ORIGINAL ARTICLE Proposed Scoring System to Determine Small Bowel Mass Lesions Using Capsule Endoscopy Li-Rung Shyung, Shee-Chan Lin, Shou-Chuan Shih, Wen-Hsiung Chang,* Cheng-Hsin Chu, Tsang-En Wang Background/Purpose: Capsule endoscopy is a highly sensitive method for the detection of small bowel lesions. False-positive findings are important confounding factors. This study reports on a scoring system for evaluating the role of capsule endoscopy in small bowel tumors. Methods: Ten men and two women (age, 23 79 years) with suspected small bowel tumors were included from 120 patients referred for capsule endoscopy between March 2004 and March 2008. The indications were gastrointestinal bleeding (n = 9), melanoma workup (n = 1), physical checkup (n = 1), and iron deficiency anemia (n = 1). The proposed tumor score was composed of five components: bleeding, mucosal disruption, an irregular surface, color, and white villi. These can be scored for probability of mass lesions seen at capsule endoscopy. Small bowel mass lesions were probably present in those with a score of 4, and a score of 2 indicated a low probability of a small bowel mass lesion. Results: Capsule endoscopy showed probable small bowel mass lesions in six patients, and a low lesion probability in the other six. Capsule endoscopy showed that new lesions were not detected by esophagogastroduodenoscopy or colonoscopy. All six patients with probable small bowel tumors were found to have pathological findings upon capsule endoscopy: two with lymphangioma, and one each with ileal ectopic pancreas, with melanoma metastasis, gastrointestinal lymphoma, and gastrointestinal stromal tumor. Conclusion: Capsule endoscopy may detect small bowel tumors more reliably by using the scoring system outlined. It should be considered in suspected cases of small bowel tumor. [J Formos Med Assoc 2009; 108(7):533 538] Key Words: capsule endoscopy, gastrointestinal hemorrhage, intestinal neoplasms The small intestine is the most difficult part of the gastrointestinal tract to evaluate because of its length and overlapping bowel loops. Capsule endoscopy allows for direct visualization of the entire length of the small bowel in a noninvasive manner, and it has become the main standard for evaluating suspected disease of the small intestine. 1 3 The investigation of small bowel tumors has long been a challenge. Small bowel barium radiology has disappointing diagnostic yields and push enteroscopy allows examination of only the proximal small intestine. However, the development of capsule endoscopy has allowed examination of the entire small intestine safely and 2009 Elsevier & Formosan Medical Association....................................................... Division of Gastroenterology, Department of Internal Medicine, Mackay Memorial Hospital, Mackay Medicine, Nursing and Management College, Taipei, Taiwan. Received: June 19, 2008 Revised: December 15, 2008 Accepted: February 5, 2009 *Correspondence to: Dr Wen-Hsiung Chang, Division of Gastroenterology, Department of Internal Medicine, Mackay Memorial Hospital, No. 92, Section 2, Chung-Shan North Road, Taipei 104, Taiwan. E-mail: luke.skywalk@msa.hinet.net J Formos Med Assoc 2009 Vol 108 No 7 533
L.R. Shyung, et al noninvasively. Diagnostic yield is superior to that of push enteroscopy and it leads to improved patient outcomes. 4 As a result of a lack of controlled trials, there is no current consensus regarding the diagnostic approach for attempting to reduce the rate of false-positive capsule endoscopy. This report describes a scoring system for evaluating the role of capsule endoscopy in small bowel tumors. transit time was calculated from the first view of the duodenum up to the cecum. The proposed tumor score was composed of five components: bleeding, mucosal disruption, an irregular surface, color, and white villi. These components can be scored for probability of mass lesions seen at capsule endoscopy. Results Patients and Methods A retrospective study was performed on 120 patients who underwent capsule endoscopy (Given Imaging Ltd., Yoqneam, Israel) between March 2004 and March 2008. Clinical and other data were collected and evaluated retrospectively. A mass was defined by the following morphological criteria: (1) a clearly-defined boundary with the surrounding mucosa; (2) height larger than the diameter; (3) a visible lumen in the frames in which it appeared; and (4) an image lasting more than 10 minutes. The following can be misdiagnosed as a small bowel mass lesion: intestinal contraction, a normal extrinsic organ or another small bowel loop, or intussusception. Twelve patients were included because of suspected small bowel mass lesions. There were 10 men and two women, with a mean age of 55.3 years (range, 23 79 years). All patients had undergone at least one endoscopy and colonoscopy prior to capsule endoscopy. All patients gave written informed consent. All patients ingested the capsule after an overnight fast of 12 hours. Patients were allowed to drink 2 hours after ingesting the capsule and to eat a light meal 4 hours