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Multiple carcinoid tumors of the small intestine preoperatively diagnosed by double-balloon endoscopy.
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MedLine Citation:
PMID:  23197242     Owner:  NLM     Status:  MEDLINE    
BACKGROUND: Multiple carcinoid tumors of the small intestine are rare and are very difficult to detect preoperatively.
CASE REPORT: A 75-year-old woman in whom the bleeding focus could not be found by upper and lower endoscopy and abdominal CT was admitted for evaluation of anemia. We examined the patient with total double-balloon endoscopy (DBE) and located multiple submucosal tumors. The multiple carcinoid tumors were resected successfully under laparoscopy.
CONCLUSIONS: We report a case of a successful laparoscopic operation for multiple carcinoid tumors in the small intestine without intraoperative endoscopy. Total digestive tract observation using DBE is very useful for laparoscopic operation for multiple tumors in the small intestine.
Se-Yong Lee; Shibuya Tomoyoshi; Keiichi Haga; Hitosi Sasaki; Chie Ogata; Osamu Nomura; Yuka Fukuo; Wataru Abe; Taro Osada; Akihito Nagahara; Tatsuo Ogihara; Hirohiko Kamiyama; Kazuhiro Sakamoto; Sumio Watanabe
Publication Detail:
Type:  Case Reports; Journal Article    
Journal Detail:
Title:  Medical science monitor : international medical journal of experimental and clinical research     Volume:  18     ISSN:  1643-3750     ISO Abbreviation:  Med. Sci. Monit.     Publication Date:  2012 Dec 
Date Detail:
Created Date:  2012-11-30     Completed Date:  2013-06-26     Revised Date:  2013-07-11    
Medline Journal Info:
Nlm Unique ID:  9609063     Medline TA:  Med Sci Monit     Country:  Poland    
Other Details:
Languages:  eng     Pagination:  CS109-12     Citation Subset:  IM    
Department of Gastroenterology, Juntendo University School of Medicine, Tokyo, Japan.
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MeSH Terms
Carcinoid Tumor / diagnosis*,  pathology,  surgery*
Epithelial Cells / pathology
Intestinal Neoplasms / diagnosis,  pathology,  surgery
Intestine, Small / pathology*,  surgery*
Preoperative Care*

From MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine

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Journal Information
Journal ID (nlm-ta): Med Sci Monit
Journal ID (iso-abbrev): Med. Sci. Monit
Journal ID (publisher-id): Medical Science Monitor
ISSN: 1234-1010
ISSN: 1643-3750
Publisher: International Scientific Literature, Inc.
Article Information
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© Med Sci Monit, 2011
Received Day: 17 Month: 5 Year: 2012
Accepted Day: 06 Month: 9 Year: 2012
collection publication date: Year: 2012
Electronic publication date: Day: 01 Month: 12 Year: 2012
Volume: 18 Issue: 12
First Page: CS109 Last Page: CS112
PubMed Id: 23197242
ID: 3560802
Publisher Id: 883588

Multiple carcinoid tumors of the small intestine preoperatively diagnosed by double-balloon endoscopy
Se-Yong Lee1ABCDEF
Tomoyoshi Shibuya1ABCDEF
Keiichi Haga1BDE
Hitosi Sasaki1BCD
Chie Ogata1B
Osamu Nomura1B
Yuka Fukuo1B
Wataru Abe1BC
Taro Osada1BCD
Akihito Nagahara1CD
Tatsuo Ogihara1CD
Hirohiko Kamiyama2BD
Kazuhiro Sakamoto2BD
Sumio Watanabe1ABCDEF
1Department of Gastroenterology, Juntendo University School of Medicine, Tokyo, Japan
2Department of Coloproctological Surgery, Juntendo University School of Medicine, Tokyo, Japan
Correspondence: Tomoyoshi Shibuya, Department of Gastroenterology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan, e-mail:
AStudy Design
BData Collection
CStatistical Analysis
DData Interpretation
EManuscript Preparation
FLiterature Search
GFunds Collection


Tumors of the small intestine account for 1% to 2% of all gastrointestinal neoplasms (only 0.3% of all neoplasms) [1]. However, the incidence of small intestine cancer has increased dramatically over the past 30 years [2], and the increase in carcinoid tumors has been largely responsible. Carcinoids of the ileum account for 15.4% of all gastrointestinal carcinoids [3] and are multicentric in 20–30% of patients [4]. The lack of signs and symptoms, lack of definitive preoperative diagnostic tests, and the variable efficacy of available tests make small intestine tumors difficult to diagnose [5]. The recent development of capsule endoscopy (CE) and double balloon endoscopy (DBE) has improved diagnostic capabilities for the small intestine. We report the first case of multiple carcinoid tumors of the small intestine preoperatively diagnosed by DBE and treated with laparoscopic surgery.

