Endoscopy essentials
327
Authors
Claudia P. Diaz-Tobar, Lucia C. Fry, Klaus Mönkemüller
Institution
Basil I. Hirschowitz Endoscopic Center of Excellence, Division of Gastroenterology and Hepatology, Birmingham, Alabama, USA
Bibliography DOI http://dx.doi.org/ 10.1055/s-0034-1365072 Published online: 6.3.2014 Endoscopy 2014; 46: 327–332 © Georg Thieme Verlag KG Stuttgart · New York ISSN 0013-726X
Double-balloon enteroscopy for mesenchymal tumors of the small bowel: nine years experience (He et al., World J Gastroenterol 2013 [1])
Corresponding author Klaus Mönkemüller, MD, PhD, FASGE Basil I. Hirschowitz Endoscopic Center of Excellence Division of Gastroenterology and Hepatology Endoscopy Unit, JT 664 619 19th Street S Birmingham, AL 35249 USA Fax: +1-205-934-1537 [email protected]
!
Although the small intestine is the largest hollow organ of the gastrointestinal tract and its mucosa encompasses about 90 % of the luminal surface area of the digestive system, small-bowel polyps and tumors are relatively rare [2]. However, the incidence of small-bowel neoplasms has increased significantly over the past 20 years [2]. The advent of video capsule endoscopy (VCE) and deep enteroscopy has enabled the diagnosis of these lesions at earlier stages. Common smallbowel tumors include neuroendocrine tumors (NET), adenocarcinomas, lymphomas, and gastro" Table 1; intestinal stromal tumors (GIST) [3 – 8] (● " Fig. 1). However, it appears that the most ● common tumors diagnosed during deep entero" Table 1) scopy are adenocarcinomas and GISTs (● [3 – 8].
Table 1
In a retrospective, observational, cohort study of 783 patients undergoing double-balloon enteroscopy (DBE) during a 9-year period, He et al. from Zhejiang University in Hangzhou, China, found 77 patients with gastrointestinal mesenchymal tumors (GIMT) (9.8 %) [1]. Based on the available literature, it appears that mesenchymal tumors are one of the most common malignant tumors found during deep enteroscopy [6 – 7] " Table 1). However, other studies have shown (● that other tumors, such as carcinoids, are more common [3, 8]. Thus, there seems to be geographic variation in the type of tumor diagnosed. In Japan and Korea, lymphomas are diagnosed more frequently than in Europe. Nonetheless, submucosal tumors such as GIST are common across " Table 1 summarizes the key papers the world. ● published to date on deep enteroscopy for the diagnosis of small-bowel polyps and tumors. Another key observation from these studies is that the proportion of polyps and tumors detected by deep enteroscopy was about 10 % – 15 %, which was independent of geographic location [3 – 8].
Summary of studies using double-balloon enteroscopy for the diagnosis of small-bowel tumors.
Study, first author,
Patients/procedures, n
Procedure1
Tumors, n (%)2
Most common tumors (%)
year, country [ref] Fry, 2009 Germany [3]
Endoscopy Essentials Reviews in the Endoscopy essentials series cite publications from the past year which, in the authors’ opinion, reflect the state-ofthe-art in endoscopy. Alongside a short summary of each paper, authors explain why they consider their selected articles to be of importance.
301/402
DBE
40 (13.3)
Adenocarcinoma (35) NET (28.5)
78/96
DBE
9 (11.5)
GIST (33) Adenocarcinoma (33)
1035/1608
DBE
144 (13.9)
Lymphoma (21.5) GIST (18.8)
Lee, 2011 Korea [7]
645/877
DBE
112 (17.4)
GIST (25.8) Lymphomas (16.1)
Chen, 2013 China [5]
400/440
DBE
67 (16.8)
1106/1652
DBE
134 (12.1)
Almeida, 2009 Portugal [4] Mitsui, 2009 Japan [6]
Cangemi, 2013 USA [8]
Adenocarcinoma (29) GIST (24.5) NET (19.4) GIST (7.5)
DBE, double-balloon enteroscopy; GIST, gastrointestinal stromal tumor; NET, neuroendocrine tumor. 1 There have been no studies published using single-balloon or spiral enteroscopy for the diagnosis of small-bowel tumors. 2 The percentage of tumors was calculated based on the number of patients.
Diaz-Tobar Claudia P et al. Small-bowel endoscopy … Endoscopy 2014; 46: 327–332
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Small-bowel endoscopy
Endoscopy essentials
Fig. 1 Common small-bowel tumors. The most common small-bowel tumors are gastrointestinal stromal tumors (GIST) (a,b) and adenocarcinomas (c, d). The submucosal location of GISTs makes them very difficult to detect using video capsule endoscopy (VCE). Often, the extraluminal part of a GIST occupies a larger volume than the intraluminal part (b). If the VCE becomes entrapped in a lumen-occluding adenocarcinoma, the VCE can be considered as having served its diagnostic purpose. However, VCE is suboptimal for the diagnosis of small-bowel tumors. Histology can only be obtained through device-assisted enteroscopy (d).
