ORIGINAL ARTICLE
Retrieval of Retained Capsule Endoscopy at Small Bowel Stricture by Double-Balloon Endoscopy Significantly Decreases Surgical Treatment Keigo Mitsui, MD, PhD, Shunji Fujimori, MD, PhD, Shu Tanaka, MD, PhD, Akihito Ehara, MD, Jun Omori, MD, Naohiko Akimoto, MD, Kotaro Maki, MD, Masahiro Suzuki, MD, Yuki Kosugi, MD, Yukiko Ensaka, MD, Yoko Matsuura, MD, PhD, Tsuyoshi Kobayashi, MD, Masaoki Yonezawa, MD, PhD, Atsushi Tatsuguchi, MD, PhD, and Choitsu Sakamoto, MD, PhD
Goals: The aim is to elucidate the efficacy and safety of doubleballoon endoscopy (DBE) for small bowel capsule endoscopy (SBCE) retrieval from small bowel stricture and to follow the outcome of the stricture where the SBCE was entrapped. Background: The retention of SBCE is a serious adverse event and most retained capsules are retrieved by surgery. There is still no report analyzing the follow-up of patients with stricture after retrieval of entrapped SBCEs by DBE. Methods: This study was designed a retrospective cohort study. Subjects were 12 consecutive patients with small bowel stricture where retrieval of entrapped SBCE was attempted using DBE. Success rate of the SBCE retrieval by DBE, surgical rate of the small bowel stricture, adverse events of DBE, and outcomes in the follow-up period were evaluated. Results: Diagnoses were Crohn’s disease, nonsteroidal antiinflammatory drugs–induced enteropathy, ischemic enteritis, and carcinoma in 8, 2, 1, and 1 patients, respectively. SBCE was successfully retrieved in 11 of the 12 patients (92%). No adverse events were encountered in all endoscopic procedures such as retrieval of SBCEs and dilation of the strictures. Nine of the 12 patients (75%) did not undergo surgical treatment for the stricture where SBCE was entrapped through the follow-up period (mean, 1675 ± 847 d). Conclusions: Retrieval of SBCEs using DBE was safe, had a high success rate, and was useful to evaluate the need for surgery. Seventy-five percent of patients with small bowel stricture where the SBCE was entrapped did not require surgery through approximately 5 years. Key Words: small bowel, stricture, capsule endoscopy, doubleballoon endoscopy, foreign body removal, outcome
(J Clin Gastroenterol 2016;50:141–146)
I
nnovative advances in enteroscopy with small bowel capsule endoscopy (SBCE)1 and double-balloon endoscopy (DBE)2 enable a high-diagnostic yield for small bowel Received for publication September 23, 2014; accepted March 23, 2015. From the Department of Gastroenterology, Nippon Medical School, Graduate School of Medicine, Tokyo, Japan. The authors declare that they have nothing to disclose. Reprints: Keigo Mitsui, MD, PhD, Department of Gastroenterology, Nippon Medical School, Graduate School of Medicine, 1-1-5, Sendagi, Bunkyo-ku, Tokyo 113-8603, Japan (e-mail: [email protected]). Copyright r 2015 Wolters Kluwer Health, Inc. All rights reserved.
J Clin Gastroenterol
Volume 50, Number 2, February 2016
disease. SBCE is a suitable tool for screening and DBE is a predominant tool for detailed observation and various endoscopic therapies. There is no doubt that SBCE is less invasive for patients and a primary endoscopic tool for small bowel examination. However, capsule endoscopy examination rarely causes the serious adverse event of capsule retention at a small bowel stricture. SBCE retention occurred in 1.4% to 2.5% of patients examined for various indications. SBCE retention occurred more frequently in patients with Crohn’s disease and with complicated abdominal pain in previous large studies (Table 1).3–7 Various attempts have been made to avoid SBCE retention. One study shows that clinical history and radiographic examination including computed tomography and enteroclysis8 may predict the risk of SBCE retention. Recently, the Agile Patency capsule, which is one of the promising tools to resolve the problem, is available.9–13 However, in obscure gastrointestinal bleeding (OGIB), which is the most frequent indication for SBCE, early examination from the beginning of symptomatic bleeding correlates with high-diagnostic yields revealed in studies using SBCE and DBE.14,15 Using the patency capsule before SBCE delays the SBCE examination, which may result in a decreased diagnostic yield. If SBCE retention occurs, removal is basically necessary. Several reports suggest that DBE is useful in removing capsules from small bowel strictures.16–19 At the same time, DBE is also useful for the evaluation and treatment of the small bowel stricture.20–22 However, these reports consist of only 8 case series and 1 or 2 actual case experiences. Currently, SBCE removal by surgery is the most common practice globally. In previous reports, surgical retrieval is performed in 53% to 100% cases and the rate of surgical treatment differs significantly by institution. Many institutions perform all extractions by surgery due to the notion that it is necessary to operate on the site of stenosis.6,7 In contrast, only a single recent case series reports that more than half of subjects suffering capsule retention are neoplastic cases, and recommends operation.23 Small bowel stenosis often arises as a consequence of benign diseases such as Crohn’s disease and nonsteroidal anti-inflammatory drugs (NSAID) enteropathy, for which stenosis does not necessarily require operative treatment. Thus, evidence is still lacking as to whether all patients having a stenosis where an SBCE is retained should undergo operation immediately. Furthermore, the long-term outcome of the www.jcge.com |
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TABLE 1. Previous Reports About Retention and Retrieval of SBCE
References
Indication of SBCE
No. SBCE
No. Retentions [n (%)]
Retrieval
Li et al3 Cheon et al4
Various Various
1000 pts 1291 pts
14 (1.4) 32 (2.5)
Rondonotti et al5
Various
733 pts
14 (1.9)
Cheifetz et al6
Known CD
38 pts
5 (13.2)
Fry et al7
Suspected CD Abdominal pain
64 pts 68 pts
1 (1.6) 2 (2.9)
Surgery Surgery Medical therapy DBE Surgery Push enteroscopy Colonoscopy Reject surgery Surgery Reject surgery Surgery Surgery
n (%) 13 17 11 4 11 1 1 1 4 1 1 2
(92.9) (53.1) (34.4) (12.5) (78.6) (7.1) (71) (7.1) (80.0) (20.0) (100) (100)
CD indicates Crohn’s disease; pts, patients; SBCE, small bowel capsule endoscopy.
benign stricture where the SBCE was entrapped is also unknown. The aim of the study is to evaluate the ability of DBE for removing retained SBCEs from small bowel strictures, and to determine the necessity of surgical intervention for strictures where SBCEs are entrapped; furthermore, to clarify whether these strictures require surgery during the follow-up period.
