The Rate of Lesions Found within Reach of Esophagogastroduodenoscopy during Push Enteroscopy Depends on the Type of Obscure Gastrointestinal Bleeding

• Introduction
• Patients and Methods
• Outcome Definitions
• Results
• Discussion
• Acknowledgment
• References

Background and Study Aims: Many lesions found during push enteroscopy to evaluate obscure gastrointestinal bleeding are within the reach of standard endoscopes. The aim of this study was to determine whether the rate of proximal lesions varies in relation to the type of obscure bleeding that is present.
Patients and Methods: A retrospective review of consecutive push enteroscopies carried out for obscure gastrointestinal bleeding between July 1996 and July 2000 was conducted. The patients were categorized into three groups: those with recurrent obscure/overt gastrointestinal bleeding; those with persistent obscure/overt gastrointestinal bleeding; and those with obscure/occult gastrointestinal bleeding.
Results: A total of 63 patients (24 men, 39 women; mean age 69.8) were included. Push enteroscopy examinations were conducted for recurrent obscure/overt bleeding in 32 patients; for persistent obscure/overt bleeding in 12 patients; and for obscure/occult bleeding in 19 patients. The overall diagnostic yield of push enteroscopy was 47 % (15 of 32) in the group with recurrent obscure/overt bleeding; 66 % (eight of 12) in the group with persistent obscure/overt bleeding; and 63 % (12 of 19) in the group with obscure/occult bleeding. However, when lesions within the reach of standard esophagogastroduodenoscopy (EGD) were excluded, the yield of push enteroscopy was slightly higher in the group with recurrent obscure/overt bleeding (41 %) than in the groups with persistent obscure/overt bleeding (33 %) and obscure/occult bleeding (26 %). There were fewer lesions within the reach of EGD in the group with recurrent obscure/overt bleeding than in the groups with persistent obscure/overt bleeding (6 % vs. 33 %; P < 0.05) or obscure/occult bleeding (6 % vs. 37 %; P < 0.05).
Conclusions: Patients undergoing push enteroscopy for recurrent obscure/overt bleeding were significantly less likely to have lesions within the reach of EGD than patients with persistent obscure/overt bleeding or obscure/occult bleeding. Patients in the latter two groups would be able to undergo a repeat EGD examination before more intense evaluation with push enteroscopy or capsule endoscopy.

Introduction

The two most commonly used endoscopic procedures for evaluating the gastrointestinal tract are esophagogastroduodenoscopy (EGD) and colonoscopy. The former is limited to the areas proximal to the ampullary region, and the latter to the distal terminal ileum. Some 10 - 20 % of patients who present with an initial gastrointestinal hemorrhage remain without a diagnosis, despite conventional endoscopic and radiographic procedures, but only 1 - 6 % suffer from recurrent bleeding. Small-bowel lesions, mostly angiectasia, are often the cause of obscure bleeding [1] [2] [3] [4] [5]. Endoscopic methods of evaluating the small bowel include sonde enteroscopy, intraoperative enteroscopy, and push enteroscopy; the latter is the method that is most often used [1] [6] [7]. Capsule endoscopy is a promising new method of evaluating the small intestine, and its role in the evaluation of obscure gastrointestinal bleeding is still being defined [8] [9].

Push enteroscopy is an extension of EGD in which the endoscope is advanced beyond the ligament of Treitz into the proximal small bowel; the technique can be easily learned and mastered by endoscopists [4] [10] [11]. The yield of push enteroscopy varies widely, with rates reported in the range of 17 - 75 % and the highest yield in patients with active bleeding. However, 20 - 75 % of lesions found during push enteroscopy are located within the reach of EGD and are presumed to have been previously missed [1] [5] [6] [12] [13]. Inconsistencies in the literature regarding the classification of gastrointestinal bleeding, indications for push enteroscopy, and reporting of the yield of push enteroscopy make it difficult to extrapolate implications for clinical practice from the results of push enteroscopy.

The primary aim of this study was to evaluate whether the rate of proximal lesions (located within the reach of EGD) detected during push enteroscopy varied relative to the type of obscure gastrointestinal bleeding. A secondary aim was to determine the yield of push enteroscopy in this group of patients.