Therefore, we propose that a potential quality measure for those performing deep enteroscopy is a small-bowel polyp and tumor detection rate of 10 %. Another important finding by He et al. was that direct visualization was better with DBE than with VCE. The diagnostic yield of DBE for GIMTs was 88.3 %. DBE was superior to VCE in the diagnosis of GIMTs (sensitivity 93.5 % vs. 61.3 %, respectively). Although comparing DBE with VCE was not the primary aim of their study, the results support previous knowledge of the decreased ability of VCE to find submucosal lesions and even cancers. VCE tends to move in one direction, may not provide a panluminal view of the small bowel, and lacks the capability to remove debris from the mucosal surface. Thus, when searching for a small-bowel tumor, a diagnosis should not be made based on a negative VCE study alone, but instead the search should continue using direct visualization from device-assisted enteroscopy (DAE) and radiographic studies such as computed tomography (CT), CT angiography, or magnetic resonance tomography and enterography.
Diaz-Tobar Claudia P et al. Small-bowel endoscopy … Endoscopy 2014; 46: 327–332
Capsule endoscopy is superior to small-bowel followthrough and equivalent to ileocolonoscopy in suspected Crohn’s disease (Leighton et al., Clin Gastroenterol Hepatol 2013 [9]) !
Crohn’s disease is a chronic inflammatory condition of the gastrointestinal tract that results in local and systemic inflammation, and bowel stricturing and fistulization. Diagnosis relies on clinical history, abnormal laboratory parameters, characteristic radiologic and endoscopic changes within the gastrointestinal tract, and most importantly, specific histologic findings. However, the diagnosis of Crohn’s disease, especially in cases of isolated small-bowel involvement remains challenging. For decades great emphasis has been paid to small-bowel contrast studies such as small-bowel follow-through (SBFT) [10]. Despite being a poor test for detecting mucosal changes, SBFT continues to be used in routine clinical practice. The main use of SBFT is for the discovery of strictures or fistulas. But even for these complications this test is not always accurate. In a well-designed, prospective study, Leighton et al. from the Mayo Clinic in Scottsdale, Arizona, compared the diagnostic yields of VCE with those of SBFT in patients with suspected small-bowel Crohn’s disease [9]. A total of 80 patients with signs
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
328
Fig. 2 Inflammatory enteritis. The spectrum of inflammatory enteropathies is large. Crohn’s disease is one of the most common causes of ulcerative enteropathy. a On capsule endoscopy multiple erosions and ulcers are visible. b These lesions are also easily detectable during double-balloon enteroscopy (DBE). c However, only DBE allows for histological sampling. In this case granulomas are clearly visible. Other conditions such as common variable immunodeficiency (d, e, f) and nonsteroidal anti-inflammatory drug enteropathy (g, h, i) also result in significant mucosal damage that is often indistinguishable from Crohn’s disease. Histology is thus important to rule out other conditions that mimic Crohn’s disease (f, i).
and/or symptoms of small-bowel Crohn’s disease underwent VCE, followed by SBFT and ileocolonoscopy. Readers were blinded to other test results. The primary outcome was the diagnostic yield for inflammatory lesions found on VCE before ileocolonoscopy compared with SBFT and ileocolonoscopy. A secondary outcome was the incremental diagnostic yield of VCE vs. ileocolonoscopy and VCE vs. SBFT. The authors found that the combination of VCE and ileocolonoscopy detected 107 of 110 inflammatory lesions (97.3 %), whereas the combination of SBFT and ileocolonoscopy detected only 63 lesions (57.3 %). Interestingly, the diagnostic yield of VCE was not different from that of ileocolonoscopy. However, the diagnostic yield was higher for VCE than for SBFT. Of the 80 patients with suspected Crohn’s disease, 25 (31.3 %) had the diagnosis confirmed. A total of 11 were diag-
nosed by VCE findings alone and 5 by ileocolonoscopy findings alone. In the remaining nine patients, diagnostic findings were identified by at least two of the three modalities. No diagnoses were made on the basis of SBFT findings alone. The main conclusions of this study were that VCE was better than SBFT and equivalent to ileocolonoscopy in detecting small-bowel inflammation. Thus, ileocolonoscopy remains the initial diagnostic test of choice for evaluating patients with possible Crohn’s disease, but VCE should be used when ileocolonoscopy results are negative or if the terminal ileum cannot be evaluated. SBFT should be reserved for patients with suspected fistulizing or stricturing disease. However, other radiologic tests such as magnetic resonance enteroclysis may provide more information because they allow extraluminal organs to be evaluated [9].
Diaz-Tobar Claudia P et al. Small-bowel endoscopy … Endoscopy 2014; 46: 327–332
329
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Endoscopy essentials
Endoscopy essentials
A critical issue that still needs to be resolved is the reliability of existing VCE criteria to establish a diagnosis of Crohn’s disease. In a multicenter study comparing VCE with other endoscopic and radiologic methods, VCE had a similar sensitivity to ileocolonoscopy but lower specificity compared with CT enteroclysis or ileocolonoscopy [11]. There are many other disease processes " Fig. 2). As menthat mimic Crohn’s disease endoscopically (● tioned above, the ideal gold standard for securing a diagnosis of Crohn’s disease is histology. However, granulomas or classic histologic findings consistent with Crohn’s disease are rarely found on biopsies. Nevertheless, histology (obtained through deep enteroscopy) may play a crucial role in ruling out other conditions such as vasculitis, infections, common variable immunodeficiency, ischemia, and nonsteroidal anti-inflammatory enteropathy " Fig. 2). It should be borne in mind that deep enteroscopy, (● with its inherent ability to obtain tissue, also plays an important role in the evaluation of small-bowel Crohn’s disease [12, 13].