MATERIALS AND METHODS Patients Subjects were 12 consecutive patients on whom retrieval of capsule endoscopy by DBE at the small bowel was attempted, between September 2004 and March 2013, at Nippon Medical School, Tokyo. During the study period, 896 DBEs were performed at our institution. The patients consisted of 11 males and 1 female; mean age was 44 ± 17 years (range, 22 to 81 y). Indications of SBCE were OGIB in 9 (75.0%) and unexplained abdominal pain in 3 (25.0%) patients. The bleeding types of 9 patients with OGIB were hematochezia, melena, and occult bleeding in 2, 4, and 3 patients, respectively. Patient findings of SBCE, symptom of entrapment, term of retention, findings of DBE, site of stricture, device for retrieval, and diagnosis and outcome in the follow-up period were retrospectively reviewed and evaluated. Details are shown in Table 2. Each patient enrolled in this study was followed up either at the authors’ hospital or affiliated facilities until the end of the study in March 2013. In the outpatient clinic, patients were directly interviewed, and in affiliated facilities, data were obtained through electronic medical record system and telephone contact. This study was approved by the authors’ institutional review board.
Capsule Endoscopy Before capsule endoscopy, all patients had undergone a clinical history and physical examination, and appropriate laboratory tests and radiologic examinations including computed tomography. The Given video capsule system was used (Pillcam; Given Imaging Ltd., Yoqneam, Israel). Capsule endoscopy procedures, including methods for reviewing images, were conducted as previously described. Briefly, after a 12-hour fast, subjects were equipped with a sensor array and recorder/battery belt pack and given a capsule to swallow, which transmitted
continuous video images at 2 frames per second for over 8 hours, at which point the apparatus was disconnected and the images processed. All video images were analyzed by skilled reviewers.
DBE DBE was performed by using 2 high-resolution video endoscopes (Fujinon Corp., Saitama, Japan): (1) an EN450P5/20 endoscope with a 200 cm working length, 8.5 mm outer diameter, 2.2 mm working channel, and a 145 cm flexible overtube with an outer diameter of 12.2 mm; and (2) a EN-450T5/W endoscope with a 200 cm working length, an outer diameter of 9.4 mm, a 2.8 mm working channel, and a 145 cm flexible overtube with an outer diameter of 13.2 mm. At first, all analyzed patients underwent the antegrade DBE to try removing the retained SBCE. Preparation for all oral DBE examination was overnight fasting only in all patients. The localization of small bowel stricture was determined by the summation of each insertion length24 and x-ray fluoroscopy with contrast medium TABLE 2. Patient Demographics Gender Age (y) Follow-up period (d) Indication of SBCE OGIB Hematochezia Melena Occult Unexplained abdominal pain Insertion route of DBE Antegrade Device for capture of SBCE Net forcep Snare forcep Basket forcep Not attempted Diagnosis Crohn’s disease NSAIDs enteropathy Ischemic enteritis Carcinoma
11 males 1 female 44 ± 17 (range, 22-81) 1675 ± 847 (range, 74-3114) 9 cases (75.0%) 2 cases 4 cases 3 cases 3 cases (25.0%) 12 cases (100%) 9 cases 1 case 1 case 1 case
(75.0%) (8.3%) (8.3%) (8.3%)
8 cases 2 cases 1 case 1 case
(66.7%) (16.7%) (8.3%) (8.3%)
DBE indicates double-balloon endoscopy; NSAIDs, nonsteroidal antiinflammatory drugs; OGIB, obscure gastrointestinal bleeding; SBCE, small bowel capsule endoscopy.
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J Clin Gastroenterol
Volume 50, Number 2, February 2016
during DBE. The jejunum was defined as the proximal two fifths of the length, and the distal three fifths as the ileum.
Efficacy and Safety of DBE for SBCE Retrieval
not need surgical treatment for stenosis for the approximate 5 years following SBCE entrapment.
Methods of Diagnosis and Removing Retained SBCE When patients had not confirmed evacuation of the SBCE at the next defecation or it was suspected to be retained at a small bowel stricture by reviewing the SBCE result, an abdominal plain x-ray was taken. If it was judged that SBCE remained in the small bowel, DBE was performed as soon as possible with an antegrade approach. If DBE showed the retained SBCE at a small bowel stricture, the SBCE was retrieved after the evaluation of the stricture, such as the observation of the stricture, biopsy, and fluoroscopy. Forceps were chosen depending on the diameter of the channel.
Statistical Analysis Results are presented as a mean (SD or range) for continuous data and frequency (percentage) for categorical data. Cumulative nonsurgery rate was calculated by the Kaplan-Meier method using Graphpad Prism 5 for Windows.
