A retrospective study of the application on double-balloon enteroscopy in 378 patients with suspected small-bowel diseases

• Introduction
• Patients and methods
• Results
• DBE procedure and diagnostic yields
• DBE results, management decisions, and patient outcomes
• Severity of obscure gastrointestinal bleeding pre- and post-DBE
• Complications of diagnostic and therapeutic DBE procedures
• Discussion
• References

Background and study aims: The diagnostic yield of double-balloon enteroscopy (DBE) is variable, depending on the indication for the investigaton. The aim of this study was to investigate the diagnostic yield of DBE, and impact on subsequent management. Patients and methods: A total of 378 patients with obscure gastrointestinal bleeding, abdominal pain, diarrhea, or small-bowel obstruction were included in this retrospective study. DBE procedures were followed by active treatments, symptomatic treatments, or follow-up without any treatment. A special scoring system was designed for evaluating the severity of gastrointestinal bleeding, and the scores were compared before and after DBE examination. Results: Lesions were detected in 247/378 patients (65.3 %). The diagnostic yields were 80.6 % for obscure gastrointestinal bleeding, 37.7 % for abdominal pain, 36.5 % for diarrhea, and 81.3 % for small-bowel obstruction. In 208/247 patients with a confirmed diagnosis (84.2 %), specific treatments were performed. Symptoms disappeared or improved in 190/208 patients (91.3 %). The mean score (± standard deviation) for the severity of gastrointestinal bleeding in the 154 patients with positive findings before DBE was 6.8 ± 2.2, and this dropped to 1.5 ± 0.5 (P < 0.01) in patients who underwent specific treatments, to 3.6 ± 0.7 (P < 0.05) in patients who received symptomatic relief, and to 3.9 ± 0.9 (P < 0.05) in patients who received no treatment. Conclusions: Double-balloon enteroscopy had high diagnostic yield in patients with obscure gastrointestinal bleeding and obstruction. The results of DBE had a substantial impact on subsequent management decisions.

Introduction

Elucidation of the cause of small-bowel disease is usually an extraordinarily difficult job because of the length and arrangement of this section of the bowel and because of the lack of diagnostic tools which can directly visualize the whole small bowel. However, two novel techniques, capsule endoscopy and double-balloon enteroscopy (DBE), have been developed and applied to clinical practice since the turn of the century. Several clinical studies of capsule endoscopy and early studies of DBE have suggested that the diagnostic yields of these two techniques are markedly higher than the yields of other classic methods, such as push-enteroscopy and enteroclysis [1] [2] [3]. DBE not only allows the entire small bowel to be visualized, usually by combining peroral and peranal examinations, but also allows some endotherapeutic interventions [4] [5]. Decisions on the clinical management of small-bowel diseases depend mainly on the availability of a confirmed diagnosis. To date, a few studies have focused on the influence of the diagnostic results of capsule endoscopy on patient management and follow-up, but no similar clinical study of DBE has been available because of the relatively short duration of its application. In this retrospective study, the diagnostic yield of DBE in 378 patients with a variety of indications was evaluated, and the impact of the results of the DBE examination on the subsequent management of patients was also studied during a 6-month follow-up period.

Patients and methods

The double-balloon endoscopes used in the study were manufactured by Fujinon (EN-450P5/20, EN-450T5/20; Fujinon Inc, Saitama, Japan). The DBE system comprised a main processor, the enteroscope, an overtube, and air-controlling pump. Latex balloons were attached at the tips of the enteroscope and the overtube. The therapeutic enteroscope (EN-450T5/20) had a 2.8-mm working channel, which permitted the introduction of therapeutic accessories. The principles of the DBE technique and details of the insertion procedure have been described by others. The enteroscope could be inserted either via the oral route (i. e. antegrade) or the anal route (i. e. retrograde) [6]. India ink (0.5 - 1.0 mL) was injected submucosally as a tattoo to mark where the enteroscope had reached into the small bowel, and this was used at the next procedure (performed from the opposite route, and on another day) to ensure that the entire small bowel was visualized.