Long-term outcomes after single-balloon enteroscopy in patients with obscure gastrointestinal bleeding (Kushnir et al., Dig Dis Sci 2013 [14])
(35.4 %). A total of 110 patients (mean age 70.6 ± 11.3 years; 56.4 % female) were followed for a mean of 23.9 months after initial SBE. During follow-up, OGIB recurred in 39.5 % of patients in whom a source of OGIB had been identified on SBE and in 55.9 % of patients who had normal findings on SBE. OGIB recurred in 47.6 % of patients in whom small-bowel vascular lesions were treated endoscopically. None of the 13 patients in whom a nonvascular lesion was identified as the source of bleeding on SBE experienced recurrent bleeding. Although more than 50 % of patients did not experience recurrent bleeding during the followup, the more striking finding of this study was the relatively high rebleeding rate observed, which demonstrates that the long-term management of OGIB due to small-bowel vascular lesions remains quite challenging. Other investigators have found that associated disease processes such as valvular heart disease and arrhythmias, chronic renal disease, atherosclerosis, and severe anemia on presentation are factors associated with rebleeding [15, 16]. However, most studies have been relatively small and may not be replicated or their findings may not be generalizable. Thus, further larger multicenter studies that investigate the risk factors for recurrent bleeding are mandatory.
!
There is a plethora of information on the feasibility and utility of DAE for the diagnosis and treatment of obscure gastrointestinal bleeding (OGIB). However, there is still paucity of data on longterm outcomes of patients who have undergone single-balloon enteroscopy (SBE) for OGIB. Kushnir et al. from Washington University in St Louis, Missouri, evaluated the long-term outcome of patients who had undergone SBE for OGIB [14]. The authors evaluated 147 consecutive patients who underwent SBE for OGIB at a tertiary care center between 2008 and 2010. Recurrence of OGIB during follow-up through 2012 was assessed by a combination of chart review and telephone interviews. The authors found that the overall diagnostic yield of SBE was 64.6 % (95/147 patients). Findings of SBE included vascular lesions (53.7 %), small-bowel neoplasm (2.7 %), inflammatory lesions (4.8 %), and normal SBE
Double balloon enteroscopy procedure in patients with surgically altered bowel anatomy: analysis of a large prospectively collected database (Patel et al., J Laparoendosc Adv Surg Tech 2013 [17]) !
In patients with altered bowel anatomy such as Roux-en-Y reconstruction after enterobiliary or pancreatic anastomosis, gastrectomy or bariatric gastric bypass, the afferent limb is not only bypassed during the passage of food but it is also excluded from " Fig. 3). In the current era of conventional endoscopic access (● an obesity epidemic, the popularity of Roux-en-Y gastric bypass surgery for weight loss has increased dramatically. According to the American Society for Bariatric Surgery, 140 000 Roux-en-Y gastric bypass procedures were performed in the USA in 2005
Fig. 3 Deep enteroscopy in patients with Roux-enY gastric bypass (RYGB). Performing endoscopy in patients with RYGB is challenging but possible using double-balloon and single-balloon enteroscopes. a Y-anastomosis. b Retroflexion inside of the excluded stomach. c The pylorus seen from the back. d Erosive gastritis in a patient with RYGB. Erosive gastritis caused by nonsteroidal anti-inflammatory drugs (NSAIDs) can also occur, even if the drug does not touch the mucosa, such as in RYGB cases. The inflammation of prostacyclins and hence, diminished vasodilation of the gastric submucosal vessels, is due to the systemic action of NSAIDs.
Diaz-Tobar Claudia P et al. Small-bowel endoscopy … Endoscopy 2014; 46: 327–332
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[18]. The utility of DAE for performing endoscopic retrograde cholangiopancreatography (ERCP) in patients with surgically altered anatomy has been well documented [19 – 21]. However, data on DAE for evaluating the bowel and excluded stomach in patients with complex postsurgical upper gastrointestinal anatomy are still scarce. In a study based on one of the largest prospectively collected DBE databases, Patel et al. from the Mayo Clinic in Jacksonville, Florida, evaluated the diagnostic yield and complication rates of DBE in patients with surgical altered bowel anatomy [17]. The authors also evaluated the success rate of DBE in achieving complete examination of the excluded segment of the small bowel and excluded stomach in these patients. A total of 1215 DBEs were performed during a 5-year period. A total of 62 patients with a history of altered bowel anatomy underwent 53 DBEs and 11 underwent DBE-assisted ERCPs. The overall diagnostic yield of DBE was 61 % and that of DBE-assisted ERCP was 64 %. No serious early or delayed DBE-associated complications were identified. In patients with surgically altered bowel anatomy containing excluded small bowel and excluded stomach, complete examination was achieved by DBE in 92 % of cases (n = 46). The authors concluded that DBE, including DBE-assisted ERCP, is feasible, safe, and associated with reasonably high diagnostic yields in patients with surgically altered bowel anatomy [17]. Although data on DBEERCP are already well known from previous studies, the utility of DBE for evaluation of the excluded stomach and afferent limb is evident from the findings of this study. Studies such as the one by Patel et al. are important, as more and more patients will present with surgically altered upper gastrointestinal anatomy and a myriad of symptoms that require endoscopic evaluation. Interestingly, very few of the patients in the Patel study were evaluated for OGIB. We have observed that patients with previous Rouxen-Y surgery who present with OGIB have different causes of gastrointestinal bleeding compared with patients with intact anatomy. Often these patients bleed from the anastomosis (gastrojejunal, jejunojejunal, and hepaticojejunal), making their treatment " Fig. 3). The number of gastric bypass procemore challenging (● dures will continue to increase. Thus, it is mandatory that large, tertiary endoscopy centers offer the capability to evaluate and treat these patients with advanced enteroscopy methods.