RESULTS The characteristics of analyzed patients are shown in Table 2. Final diagnoses of the 12 patients were 8 Crohn’s disease (including suspicion), 2 NSAIDs enteropathy, 1 ischemic enteritis, and 1 jejunal carcinoma. The mean follow-up period was 1675 ± 847 days (range, 74 to 3114 d). Detailed individual data including endoscopic findings are shown in Table 3. The sites of stricture were jejunum in 4 (33.3%) and ileum in 8 (66.7%) patients. In all patients, mucosal abnormalities were detected by SBCE at the entrapped site. The strictures were detected by SBCE in 9 (75.0%) patients. The mean entrapped period of SBCE was 31 ± 49 days (range, 1 to 156 d). According to the definition of the International Conference on Capsule Endoscopy (ICCE), 4 patients presented SBCE retention and 8 presented regional transit abnormality 2. Obstructive symptom due to SBCE entrapment was not encountered. DBE showed stricture and entrapped SBCE in 11 (91.7%) patients. DBE successfully removed the entrapped SBCE in all of them. The devices of retrieval were net, basket, and snare forcep in 9, 1, and 1 patients, respectively. No adverse event was encountered in all DBE examinations, including SBCE retrieval. In the remaining 1 patient with strictures (8.3%), entrapped SBCE was not observed. However, the strictures were successfully evaluated by fluoroscopy using DBE to diagnose as Crohn’s disease and the need for surgical intervention (Figs. 1A–D). One patient with Crohn’s disease underwent surgery to resect the stenotic lesions. After the entrapped SBCE was retrieved in 11 patients, 2 patients underwent surgery to resect the stenotic lesions during the follow-up period (mean, 1687 ± 918 d), because 1 patient was diagnosed with advanced small bowel carcinoma, and the other with ischemic enteritis with recurrent stenotic symptoms after endoscopic dilation by DBE about 2 years later. Surgical treatment was not performed on the remaining 9 patients including 1 patient with Crohn’s disease after endoscopic dilation by DBE (Figs. 1E– H). Figure 2 shows the cumulative nonsurgery rate by Kaplan Meier curve. Seventy-four percent of patients did Copyright
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DISCUSSION Overall, 3 of the 12 patients (25%) required the surgery for both retrieval of SBCE and treatment for small bowel stricture in this study. After the successful removal of entrapped SBCE at small bowel stricture by enteroscopy, only 2 out of 11 patients (18%) underwent surgery for small bowel stricture during the follow-up period. DBE was useful not only to remove the entrapped SBCE, but also to evaluate the lesion of stricture for indication of surgery. Furthermore, DBE was useful to treat the stenosis by balloon dilation in Crohn’s disease, which was the most common disease in the study. It is presumed that the balloon dilation therapy leads to a decrease in surgical rate for Crohn’s disease.25 In addition, the indication criteria of surgery using imaging devices for small bowel stenosis are equivocal and complex. Surgery was performed in only 2 out of 11 patients over the approximate 5-year follow-up period, indicating that SBCE entrapment does not necessarily mean that surgical intervention is required. Only 1 out of 12 retained SBCE patients (8.3%) required surgery to retrieve the SBCE from the small bowel stricture in this study. This rate is very low compared with previous reports.3–7 Although the SBCE could not be retrieved by DBE, stenosis could be identified by DBE as an indication of the surgical intervention. This fact suggests a high possibility of surgical indication for lesions where SBCE is not removed by DBE. If surgery is unnecessary following retained SBCE removal by DBE, the number of patient hospitalization days and medical costs may be decreased. In the present study, the use of DBE enabled a high rate of retrieval for entrapped SBCE irrespective of the small bowel site. It can be attributed to the recent advancement in skill through deep insertion into the small bowel by the antegrade approach. The recommended approach is the antegrade insertion of the scope wherever the SBCE is retained to remove it. In the study, all ileal SBCEs with the exception of 1 were removed by the antegrade approach. The retrograde approach should be considered when there is concern about the difficulty of deep insertion by the antegrade approach. Regarding the cases in this study, it was found that endoscopic intervention for strictures must be done before retrieval, and successful dilation therapy is crucial when choosing the retrograde approach. Of the 8 patients in this study, DBE was performed without waiting for 2 weeks when SBCE revealed severe stenosis as in Figures 1A–D. In these cases, SBCE examinations did not meet the ICCE definition for “retention,” which is entrapment for >2 weeks. In most cases admitted in this study, DBE was performed shortly after SBCE to reduce the duration of hospitalization. In the study cases, it was ascertained that SBCEs would be entrapped for a prolonged period of time because DBE showed the stricture diameter to be only 2 to 3 mm. Therefore, several retained SBCEs were removed before 2 weeks passed, because it was assumed that SBCE entrapment would become permanent. The correlation between the waiting period of entrapment and natural evacuation of SBCEs is an issue to address in the future.
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57 52
47
22
33 44
66
31
33
33
81
2 3
4
5
6 7
8
9
10
11
12
Ulcer, stricture Stricture Irregular mucosa
Ulcer, SMT OGIB Hematochezia Ulcer, stricture OGIB Melena Ulcer OGIB Occult Ulcer, bleeding stricture OGIB Melena Ulcer, stricture Abdominal Abdominal Ulcer, pain pain stricture OGIB Occult Ulcer, bleeding stricture OGIB Melena Ulcer, stricture OGIB Occult Ulcer, bleeding stricture
Abdominal Abdominal pain pain OGIB Hematochezia Abdominal Abdominal pain pain, melena OGIB Melena
SBCE Findings
3 (RTA2)
5 (RTA2)
156
3 (RTA2)
4 (RTA2)
57 3 (RTA2)
38
3 (RTA2)
1 (RTA2) 4 (RTA2)
94
Term of Retention (d)
Exacerbation of Symptom After SBCE
Ulcer, stricture
Ulcer, stricture
Ulcer, stricture
Ulcer, stricture
Ulcer, stricture
Ulcer, stricture Ulcer, stricture
Ulcer, stricture
Ulcer, stricture
Ulcer, stricture Circumferential tumor
Ulcer, stricture
DBE Findings
Ileum
Ileum
Ileum
Ileum
Jejunum
Ileum Ileum
Jejunum
Ileum
Jejunum Jejunum
Ileum
Net
Net
Net
Net
Snare
Net Not tried
Net
Net
Net Basket
Net
NSAIDs
CD
NSAIDs
Ischemia
CD
CD CD
CD
CD
CD Carcinoma
CD
EBD, surgery
Surgery
EBD
Surgery
Site of Device for Intervention Stricture Retrieval Diagnosis for Stricture
—
—
—
4 (665)
—
— (12)
0
—
— (20)
—
Term Until Intervention (surgery) (d)
74
1344
1210
1476
1748
1863 1859
1841
2225
2787 553
3114
Followup (d)
M
M
F
M
M
M M
M
M
M M
M
Pre-SBCE Symptoms
J Clin Gastroenterol
CD indicates Crohn’s disease; EBD, endoscopic balloon dilation; OGIB, obscure gastrointestinal bleeding; RTA2, regional transit abnormality 2; SMT, submucosal tumor; SBCE, small bowel capsule endoscopy.