The measurement of the length of the examined small bowel was based on an estimated calculation. During the procedure, the maximal distance of each advancement of the enteroscope was about 40 cm while the overtube balloon was inflated. But the actual distance of each movement was not so extensive and had to be estimated. At the end of the procedure, the recorded lengths of all the scope advances were added up. It was our experience that there was about a 10 % - 15 % deviation in bowel length assessment between the endoscopists’ estimation and the measurements the surgeons made during exploratory operations in patients with surgical indications.

DBE via the oral route was performed after 12 hours’ fasting. DBE via the anal route was preceded by the same bowel cleansing routine used before colonoscopy. In most cases, DBE could be performed under conscious sedation (intravenous midazolam, 0.05 - 0.1 mg/kg). General anesthesia (intravenous propofol, 1 - 2 mg/kg per hour) was needed in 42 procedures. Theoretically, all patients need both antegrade and retrograde DBE, but, in practice, we only used both approaches in patients with negative findings but alarming symptoms, especially in cases of obscure gastrointestinal bleeding.

From April 2003 to June 2005, 378 patients with a variety of indications were included in the DBE study. All patients were followed up clinically for at least 6 months after the examination and subsequent management. The study was finished in January 2006 and no patients dropped out during the follow-up period. A total of 378 patients were enrolled: 236 patients from our own clinical center and 142 patients referred from other hospitals; 243 men (mean age ± standard deviation [SD] 54.1 ± 13.6 years, range 7 - 82 years; and 135 women (mean age ± SD 49 ± 15.6 years, range 9 - 78 years). The indications were obscure gastrointestinal bleeding (n = 191), abdominal pain (n = 69), diarrhea/malabsorption of unknown cause (n = 63), or small-bowel obstruction (n = 48). Seven patients with specific manifestations (fever and diarrhea one patient, flushing and abdominal pain in one patient, fecal urine in one patient, intestinal-vaginal fistula in one patient, eosinophilia in two patients, and a family history of Peutz-Jeghers syndrome in one patient) also underwent DBE examination.

All patients with obscure gastrointestinal bleeding had undergone both gastroscopy and ileocolonoscopy with negative findings prior to DBE. In our clinic, ileoscopy is included in the colonoscopy procedure, particularly in patients with gastrointestinal bleeding. Gastrointestinal bleeding accounts for 30 % of all colonoscopy procedures. A special scoring system for assessing the severity of obscure gastrointestinal bleeding was developed (see [Table 1]).

Patients with abdominal pain were included if they fulfilled the following criteria: (a) duration of symptoms > 6 months; (b) no evidence of irritable bowel syndrome (excluded on the basis of the Rome II criteria); (c) no apparent cause found on clinical examination or relevant investigations (gastroscopy, pancolonoscopy, abdominal ultrasonography, computed tomography [CT]); (d) no active gynecological disorders in female patients; (e) presence of concomitant symptoms, but with abdominal pain the principal symptom; (f) progressive worsening or at least failure to respond after formal medical treatments.

Patients with diarrhea were included if they fulfilled the following criteria: (a) duration of symptoms > 6 months; (b) infectious causes excluded; (c) no apparent cause (e. g. diabetes, hyperthyroidism) found on clinical examination or relevant investigations (gastroscopy, pancolonoscopy, abdominal ultrasonography, CT); (d) diarrheal type of irritable bowel syndrome excluded; (e) liver, pancreas, and gallbladder diseases excluded; (f) progressive worsening or at least failure to respond after symptomatic treatments.

Many of the patients underwent other traditional examinations prior to DBE, including enteroclysis (n = 53, 14 %), capsule endoscopy (n = 32, 8.5 %), multislice CT enterography (n = 28, 7.4 %), and angiography (n = 22, 6 %), but no confirmatory diagnosis was obtained from these investigations. In patients with obscure gastrointestinal bleeding, an average of 2.4 gastroscopies and 1.6 ileocolonoscopies were performed per patient. The route of the DBE procedure (i. e. antegrade or retrograde) was determined on the basis of findings of previous investigations and the clinical presentation.