Video capsule endoscopy impacts decision making in pediatric IBD: a single tertiary care center experience (Min et al., Inflamm Bowel Dis 2013 [22]) !
The utility of VCE for the diagnosis of Crohn’s disease in adult patients is well established [23]. However, few studies have evaluated the utility of VCE in children. The three main aspects that make VCE different in children are: 1) potential difficulties in swallowing, 2) potential monitoring difficulties and, 3) pathophysiologic differences in the presentation of Crohn’s disease, as proximal small-bowel disease is more common and can be a very severe manifestation of Crohn’s disease in the young patient. If the diagnosis is delayed and the management is not well conceived, these patients are likely to experience an increase risk of disease morbidity. Thus, studies evaluating the diagnostic and therapeutic consequences of VCE in the pediatric population are a valuable addition to the literature. Min et al. evaluated the added value of VCE in pediatric patients with established or suspected inflammatory bowel disease (IBD), by assessing changes in treatments and outcomes before and
after VCE [22]. A retrospective chart review was performed in children with established (n = 66) or suspected (n = 17) IBD who underwent VCE. The primary indications for VCE included patients who were being treated for Crohn’s disease and had poor growth or active symptoms (60 %), patients with ulcerative colitis/IBD-unclassified (19 %), and suspected IBD (20 %). Abnormal findings were seen on VCE in 86 % of patients with Crohn’s disease, 75 % of whom underwent treatment escalation. At 1 year after VCE examination, patients with Crohn’s disease showed increased growth and body mass index, an improved Harvey – Bradshaw index, and less inflammation as depicted by a lower mean erythrocyte sedimentation rate. In 43 % of the patients with Crohn’s disease, VCE revealed more extensive disease than concurrent imaging modalities. In patients undergoing VCE for the evaluation of suspected Crohn’s disease, VCE “ruled out” IBD in 94 %. In 50 % of patients with presumed ulcerative colitis/IBDunclassified, VCE results changed the diagnosis to Crohn’s disease. This study demonstrates that VCE can provide additional clinical information that may affect the management of pediatric patients with IBD. Furthermore, the therapeutic consequences of VCE in this study were favorable, which translated into improved outcomes. Competing interests: None
Acknowledgment !
Dr. Claudia Diaz-Tobar performed this work during her “Boston Scientific Visiting Fellowship” at the Basil I. Hirschowitz Endoscopic Center of Excellence, Division of Gastroenterology and Hepatology, University of Alabama at Birmingham, USA.
References 1 He Q, Bai Y, Zhi F-C et al. Double-balloon enteroscopy for mesenchymal tumors of the small bowel: nine years’ experience. World J Gastroenterol 2013; 19: 1820 – 1826 2 Fry LC, Gutierrez JP, Jovanovic I et al. Small bowel neoplasias: current options for diagnosis, staging and therapeutic management. Gastrointest Tumors 2014; 1: 9 – 17 3 Fry LC, Neumann H, Kuester D et al. Small bowel polyps and tumours: endoscopic detection and treatment by double-balloon enteroscopy. Aliment Pharmacol Ther 2009; 29: 135 – 142 4 Almeida N, Figueiredo P, Lopes S et al. Double-balloon enteroscopy and small bowel tumors: a South-European single-center experience. Dig Dis Sci 2009; 54: 1520 – 1524 5 Chen WG, Shan GD, Zhang H et al. Double-balloon enteroscopy in small bowel tumors: a Chinese single-center study. World J Gastroenterol 2013; 19: 3665 – 3671 6 Mitsui K, Tanaka S, Yamamoto H et al. Role of double-balloon endoscopy in the diagnosis of small-bowel tumors: the first Japanese multicenter study. Gastrointest Endosc 2009; 70: 498 – 504 7 Lee BI, Choi H, Choi KY et al. Clinical characteristics of small bowel tumors diagnosed by double-balloon endoscopy: KASID multi-center study. Dig Dis Sci 2011; 56: 2920 – 2927 8 Cangemi DJ, Patel MK, Gomez V et al. Small bowel tumors discovered during double-balloon enteroscopy: analysis of a large prospectively collected single-center database. J Clin Gastroenterol 2013; 47: 769 – 772 9 Leighton JA, Gralnek IM, Cohen SA et al. Capsule endoscopy is superior to small-bowel follow-through and equivalent to ileocolonoscopy in suspected Crohn’s disease. Clin Gastroenterol Hepatol 2013: DOI 10.1016/j.cgh.2013.09.028 [Epub ahead of print] 10 Grand DJ, Harris A, Loftus EVJr. Imaging for luminal disease and complications: CT enterography, MR enterography, small-bowel followthrough, and ultrasound. Gastroenterol Clin North Am 2012; 41: 497 – 512
Diaz-Tobar Claudia P et al. Small-bowel endoscopy … Endoscopy 2014; 46: 327–332
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Endoscopy essentials