33
1
Age Indication Case (y) Gender of SBCE
TABLE 3. Clinical Features and Endoscopic Findings of 12 Patients
Mitsui et al Volume 50, Number 2, February 2016
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Efficacy and Safety of DBE for SBCE Retrieval
FIGURE 1. A and B, Endoscopic views of ileal ulcer and stricture before the site of retention. C and D, Fluoroscopic views of the retention site. E–G, Endoscopic views of the circumferential ulcer and stricture of the jejunum, and retrieval with a net forcep. H, Fluoroscopic findings of the stricture and retained small bowel capsule endoscopy.
The majority of patients in the study were male. The frequency of Crohn’s disease in this study and the previous report is similar.4 Male is the dominant gender for Crohn’s disease in Japan. Recently, medical therapy for Crohn’s Copyright
r
disease is advancing, enabling delayed disease progression. This could explain the low number of patients requiring balloon dilation in the study period. If surgery for stenosis can be avoided by endoscopic balloon dilation, the removal
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10. 11.
12.
13.
14. FIGURE 2. Cumulative nonsurgery rate of stenosis.
of a retained SBCE is important as these patients may otherwise be controlled by medical therapy. In conclusion, retrieval of entrapped SBCE by DBE was performed safely at a high success rate. Furthermore, most small bowel strictures that retained SBCE did not require surgical procedures in this prolonged approximate 5-year follow-up period. Thus, SBCE retention alone does not mean an indication for surgical intervention for small bowel stricture. REFERENCES 1. Iddan G, Meron G, Glukhovsky A, et al. Wireless capsule endoscopy. Nature. 2000;405:417. 2. Yamamoto H, Sekine Y, Sato Y, et al. Total enteroscopy with a nonsurgical steerable double-balloon method. Gastrointest Endosc. 2001;53:216–220. 3. Li F, Gurudu SR, De Petris G, et al. Retention of the capsule endoscope: a single-center experience of 1000 capsule endoscopy procedures. Gastrointest Endosc. 2008;68:174–180. 4. Cheon JH, Kim YS, Lee IS, et al. Can we predict spontaneous capsule passage after retention? A nationwide study to evaluate the incidence and clinical outcomes of capsule retention. Endoscopy. 2007;39:1046–1052. 5. Rondonotti E, Herrerias JM, Pennazio M, et al. Complications, limitations, and failures of capsule endoscopy: a review of 733 cases. Gastrointest Endosc. 2005;62:712–716, quiz 752, 754. 6. Cheifetz AS, Kornbluth AA, Legnani P, et al. The risk of retention of the capsule endoscope in patients with known or suspected Crohn’s disease. Am J Gastroenterol. 2006;101:2218–2222. 7. Fry LC, Carey EJ, Shiff AD, et al. The yield of capsule endoscopy in patients with abdominal pain or diarrhea. Endoscopy. 2006;38:498–502. 8. Matsumoto T, Esaki M, Kurahara K, et al. Double-contrast barium enteroclysis as a patency tool for nonsteroidal antiinflammatory drug-induced enteropathy. Dig Dis Sci. 2011;56: 3247–3253. 9. Delvaux M, Ben Soussan E, Laurent V, et al. Clinical evaluation of the use of the M2A patency capsule system
15. 16.