Written consent was obtained from all patients for the DBE procedures, including examination via the other approach if the initial procedure failed to find lesions, and for potential endoscopic interventions. The end points of the study were the diagnostic yield of DBE in patients with different indications and the impact of the DBE results on management decisions and prognosis during the 6-month follow-up period.

Results

DBE procedure and diagnostic yields

DBE was performed perorally in 139 patients (36.8 %), and via the anus in 146 patients; both routes were used in 93 patients (24.6 %), of whom 53 patients (55.9 %) had their entire small bowel successfully visualized. The length of the small bowel examined ranged from 30 cm to 360 cm (mean ± SD, 210 cm ± 70 cm) above the ileocecal valve in anal-route examinations, and from 20 cm to 460 cm (mean ± SD, 280 ± 120 cm) below the ligament of Treitz in oral-route examinations.

The diagnostic yield reached 69.1 % in antegrade procedures, 64.4 % in retrograde procedures, and 61.3 % in patients examined via both routes. The overall diagnostic yield of the DBE procedures was 65.3 % (247/378).

The diagnostic yields for each indication and procedure route are listed in [Table 2]. The lesions detected by DBE in patients with different indications are listed in [Table 3], and illustated in [Figure 1] - [Figure 10].

DBE results, management decisions, and patient outcomes

Different treatments were carried out in patients with different indications after the DBE examination. Patients with a confirmed diagnosis after DBE underwent specific treatments, including targeted medication, endoscopic intervention, or surgical exploration or resection. Patients whose diagnosis was made or whose lesion was detected by DBE but for whom no specific management was indicated received symptomatic treatment or were followed up without any treatment. Surgical intervention was recommended in patients with tumor or carvernous angioma. For active bleeding from angiodysplasia seen during DBE, we performed argon plasma coagulation (APC) or occasionally used metal clips to achieve hemostasis. For benign strictures, we performed dilation. For patients with Crohn’s disease and patients with multiple angiodysplasias, we recommended medication and follow-up. If there were no positive findings, we monitored patients closely.

Specific management was organized in 208/247 patients (84.2 %) with a definitive diagnosis. Relevant symptoms disappeared or were controlled in 190/247 patients with positive DBE findings (76.9 %). Symptomatic treatment was given to 28 patients with a confirmed diagnosis; 11 patients were followed up without any treatment. The symptoms in 20 of the 39 patients who were either receiving symptomatic treatment alone or who were just being followed up were not relieved. The outcomes of different management pathways in patients with positive findings on DBE are summarized in [Table 4].

Among the patients with obscure gastrointestinal bleeding, two patients with Crohn’s disease developed intermittent melena while on steroids and immunosuppressant therapy and were referred for segmental bowel resection. One patient diagnosed as having a small-bowel ulcer caused by a nonsteroidal anti-inflammatory drug could not be persuaded to stop using the causative drug and had another episode of black stool during the follow-up period. One patient with radiation enteritis had a bloody stool, and one patient with ileal tuberculosis had a positive fecal occult blood test.

A patient with an adenoma in the proximal jejunum developed active bleeding after removal of the adenoma. The bleeding was stopped after treatment using a metal clip. Massive bleeding recommenced 1 week later, and the patient was readmitted and underwent emergency surgery. Two patients with multiple angiodysplasias developed melena intermittently during the follow-up period, despite undergoing APC therapy to the lesions during the DBE procedure. One patient with jejunal carcinoma underwent palliative resection (due to peritoneal metastasis), but died 5 months later. Hemostasis was achieved in one patient with lymphoma after segmental bowel resection, but a small-bowel obstruction developed 4 months later. One patient had a positive fecal occult blood test 4 months after a partial small-bowel resection.

Of the patients with obscure gastrointestinal bleeding who received symptomatic treatment, bleeding was observed in one patient with deep anastomotic ulcers during the follow-up period but this resolved after surgical reconstruction; rebleeding was noted in seven patients - one patient with a nonspecific ulcer of the jejunum, two patients with arteriovenous malformations, two patients with angiodysplasia, and two patients with diverticulosis. Of the patients who did not receive any treatment, three patients (one patient with blind-loop bleeding, one patient with angiodysplasia, and one patient with diverticulosis) passed black stools during the observation period after the DBE examination.