Endoscopy essentials 11 Solem CA, Loftus EVJr, Fletcher JG et al. Small-bowel imaging in Crohn’s disease: a prospective, blinded, 4-way comparison trial. Gastrointest Endosc 2008; 68: 255 – 266 12 Schulz C, Mönkemüller K, Salheiser M et al. Double-balloon enteroscopy in the diagnosis of suspected isolated Crohn’s disease of the small bowel. Dig Endosc 2013: DOI 10.1111/den.12142 [Epub ahead of print] 13 Tharian B, Caddy G, Tham TCK. Enteroscopy in small bowel Crohn’s disease: a review. World J Gastrointest Endosc 2013; 5: 476 – 486 14 Kushnir VM, Tang M, Goodwin J et al. Long-term outcomes after singleballoon enteroscopy in patients with obscure gastrointestinal bleeding. Dig Dis Sci 2013; 58: 2572 – 2579 15 Samaha E, Rahmi G, Landi B. Long-term outcome of patients treated with double balloon enteroscopy for small bowel vascular lesions. Am J Gastroenterol 2012; 107: 240 – 246 16 Arakawa D, Ohmiya N, Nakamura M et al. Outcome after enteroscopy for patients with obscure GI bleeding: diagnostic comparison between double-balloon endoscopy and videocapsule endoscopy. Gastrointest Endosc 2009; 69: 866 – 874
Diaz-Tobar Claudia P et al. Small-bowel endoscopy … Endoscopy 2014; 46: 327–332
17 Patel MK, Horsley-Silva JL, Gomez V et al. Double balloon enteroscopy procedure in patients with surgically altered bowel anatomy: analysis of a large prospectively collected database. J Laparoendosc Adv Surg Tech 2013; 5: 409 – 413 18 Smith BR, Schauer P, Nguyen NT. Surgical approaches to the treatment of obesity: bariatric surgery. Endocrinol Metab Clin North Am 2008; 37: 943 – 964 19 Mönkemüller K, Fry LC, Bellutti M et al. ERCP with the double balloon enteroscope in patients with Roux-en-Y anastomosis. Surg Endosc 2009; 23: 1961 – 1967 20 Neumann H, Fry LC, Meyer F et al. Endoscopic retrograde cholangiopancreatography using the single balloon enteroscope technique in patients with Roux-en-Y anastomosis. Digestion 2009; 80: 52 – 57 21 Koornstra JJ, Fry LC, Mönkemüller K. ERCP with the balloon-assisted enteroscopy technique: a systematic review. Dig Dis 2008; 26: 324 – 329 22 Min SB, Le-Carlson M, Singh N et al. Video capsule endoscopy impacts decision making in pediatric IBD: a single tertiary care center experience. Inflamm Bowel Dis 2013; 19: 2139 – 2145 23 Neumann H, Fry LC, Neurath MF. Review article on current applications and future concepts of capsule endoscopy. Digestion 2013; 87: 91 – 99
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327
Authors
Claudia P. Diaz-Tobar, Lucia C. Fry, Klaus Mönkemüller
Institution
Basil I. Hirschowitz Endoscopic Center of Excellence, Division of Gastroenterology and Hepatology, Birmingham, Alabama, USA
Bibliography DOI http://dx.doi.org/ 10.1055/s-0034-1365072 Published online: 6.3.2014 Endoscopy 2014; 46: 327–332 © Georg Thieme Verlag KG Stuttgart · New York ISSN 0013-726X
Double-balloon enteroscopy for mesenchymal tumors of the small bowel: nine years experience (He et al., World J Gastroenterol 2013 [1])
Corresponding author Klaus Mönkemüller, MD, PhD, FASGE Basil I. Hirschowitz Endoscopic Center of Excellence Division of Gastroenterology and Hepatology Endoscopy Unit, JT 664 619 19th Street S Birmingham, AL 35249 USA Fax: +1-205-934-1537 [email protected]
!
Although the small intestine is the largest hollow organ of the gastrointestinal tract and its mucosa encompasses about 90 % of the luminal surface area of the digestive system, small-bowel polyps and tumors are relatively rare [2]. However, the incidence of small-bowel neoplasms has increased significantly over the past 20 years [2]. The advent of video capsule endoscopy (VCE) and deep enteroscopy has enabled the diagnosis of these lesions at earlier stages. Common smallbowel tumors include neuroendocrine tumors (NET), adenocarcinomas, lymphomas, and gastro" Table 1; intestinal stromal tumors (GIST) [3 – 8] (● " Fig. 1). However, it appears that the most ● common tumors diagnosed during deep entero" Table 1) scopy are adenocarcinomas and GISTs (● [3 – 8].
Table 1
In a retrospective, observational, cohort study of 783 patients undergoing double-balloon enteroscopy (DBE) during a 9-year period, He et al. from Zhejiang University in Hangzhou, China, found 77 patients with gastrointestinal mesenchymal tumors (GIMT) (9.8 %) [1]. Based on the available literature, it appears that mesenchymal tumors are one of the most common malignant tumors found during deep enteroscopy [6 – 7] " Table 1). However, other studies have shown (● that other tumors, such as carcinoids, are more common [3, 8]. Thus, there seems to be geographic variation in the type of tumor diagnosed. In Japan and Korea, lymphomas are diagnosed more frequently than in Europe. Nonetheless, submucosal tumors such as GIST are common across " Table 1 summarizes the key papers the world. ● published to date on deep enteroscopy for the diagnosis of small-bowel polyps and tumors. Another key observation from these studies is that the proportion of polyps and tumors detected by deep enteroscopy was about 10 % – 15 %, which was independent of geographic location [3 – 8].