Case Report

A 75-year-old woman was referred to our hospital with melena and severe anemia (hemoglobin (Hb) 7.2 g/dL). She had a history of stroke at age 59 years, and was being treated with antiplatelet therapy at the time of admission to the referring hospital. At that hospital, the source of GI bleeding was not revealed by upper and lower gastrointestinal endoscopy examination, abdominal computed tomography (CT), or ultrasound (US). Through radiological enteroclysis, an elevated lesion was found in the ileum, which was suspected to be a submucosal tumor and measured 15 mm in diameter. Melena had resolved after stopping low-dose aspirin. Anemia was also improved by administration of an iron preparation without a blood transfusion. After 2 months at the referring hospital, she was admitted to our hospital for a thorough investigation of the small intestine. Physical examination revealed her abdomen to be soft and flat without any pain or tenderness. Results of blood tests were as follows: Hb 11.3 g/dL (normal: 11.1–15.2 g/dL), red blood cell count 418 104/mL (normal: 380–540 104/mL), and hematocrit 35.3% (normal: 35.6–45.4%). The remaining results were also normal. No findings were noted on abdominal X-ray. We then examined the patient with peroral DBE (EN-450P5: FUJIFILM Medical Co., Ltd., Tokyo, Japan). A tumor was located about 250 cm from the ligament of Treitz and measured 8 mm in diameter (Figure 1). The tumor was yellowish in color and covered with mucosa of normal appearance. However, active bleeding was not observed during the procedure. Histologic examination of the biopsy sample obtained by endoscopy confirmed the diagnosis of a carcinoid tumor. The tumor was composed of small uniform epithelial cells, which stained positively for chromogranin A and synaptophysin.

Another tumor detected through peranal DBE was located about 110 cm from the ileocecal valve and measured 15 mm in diameter. Also, other small tumors were detected that measured 3 mm and 5 mm in diameter and had a relatively smooth surface, similar to a submucosal tumor. These small tumors were diagnosed as carcinoid tumors by endoscopic findings, whereas histologic examination could not make this diagnosis. The largest tumor had ulcerations, which could account for the GI bleeding (Figure 2). However, active bleeding was not observed from the ulcer during the procedure. Thus, endoscopic treatment was not required. The patient underwent partial resection of the small intestine by laparoscopic surgery (resected portion: 23.8 cm). She had already undergone a preoperative total small intestinal examination using DBE; therefore, it was not necessary to perform intraoperative endoscopy. The resected specimen contained tumors measuring 14×10 mm, with central ulceration (Figure 3), 2.8×6 mm and a tumor 3 mm in diameter. Microscopically, the tumors were composed of small uniform epithelial cells (Figure 4B), which stained positively for chromogranin A and synaptophysin (Figure 5). Furthermore, the largest tumor had invaded the muscularis propria (Figure 4A). MIB-1 index was less than 1%. No metastases were found in the regional lymph nodes, and the surgical margins were negative for tumor cells. After the surgery, the patient had no gastrointestinal bleeding. Follow-up DBE was performed 18 months later, and there was no sign of recurrence in the small intestine.


This is the first report of laparoscopic surgery without the use of intraoperative endoscopy for multiple carcinoid tumors of the small intestine, which was possible because the tumors were diagnosed before surgery by DBE.

Carcinoid is the second most common malignancy, accounting for approximately 20–25% of all small intestine lesions [6]. Carcinoid tumors are more common in the ileum (most within 60 cm of the ileocecal valve) than in the jejunum or duodenum, and lesions may be multiple and/or metastatic (liver and lungs) at the time of diagnosis because one fourth of carcinoid tumors in the small intestine are multiple [7]. On the guideline, by far the majority of small intestinal neuroendocrine tumors (NETs, including carcinoid) are malignant in nature. Whether liver metastases are present or not, resection of the primary tumor is appropriate to cure or to delay progression that would otherwise endanger the small bowel [8].

It is difficult and rare to preoperatively diagnose carcinoid tumors in the small intestine [5]. Carcinoids of the rectum, stomach, and duodenum generally are found by endoscopy at an early stage, whereas carcinoid tumors of the small intestine usually are discovered after resection of the small intestine for symptoms of obstruction or during exploration of the small intestine in search of a primary tumor after distant metastases have been found [2,912]. Through conventional imaging techniques (e.g., CT, US, double contrast barium study), few tumors of a small diameter are identified.

Currently, with advancement in methods of CE, small intestine tumors can be located. CE had a high diagnostic yield of 45% for identification of primary small intestinal carcinoid tumors [13]. CE is a simple, safe and comfortable diagnostic technique [14]. However, it remains purely a diagnostic procedure at present because it is not suitable for histological diagnosis and procedures. For this reason, if laparoscopic surgery is performed in a patient who was diagnosed as having multiple carcinoid tumors of the small intestine, it is usually necessary to perform intraoperative endoscopy to confirm that the lesion is a carcinoid tumor. It is notable that in reporting the results of their study, M. Bellutti et al. suggested that intraoperative endoscopy is a potential gold standard for NETs [15].

On the other hand, DBE can detect these lesions and perform therapeutic procedures and diagnostic interventions [16]. A submucosal tumor of the ileum or the jejunum was detected by DBE in 7 of 12 patients (58%) with suspected carcinoid syndrome [15]. In addition, tumor marking using injection of ink for the exact location during DBE has been helpful for subsequent operations, especially for laparoscopic resection. By utilizing DBE, we were able to locate the multiple ileal tumors and to perform laparoscopic surgery without intraoperative endoscopy in the patient reported here.

DBE is a safe procedure, with low complication rates even when therapeutic maneuvers are performed [17]. As only DBE allows direct, controlled visualization of small intestine tumors and their histological confirmation preoperatively, it may be considered the gold standard for the diagnosis of such tumors [18]. DBE is extremely useful to detect and diagnose asymptomatic small lesions in the small intestine.


Based on the case presented here, we recommend total digestive tract observation using DBE before performing laparoscopic operation for multiple tumors of the small intestine.



The authors declare no conflicts of interest.

fn9-medscimonit-18-12-cs109Source of support: No funding support

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Article Categories:
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Keywords: double balloon endoscopy, carcinoid tumor, small intestine, capsule endoscopy.

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