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before a capsule endoscopy procedure, in patients with known or suspected intestinal stenosis. Endoscopy. 2005;37:801–807. Leighton JA. Recent advances in endoscopic capsule imaging: see what we have been missing. Rev Gastroenterol Disord. 2006;6(suppl 1):S19–S27. Spada C, Shah SK, Riccioni ME, et al. Video capsule endoscopy in patients with known or suspected small bowel stricture previously tested with the dissolving patency capsule. J Clin Gastroenterol. 2007;41:576–582. Herrerias JM, Leighton JA, Costamagna G, et al. Agile patency system eliminates risk of capsule retention in patients with known intestinal strictures who undergo capsule endoscopy. Gastrointest Endosc. 2008;67:902–909. Postgate AJ, Burling D, Gupta A, et al. Safety, reliability and limitations of the given patency capsule in patients at risk of capsule retention: a 3-year technical review. Dig Dis Sci. 2008; 53:2732–2738. 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;126:643–653. Tanaka S, Mitsui K, Yamada Y, et al. Diagnostic yield of double-balloon endoscopy in patients with obscure GI bleeding. Gastrointest Endosc. 2008;68:683–691. Tanaka S, Mitsui K, Shirakawa K, et al. Successful retrieval of video capsule endoscopy retained at ileal stenosis of Crohn’s disease using double-balloon endoscopy. J Gastroenterol Hepatol. 2006;21:922–923. Al-toma A, Hadithi M, Heine D, et al. Retrieval of a video capsule endoscope by using a double-balloon endoscope. Gastrointest Endosc. 2005;62:613. Lee BI, Choi H, Choi KY, et al. Retrieval of a retained capsule endoscope by double-balloon enteroscopy. Gastrointest Endosc. 2005;62:463–465. May A, Nachbar L, Ell C. Extraction of entrapped capsules from the small bowel by means of push-and-pull enteroscopy with the double-balloon technique. Endoscopy. 2005;37: 591–593. Sunada K, Yamamoto H, Kita H, et al. Clinical outcomes of enteroscopy using the double-balloon method for strictures of the small intestine. World J Gastroenterol. 2005;11:1087–1089. Ohmiya N, Arakawa D, Nakamura M, et al. Small-bowel obstruction: diagnostic comparison between double-balloon endoscopy and fluoroscopic enteroclysis, and the outcome of enteroscopic treatment. Gastrointest Endosc. 2009;69:84–93. Fukumoto A, Tanaka S, Yamamoto H, et al. Diagnosis and treatment of small-bowel stricture by double balloon endoscopy. Gastrointest Endosc. 2007;66:S108–S112. Van Weyenberg SJ, Van Turenhout ST, Bouma G, et al. Double-balloon endoscopy as the primary method for smallbowel video capsule endoscope retrieval. Gastrointest Endosc. 2010;71:535–541. May A, Nachbar L, Schneider M, et al. Push-and-pull enteroscopy using the double-balloon technique: method of assessing depth of insertion and training of the enteroscopy technique using the Erlangen Endo-Trainer. Endoscopy. 2005; 37:66–70. Hirai F, Beppu T, Takatsu N, et al. Long-term outcome of endoscopic balloon dilation for small bowel strictures in patients with Crohn’s disease. Dig Endosc. 2014;26:545–551.
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Retrieval of Retained Capsule Endoscopy at Small Bowel Stricture by Double-Balloon Endoscopy Significantly Decreases Surgical Treatment Keigo Mitsui, MD, PhD, Shunji Fujimori, MD, PhD, Shu Tanaka, MD, PhD, Akihito Ehara, MD, Jun Omori, MD, Naohiko Akimoto, MD, Kotaro Maki, MD, Masahiro Suzuki, MD, Yuki Kosugi, MD, Yukiko Ensaka, MD, Yoko Matsuura, MD, PhD, Tsuyoshi Kobayashi, MD, Masaoki Yonezawa, MD, PhD, Atsushi Tatsuguchi, MD, PhD, and Choitsu Sakamoto, MD, PhD
Goals: The aim is to elucidate the efficacy and safety of doubleballoon endoscopy (DBE) for small bowel capsule endoscopy (SBCE) retrieval from small bowel stricture and to follow the outcome of the stricture where the SBCE was entrapped. Background: The retention of SBCE is a serious adverse event and most retained capsules are retrieved by surgery. There is still no report analyzing the follow-up of patients with stricture after retrieval of entrapped SBCEs by DBE. Methods: This study was designed a retrospective cohort study. Subjects were 12 consecutive patients with small bowel stricture where retrieval of entrapped SBCE was attempted using DBE. Success rate of the SBCE retrieval by DBE, surgical rate of the small bowel stricture, adverse events of DBE, and outcomes in the follow-up period were evaluated. Results: Diagnoses were Crohn’s disease, nonsteroidal antiinflammatory drugs–induced enteropathy, ischemic enteritis, and carcinoma in 8, 2, 1, and 1 patients, respectively. SBCE was successfully retrieved in 11 of the 12 patients (92%). No adverse events were encountered in all endoscopic procedures such as retrieval of SBCEs and dilation of the strictures. Nine of the 12 patients (75%) did not undergo surgical treatment for the stricture where SBCE was entrapped through the follow-up period (mean, 1675 ± 847 d). Conclusions: Retrieval of SBCEs using DBE was safe, had a high success rate, and was useful to evaluate the need for surgery. Seventy-five percent of patients with small bowel stricture where the SBCE was entrapped did not require surgery through approximately 5 years. Key Words: small bowel, stricture, capsule endoscopy, doubleballoon endoscopy, foreign body removal, outcome
(J Clin Gastroenterol 2016;50:141–146)
I
nnovative advances in enteroscopy with small bowel capsule endoscopy (SBCE)1 and double-balloon endoscopy (DBE)2 enable a high-diagnostic yield for small bowel Received for publication September 23, 2014; accepted March 23, 2015. From the Department of Gastroenterology, Nippon Medical School, Graduate School of Medicine, Tokyo, Japan. The authors declare that they have nothing to disclose. Reprints: Keigo Mitsui, MD, PhD, Department of Gastroenterology, Nippon Medical School, Graduate School of Medicine, 1-1-5, Sendagi, Bunkyo-ku, Tokyo 113-8603, Japan (e-mail: [email protected]). Copyright r 2015 Wolters Kluwer Health, Inc. All rights reserved.