Summary of studies using double-balloon enteroscopy for the diagnosis of small-bowel tumors.
Study, first author,
Patients/procedures, n
Procedure1
Tumors, n (%)2
Most common tumors (%)
year, country [ref] Fry, 2009 Germany [3]
Endoscopy Essentials Reviews in the Endoscopy essentials series cite publications from the past year which, in the authors’ opinion, reflect the state-ofthe-art in endoscopy. Alongside a short summary of each paper, authors explain why they consider their selected articles to be of importance.
301/402
DBE
40 (13.3)
Adenocarcinoma (35) NET (28.5)
78/96
DBE
9 (11.5)
GIST (33) Adenocarcinoma (33)
1035/1608
DBE
144 (13.9)
Lymphoma (21.5) GIST (18.8)
Lee, 2011 Korea [7]
645/877
DBE
112 (17.4)
GIST (25.8) Lymphomas (16.1)
Chen, 2013 China [5]
400/440
DBE
67 (16.8)
1106/1652
DBE
134 (12.1)
Almeida, 2009 Portugal [4] Mitsui, 2009 Japan [6]
Cangemi, 2013 USA [8]
Adenocarcinoma (29) GIST (24.5) NET (19.4) GIST (7.5)
DBE, double-balloon enteroscopy; GIST, gastrointestinal stromal tumor; NET, neuroendocrine tumor. 1 There have been no studies published using single-balloon or spiral enteroscopy for the diagnosis of small-bowel tumors. 2 The percentage of tumors was calculated based on the number of patients.
Diaz-Tobar Claudia P et al. Small-bowel endoscopy … Endoscopy 2014; 46: 327–332
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
Small-bowel endoscopy
Endoscopy essentials
Fig. 1 Common small-bowel tumors. The most common small-bowel tumors are gastrointestinal stromal tumors (GIST) (a,b) and adenocarcinomas (c, d). The submucosal location of GISTs makes them very difficult to detect using video capsule endoscopy (VCE). Often, the extraluminal part of a GIST occupies a larger volume than the intraluminal part (b). If the VCE becomes entrapped in a lumen-occluding adenocarcinoma, the VCE can be considered as having served its diagnostic purpose. However, VCE is suboptimal for the diagnosis of small-bowel tumors. Histology can only be obtained through device-assisted enteroscopy (d).
Therefore, we propose that a potential quality measure for those performing deep enteroscopy is a small-bowel polyp and tumor detection rate of 10 %. Another important finding by He et al. was that direct visualization was better with DBE than with VCE. The diagnostic yield of DBE for GIMTs was 88.3 %. DBE was superior to VCE in the diagnosis of GIMTs (sensitivity 93.5 % vs. 61.3 %, respectively). Although comparing DBE with VCE was not the primary aim of their study, the results support previous knowledge of the decreased ability of VCE to find submucosal lesions and even cancers. VCE tends to move in one direction, may not provide a panluminal view of the small bowel, and lacks the capability to remove debris from the mucosal surface. Thus, when searching for a small-bowel tumor, a diagnosis should not be made based on a negative VCE study alone, but instead the search should continue using direct visualization from device-assisted enteroscopy (DAE) and radiographic studies such as computed tomography (CT), CT angiography, or magnetic resonance tomography and enterography.
Diaz-Tobar Claudia P et al. Small-bowel endoscopy … Endoscopy 2014; 46: 327–332
Capsule endoscopy is superior to small-bowel followthrough and equivalent to ileocolonoscopy in suspected Crohn’s disease (Leighton et al., Clin Gastroenterol Hepatol 2013 [9]) !
Crohn’s disease is a chronic inflammatory condition of the gastrointestinal tract that results in local and systemic inflammation, and bowel stricturing and fistulization. Diagnosis relies on clinical history, abnormal laboratory parameters, characteristic radiologic and endoscopic changes within the gastrointestinal tract, and most importantly, specific histologic findings. However, the diagnosis of Crohn’s disease, especially in cases of isolated small-bowel involvement remains challenging. For decades great emphasis has been paid to small-bowel contrast studies such as small-bowel follow-through (SBFT) [10]. Despite being a poor test for detecting mucosal changes, SBFT continues to be used in routine clinical practice. The main use of SBFT is for the discovery of strictures or fistulas. But even for these complications this test is not always accurate. In a well-designed, prospective study, Leighton et al. from the Mayo Clinic in Scottsdale, Arizona, compared the diagnostic yields of VCE with those of SBFT in patients with suspected small-bowel Crohn’s disease [9]. A total of 80 patients with signs
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
328
Fig. 2 Inflammatory enteritis. The spectrum of inflammatory enteropathies is large. Crohn’s disease is one of the most common causes of ulcerative enteropathy. a On capsule endoscopy multiple erosions and ulcers are visible. b These lesions are also easily detectable during double-balloon enteroscopy (DBE). c However, only DBE allows for histological sampling. In this case granulomas are clearly visible. Other conditions such as common variable immunodeficiency (d, e, f) and nonsteroidal anti-inflammatory drug enteropathy (g, h, i) also result in significant mucosal damage that is often indistinguishable from Crohn’s disease. Histology is thus important to rule out other conditions that mimic Crohn’s disease (f, i).
