectal cancers due to its lower invasiveness, its cost-effectiveness, and the short hospital stay involved [43] [52] [53] [54]. Data on endoscopic resection in the duodenum are scarce; it has mainly been used to resect adenomas in the duodenum or at the papilla [52] [53] [54] [55] [56].

Since the duodenal mucosa is quite thin, the risk of perforation during endoscopic resection is high. This complication can be minimized by injecting either saline or a diluted epinephrine solution submucosally before the resection (the “lift-and-cut” polypectomy technique) [50] [52] [53] [54] [55]. At present there have only been two studies [50] [51] and few case reports [57] [58] [59] [60] [61] [62] [63] [64] on the treatment of early duodenal carcinoma by endoscopic resection. In the studies by Oka et al. [51] and Hirasawa et al. [50], including 15 and 14 patients, respectively, no major complications such as massive bleeding or perforation occurred. Both studies show that endoscopic resection is a safe and effective treatment for early duodenal cancers that have not invaded the submucosa.

The indication for endoscopic resection in early gastric carcinoma is based on the depth of invasion and the macroscopic size and type of carcinoma [43] [53] [65] and is well established. The probability of lymph-node metastasis in association with mucosal gastric cancer has been shown to be as low as 0 - 5 % [43] [66]. According to the studies by Oka et al. [51] and Hirasawa et al. [50], the selection of endoscopic treatment for early duodenal carcinoma should be made in analogy with early gastric cancer, on the basis of the tumor’s size, location, and gross appearance. Nagatani et al. [47] analyzed 127 cases of early duodenal cancer reported in Japan and found lymph-node metastases in 0 % of intramucosal carcinomas and 5 % of submucosal carcinomas. These findings suggest that submucosal cancer is a risk factor for lymph-node metastasis, so that endoscopic resection is only indicated in strictly intramucosal carcinomas. In addition, Hirasawa et al. [50] reviewed the Japanese literature (67 journal reports) and concluded that lymph-node metastasis did not occur when protruding (I) or elevated (IIa) tumors were less than 50 mm in diameter, but did occur when depressed (IIc) tumors were more than 10 mm in diameter. The authors therefore suggest that type I or IIa tumors with a diameter of less than 50 mm can be removed completely by endoscopic resection, but that type IIc tumors should be resected surgically, due to possible lymph-node metastases.

However, no differentiation was made in these studies with regard to the depth of invasion of the submucosa (sm1 to sm3). In a study by Ono et al. [67] on endoscopic mucosal resection for the treatment of early gastric cancer no lymph node metastases were reported even in early gastric carcinoma with minute submucosal invasion (sm1, without invasion of blood and lymph vessels). In addition, no recurrence of cancer was observed in the cases with submucosal invasion, suggesting that it is reasonable to treat patients with minute submucosal invasion (sm1) by EMR. It is not uncommon that EMR results in upgrading of histopathologic staging. After EMR approx. 44 % of patients have to be upgraded according to the histologic examination of the resected specimen [68]. This showes the limitation of preoperative diagnostics and the importance of histologic clarification i. e. by EMR. Our own group recently treated a case of a patient with an early-stage duodenal adenocarcinoma classified as type IIa + c. On the basis of our experience with endoscopic resection of early-stage cancer, and taking into account the endosonographic and computed tomography (CT) findings (limited to the mucosa, absence of enlarged lymph nodes), it was decided to carry out local treatment, which was done successfully. The histological examination of the resected specimen revealed an adenocarcinoma, which was mainly limited to the mucosal layer. However, at one site, initial infiltration of the submucosa without involvement of lymphatic or blood vessels was found (pT1 - sm1). Since the basal resection line was tumor-free and the lymphatic and blood vessels were not infiltrated, the risk of lymph-node metastases in this case was extremely low. Weighing up the risks and benefits, therefore, we did not see any indication for a surgical intervention. A follow-up examination after 6 months showed no signs of tumor recurrence [64] (Figure [2]). However, close surveillance after this form of therapy is mandatory, especially in a borderline case such as this.

Large studies are needed in order to establish the indication for endoscopic resection in early-stage duodenal cancer. Further evaluation of the risk of metastasis from early-adenocarcinomas invading the submucosa in relation to their depth of invasion (sm1 to sm3) is also necessary.

Outlook

With the development of capsule endoscopy, push enteroscopy, and double-balloon enteroscopy, the diagnosis of primary early-stage small-intestinal cancer will certainly improve in the future. Push enteroscopy and double-balloon enteroscopy are of great value in identifying and biopsying small-bowel lesions seen on small-bowel barium studies, enteroclysis, capsule endoscopy, or computed tomography (CT), in evaluating occult gastrointestinal bleeding, and for surveillance of patients with Peutz-Jeghers syndrome and familial adenomatous polyposis syndrome [19] [24].

Following the establishment of the method of endoscopic resection for early gastrointestinal carcinoma of the stomach, esophagus, and large intestine, and the quite small studies on early duodenal carcinoma, further studies on early small-intestinal carcinoma, including the jejunum and ileum, are now needed in order to evaluate endoscopic diagnosis and resection using push enteroscopy and double-balloon enteroscopy. This treatment option could avoid the risks of surgery for patients with early small-intestinal carcinoma.

In summary, this review of early small-intestinal carcinomas, focusing on early duodenal carcinomas, demonstrates the importance of early detection of small-bowel carcinoma, as well as the availability of safe and effective treatment for early duodenal cancer using endoscopic mucosal resection.

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C. Ell, M.D.

Dept. of Medicine II, HSK Wiesbaden

Ludwig-Erhard-Strasse 100 · 65199 Wiesbaden · Germany

Fax: +49-611 43 2418

Email: ell.hsk-wiesbaden@arcor.de

References

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C. Ell, M.D.

Dept. of Medicine II, HSK Wiesbaden

Ludwig-Erhard-Strasse 100 · 65199 Wiesbaden · Germany

Fax: +49-611 43 2418

Email: ell.hsk-wiesbaden@arcor.de