Of the patients with abdominal pain, one patient who was diagnosed with Crohn’s disease still had persistent pain in the right lower quadrant and an intestino-anal fistula was observed while they were taking specific medication. One patient obtained partial symptomatic relief after endoscopic removal of a 2-cm pedunculated adenoma. Bouts of abdominal pain increased in frequency in two patients (one patient had a nonspecific ulcer and one patient had a postoperative adhesion) despite symptomatic treatment. The features and intensity of the pain in the patient with an ileal lipoma remained unchanged.

Of the 131 patients with negative findings after DBE procedures, symptoms either did not relapse or were not aggravated in 40 patients. Symptoms recurred in 37 patients who did not have further examinations during the 6-month follow-up period. Of the 54 patients whose symptoms reappeared during follow-up, 26 patients underwent repeated DBE examination and 28 patients underwent investigations by other methods: positive findings were obtained in 14/54 patients. The results of follow-up in patients with negative findings on DBE examination are also summarized in [Table 4].

Severity of obscure gastrointestinal bleeding pre- and post-DBE

The severity of obscure gastrointestinal bleeding was scored before DBE and again during the post-DBE follow-up period after specific treatments were given (according to the DBE findings). The results are summarized in [Table 5].

Complications of diagnostic and therapeutic DBE procedures

Most of the patients experienced mild to moderate abdominal distension and pain that resolved spontaneously a few hours later. Sore throat was frequently observed in patients examined via the oral route, but no specific treatment was needed. In two patients the serum amylase was raised in conjunction with epigastric pain, but this improved after symptomatic treatments. One patient who was diagnosed with Crohn’s disease on the basis of four endoscopic biopsies developed severe abdominal pain and intraperitoneal free gas. He was treated conservatively and by day 5 he had made a good recovery.

One of the 20 patients who had undergone an endotherapeutic intervention developed active bleeding after removal of an adenoma (1.2 cm in size). The hemorrhage was successfully stopped after endoscopic metal clipping. Unfortunately, massive bleeding occurred 1 week later and the patient developed hypovolemic shock. The patient was referred for emergency resection of the bleeding segment. In another patient with obscure gastrointestinal bleeding, a movable ball-like lesion, 2 cm in diameter and with oozing bleeding on its surface, was detected in the proximal jejunum (60 cm below the ligament of Treitz) at antegrade DBE examination. However, nothing was found during a exploratory operation 7 days later, even after intraoperative endoscopy has been performed.

Discussion

The diagnosis of small-bowel diseases has posed a problem in clinical practice until now because of the length and arrangement of this part of the bowel and because the routine diagnostic methods available have been insensitive and inaccurate. Direct endoscopic observation is the most valuable tool for visualizing mucosal and submucosal lesions of the small intestine. Push-enteroscopy fails to detect lesions deep in the small bowel because of limitations in the length of bowel it can examine. The diagnostic capability for detecting small-bowel lesions has been greatly improved, however, since the development and application of two promising diagnostic modalities early in the 21st century - capsule endoscopy and double-balloon enteroscopy.

Capsule endoscopy is a painless procedure that enables visualization of the entire small bowel and is highly acceptable to both doctors and patients. Several comparative studies revealed that the diagnostic yield and accuracy of capsule endoscopy was superior to that of enteroclysis and push-enteroscopy. The disadvantages and limitations of this diagnostic modality, such as inablility to control the capsule, the random nature of the images, and the lack of a facility for sampling, became increasingly recognized as growing numbers of numbers of patients with different indications were examinied using the technique, and these became the major negative factors in terms of positive diagnostic rates and accuracy. The overall diagnostic yield of capsule endoscopy reached levels of to 45 % - 75 %, but accuracy rates were only 23 % - 45 % [7] [8]. Other studies showed that the negative rates of capsule endoscopy could be high as 40 % - 60 % in patients with obscure gastrointestinal bleeding [9] [10]. In many studies, capsule endoscopy was found to be most suitable for the diagnosis of small-bowel diseases with diffuse or multiple-segment involvement [11]. The high cost of capsule endoscopy in China precludes its use as a first-line diagnostic modality for small-bowel disease, or as a “screening” test prior to DBE.