and/or symptoms of small-bowel Crohn’s disease underwent VCE, followed by SBFT and ileocolonoscopy. Readers were blinded to other test results. The primary outcome was the diagnostic yield for inflammatory lesions found on VCE before ileocolonoscopy compared with SBFT and ileocolonoscopy. A secondary outcome was the incremental diagnostic yield of VCE vs. ileocolonoscopy and VCE vs. SBFT. The authors found that the combination of VCE and ileocolonoscopy detected 107 of 110 inflammatory lesions (97.3 %), whereas the combination of SBFT and ileocolonoscopy detected only 63 lesions (57.3 %). Interestingly, the diagnostic yield of VCE was not different from that of ileocolonoscopy. However, the diagnostic yield was higher for VCE than for SBFT. Of the 80 patients with suspected Crohn’s disease, 25 (31.3 %) had the diagnosis confirmed. A total of 11 were diag-
nosed by VCE findings alone and 5 by ileocolonoscopy findings alone. In the remaining nine patients, diagnostic findings were identified by at least two of the three modalities. No diagnoses were made on the basis of SBFT findings alone. The main conclusions of this study were that VCE was better than SBFT and equivalent to ileocolonoscopy in detecting small-bowel inflammation. Thus, ileocolonoscopy remains the initial diagnostic test of choice for evaluating patients with possible Crohn’s disease, but VCE should be used when ileocolonoscopy results are negative or if the terminal ileum cannot be evaluated. SBFT should be reserved for patients with suspected fistulizing or stricturing disease. However, other radiologic tests such as magnetic resonance enteroclysis may provide more information because they allow extraluminal organs to be evaluated [9].
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A critical issue that still needs to be resolved is the reliability of existing VCE criteria to establish a diagnosis of Crohn’s disease. In a multicenter study comparing VCE with other endoscopic and radiologic methods, VCE had a similar sensitivity to ileocolonoscopy but lower specificity compared with CT enteroclysis or ileocolonoscopy [11]. There are many other disease processes " Fig. 2). As menthat mimic Crohn’s disease endoscopically (● tioned above, the ideal gold standard for securing a diagnosis of Crohn’s disease is histology. However, granulomas or classic histologic findings consistent with Crohn’s disease are rarely found on biopsies. Nevertheless, histology (obtained through deep enteroscopy) may play a crucial role in ruling out other conditions such as vasculitis, infections, common variable immunodeficiency, ischemia, and nonsteroidal anti-inflammatory enteropathy " Fig. 2). It should be borne in mind that deep enteroscopy, (● with its inherent ability to obtain tissue, also plays an important role in the evaluation of small-bowel Crohn’s disease [12, 13].
Long-term outcomes after single-balloon enteroscopy in patients with obscure gastrointestinal bleeding (Kushnir et al., Dig Dis Sci 2013 [14])
(35.4 %). A total of 110 patients (mean age 70.6 ± 11.3 years; 56.4 % female) were followed for a mean of 23.9 months after initial SBE. During follow-up, OGIB recurred in 39.5 % of patients in whom a source of OGIB had been identified on SBE and in 55.9 % of patients who had normal findings on SBE. OGIB recurred in 47.6 % of patients in whom small-bowel vascular lesions were treated endoscopically. None of the 13 patients in whom a nonvascular lesion was identified as the source of bleeding on SBE experienced recurrent bleeding. Although more than 50 % of patients did not experience recurrent bleeding during the followup, the more striking finding of this study was the relatively high rebleeding rate observed, which demonstrates that the long-term management of OGIB due to small-bowel vascular lesions remains quite challenging. Other investigators have found that associated disease processes such as valvular heart disease and arrhythmias, chronic renal disease, atherosclerosis, and severe anemia on presentation are factors associated with rebleeding [15, 16]. However, most studies have been relatively small and may not be replicated or their findings may not be generalizable. Thus, further larger multicenter studies that investigate the risk factors for recurrent bleeding are mandatory.
!
There is a plethora of information on the feasibility and utility of DAE for the diagnosis and treatment of obscure gastrointestinal bleeding (OGIB). However, there is still paucity of data on longterm outcomes of patients who have undergone single-balloon enteroscopy (SBE) for OGIB. Kushnir et al. from Washington University in St Louis, Missouri, evaluated the long-term outcome of patients who had undergone SBE for OGIB [14]. The authors evaluated 147 consecutive patients who underwent SBE for OGIB at a tertiary care center between 2008 and 2010. Recurrence of OGIB during follow-up through 2012 was assessed by a combination of chart review and telephone interviews. The authors found that the overall diagnostic yield of SBE was 64.6 % (95/147 patients). Findings of SBE included vascular lesions (53.7 %), small-bowel neoplasm (2.7 %), inflammatory lesions (4.8 %), and normal SBE
Double balloon enteroscopy procedure in patients with surgically altered bowel anatomy: analysis of a large prospectively collected database (Patel et al., J Laparoendosc Adv Surg Tech 2013 [17]) !