later. Patients were free to leave the endoscopy department, with instructions to return 7 8 hours after ingestion to have the recorder disconnected. The recorded information was downloaded onto a computer, and images from the stomach and the small bowel were analyzed using RAPID 3 software (Given Imaging Ltd., Yoqneam, Israel). The intestinal In this retrospective study, 12 patients with suspected small bowel mass lesions out of 120 patients who were referred for capsule endoscopy were examined using the scoring system. The findings are summarized in Table 1. Esophagogastroduodenoscopy and colonoscopy results showed that patient 7 did not have any abnormalities. This patient presented with intermittent, dark bloody stools for 2 months, accompanied by epigastric pain and postprandial abdominal fullness. Capsule endoscopy revealed a small red polyp in the ileum. Abdominal computed tomography (CT) and small bowel barium followthrough were not of any help. Gastrointestinal bleeding and abdominal discomfort were resolved after the lesion was removed surgically. Pathological examination demonstrated pancreatic acinar cells and a secretory duct in the ileal submucosa, which was consistent with ectopic pancreas. Patient 10 was found to have extensive small bowel mucosal lesions by capsule endoscopy. However, his earlier serial examinations esophagogastroduodenoscopy, colonoscopy, small bowel series, CT and angiography failed to disclose the source of bleeding. The final diagnosis of diffuse large B cell lymphoma was established by histology and immunohistochemical studies of a biopsy specimen by push enteroscopy. This patient was treated with systemic chemotherapy and at the time of writing remains in complete remission. In patients 1, 2, 4 and 11, a decreased likelihood of small bowel tumors was diagnosed because of as the absence of abdominal pain, weight loss, or small bowel obstruction during follow-up. 534 J Formos Med Assoc 2009 Vol 108 No 7
Capsule endoscopy for small bowel lesions Table 1. Demographic data, capsule endoscopy findings, and treatment Patient Sex/age (yr) Indications Capsule endoscopy findings Treatment 1 M/39 GI bleeding Ileal tumor (lipoma) 2 M/79 GI bleeding Terminal ileum tumor Outpatient follow-up 3 M/32 IDA Lymphangioma with Refer for double bleeding balloon enteroscopy 4 F/66 GI bleeding Suspect submucosal tumor 5 M/54 GI bleeding Entrapped in the duodenal Operation diverticulum, GIST 6 M/43 Physical check-up Lymphangioma 7 M/38 GI bleeding Red polyp with a stalk in ileum Operation 8 M/23 GI bleeding Ruled out normal bulge of Refer for double upper ileum balloon enteroscopy 9 M/65 Melanoma Melanoma with Palliative C/T with work-up metastasis dacarbazine regimen 10 M/79 GI bleeding Nodular masses with whitish, CEOP C/T lymphangiectatic, swollen villi over the proximal and distal small bowel 11 F/79 GI bleeding Suspect GIST 12 M/67 GI bleeding Ruled out submucosal tumor Operation of duodenum, diverticulosis of small bowel GI = gastrointestinal; IDA = iron deficiency anemia; GIST = gastrointestinal stromal tumor; C/T = chemotherapy; CEOP = epirubicin with cyclophosphamide, vincristine and prednisone. Table 2. Features of scoring system for 12 patients with suspected mass lesions Patient Bleeding MD IS Color WV Score 1 + 1 2 0 3 + + + + + 5 4 + 1 5 + + + + 4 6 + + + + 4 7 + + + 3 8 0 9 + + + + 4 10 + + + + + 5 11 + + 2 12 + + 2 MD = mucosal disruption; IS = irregular surface; WV = white villi. In patient 8, double balloon enteroscopy findings were unremarkable. In patient 12, no tumor was found during operation. The features of the scoring system observed in the patients are summarized in Table 2. There were probable small bowel mass lesions in those with a score of 4 (Figure 1). The etiology was lymphangioma in two patients, and ileal ectopic pancreas, melanoma, gastrointestinal lymphoma, and gastrointestinal stromal tumor in one each. J Formos Med Assoc 2009 Vol 108 No 7 535
L.R. Shyung, et al Figure 1. Probable small bowel mass lesions. Lymphangioma Ectopic pancreas Melanoma meta Β-cell lymphoma There was a low probability of small bowel mass lesions in those with a score of 2 (Figure 2). Discussion Capsule endoscopy is a new technology that has been developed to investigate diseases of the small intestine. It has been shown to be superior to current modalities such as small bowel barium radiology and push enteroscopy. 5 Capsule endoscopy, as a novel endoscopic procedure, has led to reclassification of the terminology of gastrointestinal tract diseases. 6,7 Small bowel tumors account for 3 6% of gastrointestinal tumors, and cancer of the small intestine represents < 2% of all malignant tumors in the gastrointestinal tract. 8 Prior to the advent of capsule endoscopy, methods for examining the small bowel proved inadequate, therefore, the accuracy of the previous statement is unknown. Small bowel tumors detected with capsule endoscopy are frequently revealed by obscure gastrointestinal bleeding; in our patients, the most common presentation was obstruction and pain. Our proposed tumor score was composed of five components: bleeding, mucosal disruption, an irregular surface, color, and white villi. Our proposed criteria are based on the following observations. Benign and malignant small bowel tumors cannot be reliably differentiated by capsule endoscopy. The surface of benign tumors such as hyperplasia, hamartoma, ectopic pancreas, and adenoma may show generally circumscribed ulceration. Vascular tumors often have a reddish or bluish appearance. Capsule endoscopy 536 J Formos Med Assoc 2009 Vol 108 No 7