The double-balloon endoscope, which could be introduced deep into the small bowel, was regarded as a revolutionary development for the diagnosis of small-bowel diseases. The entire small intestine could be visualized, usually with a combination of antegrade and retrograde approaches. The extent of the bowel that could be examined by DBE was much greater than was possible by push-enteroscopy. The advantages of DBE, such as the steerability of the endoscope, the clear picture, and the ability to perform endoscopic biopsy, made it possible to achieve higher diagnostic yields and accuracy in comparison with other diagnostic modalities [12]. Large-channel prototypes allowed several endoscopic therapies, such as polypectomy, balloon dilation, and APC treatment, to be performed. DBE could be used as a gold standard diagnostic modality, together with intraoperative endoscopy.

The indication for DBE was found to have a substantial influence on its results. In studies conducted by Yamamoto et al. [6] and May et al. [12], the main indications were obscure small-bowel bleeding and obstruction. The overall diagnostic yields reached 76 % - 80 % in the Yamamoto et al. study and 74 % in the May et al. study. There were fewer patients with abdominal pain and diarrhea in their studies. In our retrospective study, the diagnostic yields were 80.6 % (154/191) for obscure gastrointestinal bleeding and 81.3 % (39/48) for obstruction. Patients with unknown causes of abdominal pain and diarrhea were referred for DBE examination after previous diagnostic modalities had been negative. The diagnostic yield for these two indications only reached 37.7 % (26/69) for abdominal pain and 36.5 % (23/63) for diarrhea, even though our exclusion criteria meant that some common conditions, such as irritable bowel disease, had already been ruled out. The causes of these low rates of positive findings in patients with these indications might have included the presence of various underlying diseases without the small intestine, atypical presentation of irritable bowel syndrome, or symptoms caused by some functional disorders. In some of these patients, therefore, DBE served only as an exclusive examination.

Theoretically, all patients need dual-approach DBE, for the same reason as in colonoscopy, that a finding of one polyp, adenoma, or tumor does not guarantee that there are no more lesions in the remaining bowel. However, in clinical practice, with the limitations of the high cost, the relatively long procedure time, and the low tolerablility, we usually stop once we have identified definite findings or suspicious findings. We only perform another DBE procedure using the second route in patients who have negative findings on the first procedure but who have alarming symptoms, especially in cases of obscure gastrointestinal bleeding. We also performed DBE via both routes in patients with abdominal pain or diarrhea if the patient insisted on this. Total enteroscopy was therefore only carried out in a limited number of cases. The DBE was usually performed via one route and was continued as far as possible. The most common disease diagnosed by DBE in these two groups (abdominal pain, diarrhea) was Crohn’s disease. In the 6-month follow-up period, among the 83 patients with negative findings on DBE, only six patients experienced worsening of their symptoms, and four of these had a definite diagnosis made after re-examinations and received appropriate treatment. Based on the results of DBE performed in patients with abdominal pain and diarrhea as the principal symptom and on follow-up examinations, we could conclude that DBE does not appear to be suitable as a routine diagnostic tool for detecting the causes of abdominal pain and diarrhea, and that it was also not useful as a first-line or exclusive modality for investigating small-bowel disease in these patients. It seemed necessary to perform pre-DBE investigations, such as enteroclysis, small-bowel CT scanning, or even capsule endoscopy in order to obtain even suggestive findings.