In patients with altered bowel anatomy such as Roux-en-Y reconstruction after enterobiliary or pancreatic anastomosis, gastrectomy or bariatric gastric bypass, the afferent limb is not only bypassed during the passage of food but it is also excluded from " Fig. 3). In the current era of conventional endoscopic access (● an obesity epidemic, the popularity of Roux-en-Y gastric bypass surgery for weight loss has increased dramatically. According to the American Society for Bariatric Surgery, 140 000 Roux-en-Y gastric bypass procedures were performed in the USA in 2005
Fig. 3 Deep enteroscopy in patients with Roux-enY gastric bypass (RYGB). Performing endoscopy in patients with RYGB is challenging but possible using double-balloon and single-balloon enteroscopes. a Y-anastomosis. b Retroflexion inside of the excluded stomach. c The pylorus seen from the back. d Erosive gastritis in a patient with RYGB. Erosive gastritis caused by nonsteroidal anti-inflammatory drugs (NSAIDs) can also occur, even if the drug does not touch the mucosa, such as in RYGB cases. The inflammation of prostacyclins and hence, diminished vasodilation of the gastric submucosal vessels, is due to the systemic action of NSAIDs.
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[18]. The utility of DAE for performing endoscopic retrograde cholangiopancreatography (ERCP) in patients with surgically altered anatomy has been well documented [19 – 21]. However, data on DAE for evaluating the bowel and excluded stomach in patients with complex postsurgical upper gastrointestinal anatomy are still scarce. In a study based on one of the largest prospectively collected DBE databases, Patel et al. from the Mayo Clinic in Jacksonville, Florida, evaluated the diagnostic yield and complication rates of DBE in patients with surgical altered bowel anatomy [17]. The authors also evaluated the success rate of DBE in achieving complete examination of the excluded segment of the small bowel and excluded stomach in these patients. A total of 1215 DBEs were performed during a 5-year period. A total of 62 patients with a history of altered bowel anatomy underwent 53 DBEs and 11 underwent DBE-assisted ERCPs. The overall diagnostic yield of DBE was 61 % and that of DBE-assisted ERCP was 64 %. No serious early or delayed DBE-associated complications were identified. In patients with surgically altered bowel anatomy containing excluded small bowel and excluded stomach, complete examination was achieved by DBE in 92 % of cases (n = 46). The authors concluded that DBE, including DBE-assisted ERCP, is feasible, safe, and associated with reasonably high diagnostic yields in patients with surgically altered bowel anatomy [17]. Although data on DBEERCP are already well known from previous studies, the utility of DBE for evaluation of the excluded stomach and afferent limb is evident from the findings of this study. Studies such as the one by Patel et al. are important, as more and more patients will present with surgically altered upper gastrointestinal anatomy and a myriad of symptoms that require endoscopic evaluation. Interestingly, very few of the patients in the Patel study were evaluated for OGIB. We have observed that patients with previous Rouxen-Y surgery who present with OGIB have different causes of gastrointestinal bleeding compared with patients with intact anatomy. Often these patients bleed from the anastomosis (gastrojejunal, jejunojejunal, and hepaticojejunal), making their treatment " Fig. 3). The number of gastric bypass procemore challenging (● dures will continue to increase. Thus, it is mandatory that large, tertiary endoscopy centers offer the capability to evaluate and treat these patients with advanced enteroscopy methods.
Video capsule endoscopy impacts decision making in pediatric IBD: a single tertiary care center experience (Min et al., Inflamm Bowel Dis 2013 [22]) !
The utility of VCE for the diagnosis of Crohn’s disease in adult patients is well established [23]. However, few studies have evaluated the utility of VCE in children. The three main aspects that make VCE different in children are: 1) potential difficulties in swallowing, 2) potential monitoring difficulties and, 3) pathophysiologic differences in the presentation of Crohn’s disease, as proximal small-bowel disease is more common and can be a very severe manifestation of Crohn’s disease in the young patient. If the diagnosis is delayed and the management is not well conceived, these patients are likely to experience an increase risk of disease morbidity. Thus, studies evaluating the diagnostic and therapeutic consequences of VCE in the pediatric population are a valuable addition to the literature. Min et al. evaluated the added value of VCE in pediatric patients with established or suspected inflammatory bowel disease (IBD), by assessing changes in treatments and outcomes before and
after VCE [22]. A retrospective chart review was performed in children with established (n = 66) or suspected (n = 17) IBD who underwent VCE. The primary indications for VCE included patients who were being treated for Crohn’s disease and had poor growth or active symptoms (60 %), patients with ulcerative colitis/IBD-unclassified (19 %), and suspected IBD (20 %). Abnormal findings were seen on VCE in 86 % of patients with Crohn’s disease, 75 % of whom underwent treatment escalation. At 1 year after VCE examination, patients with Crohn’s disease showed increased growth and body mass index, an improved Harvey – Bradshaw index, and less inflammation as depicted by a lower mean erythrocyte sedimentation rate. In 43 % of the patients with Crohn’s disease, VCE revealed more extensive disease than concurrent imaging modalities. In patients undergoing VCE for the evaluation of suspected Crohn’s disease, VCE “ruled out” IBD in 94 %. In 50 % of patients with presumed ulcerative colitis/IBDunclassified, VCE results changed the diagnosis to Crohn’s disease. This study demonstrates that VCE can provide additional clinical information that may affect the management of pediatric patients with IBD. Furthermore, the therapeutic consequences of VCE in this study were favorable, which translated into improved outcomes. Competing interests: None
Acknowledgment !
Dr. Claudia Diaz-Tobar performed this work during her “Boston Scientific Visiting Fellowship” at the Basil I. Hirschowitz Endoscopic Center of Excellence, Division of Gastroenterology and Hepatology, University of Alabama at Birmingham, USA.
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