Capsule endoscopy for small bowel lesions Figure 2. Low probability small bowel mass lesions. Terminal ileum tumor Submucosal tumor of adenocarcinoma may reveal an infiltrating lesion that may show ulceration and/or bleeding. Lymphoma may have different appearances. Metastatic melanoma can often be suspected by its pigmented nature, as shown in our study. The patient with ileal ectopic pancreas had a score of 3, which corresponded to intermediate probability of a small bowel mass lesion. Early studies have suggested that there is no significant difference in the diagnostic yield of capsule endoscopy in obscure-overt and obscure-occult bleeding, but in the study by Pennazio et al, 9 patient selection was paramount for optimal use of capsule endoscopy. In patient 7, we suggest that if capsule endoscopy had been done earlier, the tumor score would have increased from 3 to 4 on account of bleeding. Neovascularization by angiogenesis occurs in pathological settings such as tumor growth. 10,11 In the present study, the increased accuracy of capsule endoscopy was dependent on the definition that the authors used (red color) to define a neoplasm. White villi were found in our patients undergoing capsule endoscopy. They were most likely to be primary lymphangiectasia, and were a normal anatomical variant. 12 Adult intestinal lymphangiectasia is secondary to many other factors, such as lymphoma, intestinal tuberculosis, and adenocarcinoma. 13 In the present study, we could not predict pathology and tumor type by using the scoring system. The major point of interest of this study was to detect the presence of small bowel tumors using the scoring system. When diagnoses are compared in a non-randomized study, as in ours, scoring systems can sometimes help mitigate the potential bias that arises from the lack of randomization. 14 One drawback of our research was the relatively small number of patients and the retrospective database, although it was constructed correctly. Therefore, further, large prospective studies are needed to confirm our results. In conclusion, we can determine criteria to indicate the presence of a small bowel mass lesion by capsule endoscopy, and reduce the false-positive rate. High or intermediate probability lesions may lead to double balloon enteroscopy or surgery, while treatment of lesions with low probability will depend on their clinical significance. References 1. Van Tuyl SA, Van Noorden JT, Kuipers EJ, et al. Results of videocapsule endoscopy in 250 patients with suspected small bowel pathology. Dig Dis Sci 2006;51:900 5. 2. Mishkin DS, Chuttani R, Croffie J, et al. AGE technology status evaluation report: wireless capsule endoscopy. Gastrointest Endosc 2006;63:539 45. 3. Leighton JA, Goldstein J, Hirota W, et al. Obscure gastrointestinal bleeding. Gastrointest Endosc 2003;58: 650 5. 4. Estevez E, Gonzalez-Conde B, Vazquez-Iglesias JL, et al. Diagnostic yield and clinical outcomes after capsule J Formos Med Assoc 2009 Vol 108 No 7 537
L.R. Shyung, et al endoscopy in 100 consecutive patients with obscure gastrointestinal bleeding. Eur J Gastroenterol Hepatol 2006; 18:881 8. 5. Triester SL, Leighton JA, Leontiadis GI, et al. A meta-analysis of the yield of capsule endoscopy compared to other diagnostic modalities in patients with obscure gastrointestinal bleeding. Am J Gastroenterol 2005;100:2407 18. 6. Gay G, Delvaux M, Fassler I. Outcome of capsule endoscopy in determining indication and route for push-and-pull enteroscopy. Endoscopy 2006;38:49 58. 7. Nakamura M, Niwa Y, Ohmiya N, et al. Preliminary comparison of capsule endoscopy and double-balloon enteroscopy in patients with suspected small-bowel bleeding. Endoscopy 2006;38:59 66. 8. O Loughlin C, Barkin JS. Wireless capsule endoscopy: summary. Gastrointest Endosc Clin N Am 2004;14:229 37. 9. Pennazio M, Santucci R, Rondonotti E, et al. Outcome of patients with obscure gastrointestinal bleeding after capsule endoscopy: report of 100 consecutive cases. Gastroenterology 2004;126:643 53. 10. Risau W. Mechanisms of angiogenesis. Nature 1997;386: 671 4. 11. Hanahan D. Signaling vascular morphogenesis and maintenance. Science 1997;277:48 50. 12. Chamouard P, Nehme-Schuster H, Simler JM, et al. Videocapsule endoscopy is useful for the diagnosis of intestinal lymphangiectasia. Dig Liver Dis 2006;38:699 703. 13. Flieger D, Keller R, May A, et al. Capsule endoscopy in gastrointestinal lymphomas. Endoscopy 2005;37:1174 80. 14. Zinsmeister AR, Connor JT. Ten common statistical errors and how to avoid them. Am J Gastroenterol 2008;103: 262 6. 538 J Formos Med Assoc 2009 Vol 108 No 7