With its capabilities of direct observation and biopsy of lesions, DBE was regarded as a reliable diagnostic tool for small-bowel lesions. The accuracy and reliability of DBE could be assessed in patients with obscure gastrointestinal bleeding who had a confirmed diagnosis made by DBE and received specific treatments: the average (± SD) scoring dropped from 6.8 ± 2.2 to 1.5 ± 0.5 in patients who received specific treatments. In the patients who received symptomatic treatment only or no treatment, the average score decreased to 3.6 ± 0.7 and 3.9 ± 0.9, respectively (i. e. a score in-between the baseline and specific treatment scores). The reasons for this partial dropping of scores included: the inclusion of some patients with non-small-bowel bleeding, partial improvement in symptoms after symptomatic treatment, and examination of patients during nonbleeding periods. Six patients had their diagnosis confirmed after relevant examinations performed because their symptoms relapsed during the follow-up period; the bleeding severity scores of five of these patients dropped dramatically after the institution of specific treatments. These results suggest that the accuracy of DBE played an important role in the determination of subsequent treatment and prognosis. It was also critical to target the source of possible bleeding in patients with gastrointestinal haemorrhage. In our experience, emergency gastroscopy (within 12 - 24 hours) and pancolonoscopy (within 24 - 48 hours) should be completed by experienced endoscopists before a small-bowel origin for the bleeding is suspected.

The implications of the negative findings on DBE were quite complicated. These could have arisen because the original lesions were located in the upper gastrointestinal tract or colon but were missed by the previous gastroscopy or pancolonoscopy, or because of features of particular conditions, such as a nonbleeding phase of an angiodysplasia, where DBE would not be able to confirm whether or not it was the real cause of the bleeding. Some lesions might be missed as a result of incomplete examination of the whole small bowel, even when DBE was performed via both routes. It therefore seemed necessary to scrutinize the entire small intestine in patients with alarming symptoms, such as definite small-bowel bleeding or obstruction. It was advisable to ensure close observation and follow-up in patients without any positive findings on the DBE examination, helpful for further assessment of potential causes of the symptoms and for selection of further diagnostic tests. In our study, 54/131 patients with initial negative findings on DBE experienced relapse of their symptoms. DBE or other diagnostic tests were performed, and positive findings were then detected in 14 patients (26 %), 11 of whom subsequently underwent specific treatments.

The determination of treatment and the impact on the prognosis were largely dependent on the results of the examination. In a comparative study of the effect of capsule endoscopy and push-enteroscopy on the clinical outcome during a 1-year follow-up period conducted by Saurin et al. [13], capsule endoscopy had a higher sensitivity rate (95 %) for the detection of small-bowel lesions and a lower specificity rate (48 %) than push-enteroscopy, and the results of capsule endocopy had a substantial influence on the subsequent managements [13]. DBE is too new an application to have influenced data on the effect of enteroscopy on clinical outcomes. In the present study, however, 208/247 DBE-examined patients with definite findings underwent specific treatment, the diseases were cured or the symptoms were markedly improved after these treatments in 190 patients, and the total effective treatment rate was 76.9 %. The ten patients who were re-examined by DBE during the 6 months of follow-up because of symptomatic relapse finally had a diagnosis confirmed. DBE, with its capability of direct observation of suspected lesions, its facility for biopsy and the introduction of some accessories (e. g. ultrasonography), undoubtedly had a higher diagnostic yield and accuracy than other diagnostic modalities, and correct and confirmatory findings were fundamental for further clinical management. Another advantage of DBE was that endoscopic interventions could be performed during the operation. Some of the interventions comprised the main target therapy and were extremely important with regard to the prognosis of some diseases, such as multiple bleeding angiodysplasias or polyps. DBE was therefore not only a modality with a high diagnostic capability, but a valuable therapeutic tool [14].

In conclusion, DBE was demonstrated to be a very important diagnostic modality for small-bowel disease, and was the most direct and accurate method for investigating mucosal and submucosal lesions in the small intestine. The selection of suitable indications and timing for the procedure, and the extent of the examination were important influential factors on the diagnostic yield. The use of screening examinations which could yield some suggestive findings before DBE might increase the positive finding and success rates. The results of the DBE examination played a decisive role in determination of subsequent management. The patients with a diagnosis confirmed by DBE usually obtained better results after specific treatment. Further diagnostic analysis and close follow-up for at least 6 months can be beneficial in patients with negative findings in the initial DBE work-up.