J Clin Gastroenterol
Volume 50, Number 2, February 2016
disease. SBCE is a suitable tool for screening and DBE is a predominant tool for detailed observation and various endoscopic therapies. There is no doubt that SBCE is less invasive for patients and a primary endoscopic tool for small bowel examination. However, capsule endoscopy examination rarely causes the serious adverse event of capsule retention at a small bowel stricture. SBCE retention occurred in 1.4% to 2.5% of patients examined for various indications. SBCE retention occurred more frequently in patients with Crohn’s disease and with complicated abdominal pain in previous large studies (Table 1).3–7 Various attempts have been made to avoid SBCE retention. One study shows that clinical history and radiographic examination including computed tomography and enteroclysis8 may predict the risk of SBCE retention. Recently, the Agile Patency capsule, which is one of the promising tools to resolve the problem, is available.9–13 However, in obscure gastrointestinal bleeding (OGIB), which is the most frequent indication for SBCE, early examination from the beginning of symptomatic bleeding correlates with high-diagnostic yields revealed in studies using SBCE and DBE.14,15 Using the patency capsule before SBCE delays the SBCE examination, which may result in a decreased diagnostic yield. If SBCE retention occurs, removal is basically necessary. Several reports suggest that DBE is useful in removing capsules from small bowel strictures.16–19 At the same time, DBE is also useful for the evaluation and treatment of the small bowel stricture.20–22 However, these reports consist of only 8 case series and 1 or 2 actual case experiences. Currently, SBCE removal by surgery is the most common practice globally. In previous reports, surgical retrieval is performed in 53% to 100% cases and the rate of surgical treatment differs significantly by institution. Many institutions perform all extractions by surgery due to the notion that it is necessary to operate on the site of stenosis.6,7 In contrast, only a single recent case series reports that more than half of subjects suffering capsule retention are neoplastic cases, and recommends operation.23 Small bowel stenosis often arises as a consequence of benign diseases such as Crohn’s disease and nonsteroidal anti-inflammatory drugs (NSAID) enteropathy, for which stenosis does not necessarily require operative treatment. Thus, evidence is still lacking as to whether all patients having a stenosis where an SBCE is retained should undergo operation immediately. Furthermore, the long-term outcome of the www.jcge.com |
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TABLE 1. Previous Reports About Retention and Retrieval of SBCE
References
Indication of SBCE
No. SBCE
No. Retentions [n (%)]
Retrieval
Li et al3 Cheon et al4
Various Various
1000 pts 1291 pts
14 (1.4) 32 (2.5)
Rondonotti et al5
Various
733 pts
14 (1.9)
Cheifetz et al6
Known CD
38 pts
5 (13.2)
Fry et al7
Suspected CD Abdominal pain
64 pts 68 pts
1 (1.6) 2 (2.9)
Surgery Surgery Medical therapy DBE Surgery Push enteroscopy Colonoscopy Reject surgery Surgery Reject surgery Surgery Surgery
n (%) 13 17 11 4 11 1 1 1 4 1 1 2
(92.9) (53.1) (34.4) (12.5) (78.6) (7.1) (71) (7.1) (80.0) (20.0) (100) (100)
CD indicates Crohn’s disease; pts, patients; SBCE, small bowel capsule endoscopy.
benign stricture where the SBCE was entrapped is also unknown. The aim of the study is to evaluate the ability of DBE for removing retained SBCEs from small bowel strictures, and to determine the necessity of surgical intervention for strictures where SBCEs are entrapped; furthermore, to clarify whether these strictures require surgery during the follow-up period.
MATERIALS AND METHODS Patients Subjects were 12 consecutive patients on whom retrieval of capsule endoscopy by DBE at the small bowel was attempted, between September 2004 and March 2013, at Nippon Medical School, Tokyo. During the study period, 896 DBEs were performed at our institution. The patients consisted of 11 males and 1 female; mean age was 44 ± 17 years (range, 22 to 81 y). Indications of SBCE were OGIB in 9 (75.0%) and unexplained abdominal pain in 3 (25.0%) patients. The bleeding types of 9 patients with OGIB were hematochezia, melena, and occult bleeding in 2, 4, and 3 patients, respectively. Patient findings of SBCE, symptom of entrapment, term of retention, findings of DBE, site of stricture, device for retrieval, and diagnosis and outcome in the follow-up period were retrospectively reviewed and evaluated. Details are shown in Table 2. Each patient enrolled in this study was followed up either at the authors’ hospital or affiliated facilities until the end of the study in March 2013. In the outpatient clinic, patients were directly interviewed, and in affiliated facilities, data were obtained through electronic medical record system and telephone contact. This study was approved by the authors’ institutional review board.
Capsule Endoscopy Before capsule endoscopy, all patients had undergone a clinical history and physical examination, and appropriate laboratory tests and radiologic examinations including computed tomography. The Given video capsule system was used (Pillcam; Given Imaging Ltd., Yoqneam, Israel). Capsule endoscopy procedures, including methods for reviewing images, were conducted as previously described. Briefly, after a 12-hour fast, subjects were equipped with a sensor array and recorder/battery belt pack and given a capsule to swallow, which transmitted
continuous video images at 2 frames per second for over 8 hours, at which point the apparatus was disconnected and the images processed. All video images were analyzed by skilled reviewers.
DBE DBE was performed by using 2 high-resolution video endoscopes (Fujinon Corp., Saitama, Japan): (1) an EN450P5/20 endoscope with a 200 cm working length, 8.5 mm outer diameter, 2.2 mm working channel, and a 145 cm flexible overtube with an outer diameter of 12.2 mm; and (2) a EN-450T5/W endoscope with a 200 cm working length, an outer diameter of 9.4 mm, a 2.8 mm working channel, and a 145 cm flexible overtube with an outer diameter of 13.2 mm. At first, all analyzed patients underwent the antegrade DBE to try removing the retained SBCE. Preparation for all oral DBE examination was overnight fasting only in all patients. The localization of small bowel stricture was determined by the summation of each insertion length24 and x-ray fluoroscopy with contrast medium TABLE 2. Patient Demographics Gender Age (y) Follow-up period (d) Indication of SBCE OGIB Hematochezia Melena Occult Unexplained abdominal pain Insertion route of DBE Antegrade Device for capture of SBCE Net forcep Snare forcep Basket forcep Not attempted Diagnosis Crohn’s disease NSAIDs enteropathy Ischemic enteritis Carcinoma
11 males 1 female 44 ± 17 (range, 22-81) 1675 ± 847 (range, 74-3114) 9 cases (75.0%) 2 cases 4 cases 3 cases 3 cases (25.0%) 12 cases (100%) 9 cases 1 case 1 case 1 case
(75.0%) (8.3%) (8.3%) (8.3%)
8 cases 2 cases 1 case 1 case
(66.7%) (16.7%) (8.3%) (8.3%)
DBE indicates double-balloon endoscopy; NSAIDs, nonsteroidal antiinflammatory drugs; OGIB, obscure gastrointestinal bleeding; SBCE, small bowel capsule endoscopy.
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J Clin Gastroenterol
Volume 50, Number 2, February 2016
during DBE. The jejunum was defined as the proximal two fifths of the length, and the distal three fifths as the ileum.
Efficacy and Safety of DBE for SBCE Retrieval
not need surgical treatment for stenosis for the approximate 5 years following SBCE entrapment.
Methods of Diagnosis and Removing Retained SBCE When patients had not confirmed evacuation of the SBCE at the next defecation or it was suspected to be retained at a small bowel stricture by reviewing the SBCE result, an abdominal plain x-ray was taken. If it was judged that SBCE remained in the small bowel, DBE was performed as soon as possible with an antegrade approach. If DBE showed the retained SBCE at a small bowel stricture, the SBCE was retrieved after the evaluation of the stricture, such as the observation of the stricture, biopsy, and fluoroscopy. Forceps were chosen depending on the diameter of the channel.
Statistical Analysis Results are presented as a mean (SD or range) for continuous data and frequency (percentage) for categorical data. Cumulative nonsurgery rate was calculated by the Kaplan-Meier method using Graphpad Prism 5 for Windows.
RESULTS The characteristics of analyzed patients are shown in Table 2. Final diagnoses of the 12 patients were 8 Crohn’s disease (including suspicion), 2 NSAIDs enteropathy, 1 ischemic enteritis, and 1 jejunal carcinoma. The mean follow-up period was 1675 ± 847 days (range, 74 to 3114 d). Detailed individual data including endoscopic findings are shown in Table 3. The sites of stricture were jejunum in 4 (33.3%) and ileum in 8 (66.7%) patients. In all patients, mucosal abnormalities were detected by SBCE at the entrapped site. The strictures were detected by SBCE in 9 (75.0%) patients. The mean entrapped period of SBCE was 31 ± 49 days (range, 1 to 156 d). According to the definition of the International Conference on Capsule Endoscopy (ICCE), 4 patients presented SBCE retention and 8 presented regional transit abnormality 2. Obstructive symptom due to SBCE entrapment was not encountered. DBE showed stricture and entrapped SBCE in 11 (91.7%) patients. DBE successfully removed the entrapped SBCE in all of them. The devices of retrieval were net, basket, and snare forcep in 9, 1, and 1 patients, respectively. No adverse event was encountered in all DBE examinations, including SBCE retrieval. In the remaining 1 patient with strictures (8.3%), entrapped SBCE was not observed. However, the strictures were successfully evaluated by fluoroscopy using DBE to diagnose as Crohn’s disease and the need for surgical intervention (Figs. 1A–D). One patient with Crohn’s disease underwent surgery to resect the stenotic lesions. After the entrapped SBCE was retrieved in 11 patients, 2 patients underwent surgery to resect the stenotic lesions during the follow-up period (mean, 1687 ± 918 d), because 1 patient was diagnosed with advanced small bowel carcinoma, and the other with ischemic enteritis with recurrent stenotic symptoms after endoscopic dilation by DBE about 2 years later. Surgical treatment was not performed on the remaining 9 patients including 1 patient with Crohn’s disease after endoscopic dilation by DBE (Figs. 1E– H). Figure 2 shows the cumulative nonsurgery rate by Kaplan Meier curve. Seventy-four percent of patients did Copyright
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DISCUSSION Overall, 3 of the 12 patients (25%) required the surgery for both retrieval of SBCE and treatment for small bowel stricture in this study. After the successful removal of entrapped SBCE at small bowel stricture by enteroscopy, only 2 out of 11 patients (18%) underwent surgery for small bowel stricture during the follow-up period. DBE was useful not only to remove the entrapped SBCE, but also to evaluate the lesion of stricture for indication of surgery. Furthermore, DBE was useful to treat the stenosis by balloon dilation in Crohn’s disease, which was the most common disease in the study. It is presumed that the balloon dilation therapy leads to a decrease in surgical rate for Crohn’s disease.25 In addition, the indication criteria of surgery using imaging devices for small bowel stenosis are equivocal and complex. Surgery was performed in only 2 out of 11 patients over the approximate 5-year follow-up period, indicating that SBCE entrapment does not necessarily mean that surgical intervention is required. Only 1 out of 12 retained SBCE patients (8.3%) required surgery to retrieve the SBCE from the small bowel stricture in this study. This rate is very low compared with previous reports.3–7 Although the SBCE could not be retrieved by DBE, stenosis could be identified by DBE as an indication of the surgical intervention. This fact suggests a high possibility of surgical indication for lesions where SBCE is not removed by DBE. If surgery is unnecessary following retained SBCE removal by DBE, the number of patient hospitalization days and medical costs may be decreased. In the present study, the use of DBE enabled a high rate of retrieval for entrapped SBCE irrespective of the small bowel site. It can be attributed to the recent advancement in skill through deep insertion into the small bowel by the antegrade approach. The recommended approach is the antegrade insertion of the scope wherever the SBCE is retained to remove it. In the study, all ileal SBCEs with the exception of 1 were removed by the antegrade approach. The retrograde approach should be considered when there is concern about the difficulty of deep insertion by the antegrade approach. Regarding the cases in this study, it was found that endoscopic intervention for strictures must be done before retrieval, and successful dilation therapy is crucial when choosing the retrograde approach. Of the 8 patients in this study, DBE was performed without waiting for 2 weeks when SBCE revealed severe stenosis as in Figures 1A–D. In these cases, SBCE examinations did not meet the ICCE definition for “retention,” which is entrapment for >2 weeks. In most cases admitted in this study, DBE was performed shortly after SBCE to reduce the duration of hospitalization. In the study cases, it was ascertained that SBCEs would be entrapped for a prolonged period of time because DBE showed the stricture diameter to be only 2 to 3 mm. Therefore, several retained SBCEs were removed before 2 weeks passed, because it was assumed that SBCE entrapment would become permanent. The correlation between the waiting period of entrapment and natural evacuation of SBCEs is an issue to address in the future.