Competing interests: None

References

• 1 Mylonaki M, Fritscher-Ravens A, Swain P. Wireless capsule endoscopy: a comparison with push enteroscopy in patients with gastroscopy and colonoscopy negative gastrointestinal bleeding.  Gut. 2003;  52 1122-1126
  CrossrefPubMedSearch in Google Scholar
• 2 Saurin J C, Delvaux M, Vahedi K. et al . Clinical impact of capsule endoscopy compared to push enteroscopy: 1-year follow-up study.  Endoscopy. 2005;  37 318-323
  Thieme ConnectPubMedSearch in Google Scholar
• 3 May A, Nachbar L, Wardak A. et al . Double-balloon enteroscopy: preliminary experience in patients with obscure gastrointestinal bleeding or chronic abdominal pain.  Endoscopy. 2003;  35 985-991
  Thieme ConnectPubMedSearch in Google Scholar
• 4 Yamamoto H, Yano T, Kita H. et al . New system of double-balloon enteroscopy for diagnosis and treatment of small-intestinal disorders.  Gastroenterology. 2003;  125 1556-1557
  PubMedSearch in Google Scholar
• 5 Yamamoto H, Sugano K. A new method of enteroscopy: the double balloon method.  Can J Gastroenterol. 2003;  17 273-274
  PubMedSearch in Google Scholar
• 6 Yamamoto H, Kita H, Sunada K. et al . Clinical outcomes of double-balloon endoscopy for the diagnosis and treatment of small-intestinal diseases.  Clin Gastroenterol Hepatol. 2004;  2 1010-1016
  CrossrefPubMedSearch in Google Scholar
• 7 Alan L B, Anita W. Videocapsule endoscopy renders obscure gastrointestinal bleeding no longer obscure.  J Clin Gastroenterol. 2003;  37 303-306
  PubMedSearch in Google Scholar
• 8 Marco P, Renato S, Emanuele R. et al . Outcome of patients with obscure gastrointestinal bleeding after capsule endoscopy: report of 100 consecutive cases.  Gastroenterology. 2004;  126 643-653
  CrossrefPubMedSearch in Google Scholar
• 9 Neu B, Ell C, May A. et al . Capsule endoscopy versus standard tests in influencing management of obscure digestive bleeding: results from a German multicenter trial.  Am J Gastroenterology. 2005;  100 1736-1742
  CrossrefPubMedSearch in Google Scholar
• 10 Magnano A, Privitera A, Calogero G. et al . The role of capsule endoscopy in the work-up of obscure gastrointestinal bleeding.  Eur J Gastroenterol Hepatol. 2004;  16 403-406
  PubMedSearch in Google Scholar
• 11 Ell C, May A. Capsule status 2004: what is the outcome in bleeding? Are there really additional indications?.  Endoscopy. 2004;  36 1107-1108
  Thieme ConnectPubMedSearch in Google Scholar
• 12 May A, Nachbar L, Ell C. Double-balloon enteroscopy (push-and-pull enteroscopy) of the small bowel: feasibility and diagnostic and therapeutic yield in patients with suspected small bowel disease.  Gastrointest Endosc. 2005;  62 62-70
  CrossrefPubMedSearch in Google Scholar
• 13 Saurin J C, Delvaux M, Gaudin J L. Diagnostic value of endoscopic capsule in patients with obscure digestive bleeding: blinded comparison with video push-enteroscopy.  Endoscopy. 2003;  35 576-584
  Search in Google Scholar
• 14 Kaffes A J, Koo J H, Meredith C. Double-balloon enteroscopy in the diagnosis and the management of small-bowel disease: an initial experience in 40 patients.  Gastrointest Endosc. 2006;  63 81-86
  CrossrefPubMedSearch in Google Scholar

T. Ma, MD

Department of Gastroenterology
Rui Jin Hospital
Shanghai Jiao Tong University

No.197 Rui Jin Er Rd
Shanghai 200025
China

Fax: +86-21-64315951

Email: xmzxmz@gmail.com

References

• 1 Mylonaki M, Fritscher-Ravens A, Swain P. Wireless capsule endoscopy: a comparison with push enteroscopy in patients with gastroscopy and colonoscopy negative gastrointestinal bleeding.  Gut. 2003;  52 1122-1126
  CrossrefPubMedSearch in Google Scholar
• 2 Saurin J C, Delvaux M, Vahedi K. et al . Clinical impact of capsule endoscopy compared to push enteroscopy: 1-year follow-up study.  Endoscopy. 2005;  37 318-323
  Thieme ConnectPubMedSearch in Google Scholar
• 3 May A, Nachbar L, Wardak A. et al . Double-balloon enteroscopy: preliminary experience in patients with obscure gastrointestinal bleeding or chronic abdominal pain.  Endoscopy. 2003;  35 985-991
  Thieme ConnectPubMedSearch in Google Scholar
• 4 Yamamoto H, Yano T, Kita H. et al . New system of double-balloon enteroscopy for diagnosis and treatment of small-intestinal disorders.  Gastroenterology. 2003;  125 1556-1557
  PubMedSearch in Google Scholar
• 5 Yamamoto H, Sugano K. A new method of enteroscopy: the double balloon method.  Can J Gastroenterol. 2003;  17 273-274
  PubMedSearch in Google Scholar
• 6 Yamamoto H, Kita H, Sunada K. et al . Clinical outcomes of double-balloon endoscopy for the diagnosis and treatment of small-intestinal diseases.  Clin Gastroenterol Hepatol. 2004;  2 1010-1016
  CrossrefPubMedSearch in Google Scholar
• 7 Alan L B, Anita W. Videocapsule endoscopy renders obscure gastrointestinal bleeding no longer obscure.  J Clin Gastroenterol. 2003;  37 303-306
  PubMedSearch in Google Scholar
• 8 Marco P, Renato S, Emanuele R. et al . Outcome of patients with obscure gastrointestinal bleeding after capsule endoscopy: report of 100 consecutive cases.  Gastroenterology. 2004;  126 643-653
  CrossrefPubMedSearch in Google Scholar
• 9 Neu B, Ell C, May A. et al . Capsule endoscopy versus standard tests in influencing management of obscure digestive bleeding: results from a German multicenter trial.  Am J Gastroenterology. 2005;  100 1736-1742
  CrossrefPubMedSearch in Google Scholar
• 10 Magnano A, Privitera A, Calogero G. et al . The role of capsule endoscopy in the work-up of obscure gastrointestinal bleeding.  Eur J Gastroenterol Hepatol. 2004;  16 403-406
  PubMedSearch in Google Scholar
• 11 Ell C, May A. Capsule status 2004: what is the outcome in bleeding? Are there really additional indications?.  Endoscopy. 2004;  36 1107-1108
  Thieme ConnectPubMedSearch in Google Scholar
• 12 May A, Nachbar L, Ell C. Double-balloon enteroscopy (push-and-pull enteroscopy) of the small bowel: feasibility and diagnostic and therapeutic yield in patients with suspected small bowel disease.  Gastrointest Endosc. 2005;  62 62-70
  CrossrefPubMedSearch in Google Scholar
• 13 Saurin J C, Delvaux M, Gaudin J L. Diagnostic value of endoscopic capsule in patients with obscure digestive bleeding: blinded comparison with video push-enteroscopy.  Endoscopy. 2003;  35 576-584
  Search in Google Scholar
• 14 Kaffes A J, Koo J H, Meredith C. Double-balloon enteroscopy in the diagnosis and the management of small-bowel disease: an initial experience in 40 patients.  Gastrointest Endosc. 2006;  63 81-86
  CrossrefPubMedSearch in Google Scholar

T. Ma, MD

Department of Gastroenterology
Rui Jin Hospital
Shanghai Jiao Tong University

No.197 Rui Jin Er Rd
Shanghai 200025
China

Fax: +86-21-64315951

Email: xmzxmz@gmail.com