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57 52
47
22
33 44
66
31
33
33
81
2 3
4
5
6 7
8
9
10
11
12
Ulcer, stricture Stricture Irregular mucosa
Ulcer, SMT OGIB Hematochezia Ulcer, stricture OGIB Melena Ulcer OGIB Occult Ulcer, bleeding stricture OGIB Melena Ulcer, stricture Abdominal Abdominal Ulcer, pain pain stricture OGIB Occult Ulcer, bleeding stricture OGIB Melena Ulcer, stricture OGIB Occult Ulcer, bleeding stricture
Abdominal Abdominal pain pain OGIB Hematochezia Abdominal Abdominal pain pain, melena OGIB Melena
SBCE Findings
3 (RTA2)
5 (RTA2)
156
3 (RTA2)
4 (RTA2)
57 3 (RTA2)
38
3 (RTA2)
1 (RTA2) 4 (RTA2)
94
Term of Retention (d)
Exacerbation of Symptom After SBCE
Ulcer, stricture
Ulcer, stricture
Ulcer, stricture
Ulcer, stricture
Ulcer, stricture
Ulcer, stricture Ulcer, stricture
Ulcer, stricture
Ulcer, stricture
Ulcer, stricture Circumferential tumor
Ulcer, stricture
DBE Findings
Ileum
Ileum
Ileum
Ileum
Jejunum
Ileum Ileum
Jejunum
Ileum
Jejunum Jejunum
Ileum
Net
Net
Net
Net
Snare
Net Not tried
Net
Net
Net Basket
Net
NSAIDs
CD
NSAIDs
Ischemia
CD
CD CD
CD
CD
CD Carcinoma
CD
EBD, surgery
Surgery
EBD
Surgery
Site of Device for Intervention Stricture Retrieval Diagnosis for Stricture
—
—
—
4 (665)
—
— (12)
0
—
— (20)
—
Term Until Intervention (surgery) (d)
74
1344
1210
1476
1748
1863 1859
1841
2225
2787 553
3114
Followup (d)
M
M
F
M
M
M M
M
M
M M
M
Pre-SBCE Symptoms
J Clin Gastroenterol
CD indicates Crohn’s disease; EBD, endoscopic balloon dilation; OGIB, obscure gastrointestinal bleeding; RTA2, regional transit abnormality 2; SMT, submucosal tumor; SBCE, small bowel capsule endoscopy.
33
1
Age Indication Case (y) Gender of SBCE
TABLE 3. Clinical Features and Endoscopic Findings of 12 Patients
Mitsui et al Volume 50, Number 2, February 2016
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Efficacy and Safety of DBE for SBCE Retrieval
FIGURE 1. A and B, Endoscopic views of ileal ulcer and stricture before the site of retention. C and D, Fluoroscopic views of the retention site. E–G, Endoscopic views of the circumferential ulcer and stricture of the jejunum, and retrieval with a net forcep. H, Fluoroscopic findings of the stricture and retained small bowel capsule endoscopy.
The majority of patients in the study were male. The frequency of Crohn’s disease in this study and the previous report is similar.4 Male is the dominant gender for Crohn’s disease in Japan. Recently, medical therapy for Crohn’s Copyright
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disease is advancing, enabling delayed disease progression. This could explain the low number of patients requiring balloon dilation in the study period. If surgery for stenosis can be avoided by endoscopic balloon dilation, the removal
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J Clin Gastroenterol
Mitsui et al
10. 11.
12.
13.
14. FIGURE 2. Cumulative nonsurgery rate of stenosis.
of a retained SBCE is important as these patients may otherwise be controlled by medical therapy. In conclusion, retrieval of entrapped SBCE by DBE was performed safely at a high success rate. Furthermore, most small bowel strictures that retained SBCE did not require surgical procedures in this prolonged approximate 5-year follow-up period. Thus, SBCE retention alone does not mean an indication for surgical intervention for small bowel stricture. REFERENCES 1. Iddan G, Meron G, Glukhovsky A, et al. Wireless capsule endoscopy. Nature. 2000;405:417. 2. Yamamoto H, Sekine Y, Sato Y, et al. Total enteroscopy with a nonsurgical steerable double-balloon method. Gastrointest Endosc. 2001;53:216–220. 3. Li F, Gurudu SR, De Petris G, et al. Retention of the capsule endoscope: a single-center experience of 1000 capsule endoscopy procedures. Gastrointest Endosc. 2008;68:174–180. 4. Cheon JH, Kim YS, Lee IS, et al. Can we predict spontaneous capsule passage after retention? A nationwide study to evaluate the incidence and clinical outcomes of capsule retention. Endoscopy. 2007;39:1046–1052. 5. Rondonotti E, Herrerias JM, Pennazio M, et al. Complications, limitations, and failures of capsule endoscopy: a review of 733 cases. Gastrointest Endosc. 2005;62:712–716, quiz 752, 754. 6. Cheifetz AS, Kornbluth AA, Legnani P, et al. The risk of retention of the capsule endoscope in patients with known or suspected Crohn’s disease. Am J Gastroenterol. 2006;101:2218–2222. 7. Fry LC, Carey EJ, Shiff AD, et al. The yield of capsule endoscopy in patients with abdominal pain or diarrhea. Endoscopy. 2006;38:498–502. 8. Matsumoto T, Esaki M, Kurahara K, et al. Double-contrast barium enteroclysis as a patency tool for nonsteroidal antiinflammatory drug-induced enteropathy. Dig Dis Sci. 2011;56: 3247–3253. 9. Delvaux M, Ben Soussan E, Laurent V, et al. Clinical evaluation of the use of the M2A patency capsule system
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