Patients and Methods

The endoscopy database at our institution was searched to identify consecutive push enteroscopies carried out between 1 July 1996 and 31 July 2000 at Wake Forest University Baptist Medical Center by a single endoscopist (B.C.P.). Patients who underwent push enteroscopy to evaluate gastrointestinal bleeding were included. Electronic and printed medical records were retrospectively reviewed to extract information using a standardized method. The medical history, laboratory results, indications for enteroscopy, and results of enteroscopy were recorded.

The patients were classified into three groups according to definitions established by the American Gastroenterological Association [11]. Group 1, with recurrent obscure/overt gastrointestinal bleeding, consisted of patients with visible gastrointestinal bleeding manifested by melena or hematochezia that recurred intermittently after at least one negative EGD and colonoscopy. Group 2, with persistent obscure/overt gastrointestinal bleeding, consisted of patients who were admitted with visible bleeding that persisted during the hospitalization period after a negative EGD and colonoscopy. Group 3, with obscure/occult gastrointestinal bleeding, consisted of patients with unexplained positive fecal blood tests and/or persistent iron-deficiency anemia and at least one negative EGD and colonoscopy.

Push enteroscopy was preferentially carried out using the Olympus SIF-100 dedicated video enteroscope (Olympus, Inc., Aizu, Japan) with an overtube under fluoroscopic guidance, as previously described [4]. Briefly, the enteroscope, lubricated with silicone, was preloaded into the overtube and advanced into the distal duodenum. With the tip of the endoscope anchored in the duodenum, the overtube was telescoped over the enteroscope under fluoroscopic guidance to the antrum or duodenum at the same time as the enteroscope was reduced. The enteroscope was then advanced beyond the ligament of Treitz. The bowel was examined during insertion, and examined more closely during withdrawal after the administration of intravenous glucagon. A pediatric colonoscope was used in one patient in the group with persistent obscure/overt bleeding and in two patients in the group with recurrent obscure/overt bleeding. Lesions were counted once. For example, a patient who had gastric and duodenal angiectasia was not counted as having two lesions. The study was approved by the institutional review board at Wake Forest University Baptist Medical Center.

Outcome Definitions

The overall yield of push enteroscopy was defined as the discovery of a lesion anywhere in the gastrointestinal tract that could account for blood loss on a per-patient basis - i. e., multiple lesions within a patient counted only once.

The true yield of push enteroscopy was defined as the discovery of any lesion in the evaluated portion of the gastrointestinal tract beyond the reach of EGD, distal to the ampullary region, that could account for blood loss on a per-patient basis. When calculating the true yield of push enteroscopy, lesions proximal to the ampullary region were counted as having been missed in previous EGD procedures.

Statistical analysis. Differences between independent samples following a normal binomial distribution were analyzed using Fisher’s exact test. Differences between means for continuous data were calculated using Student’s t-test for unpaired data. A P value below 0.05 was considered significant.

Results

A total of 74 patients underwent enteroscopy during the study period. Eleven patients were excluded, as the enteroscopy procedures were carried out for reasons other than bleeding (abnormal radiographic findings and polyp surveillance in familial adenomatous polyposis). The remaining 63 patients underwent a total of 63 push enteroscopies; their mean age was 69.8 years (range 28 - 98) and 62 % were women. Fifty-seven percent of the procedures were carried out on an outpatient basis. The patients’ characteristics are listed in Table [1].

Details of the diagnostic tests conducted before push enteroscopy are given in Table [2]. Patients in the group with persistent obscure/overt bleeding were more likely to have undergone a radiographic procedure. The 12 patients with persistent obscure/overt bleeding had undergone 15 radiographic procedures, including upper gastrointestinal and small-bowel follow-through barium studies, enteroclysis, computed tomography (CT), tagged red blood cell scanning, and angiography. By contrast, the 32 patients in the group with recurrent obscure/overt bleeding underwent 25 radiographic procedures and the 19 patients in the group with obscure/occult bleeding underwent nine radiographic procedures. There was a higher number of endoscopic procedures (EGD and colonoscopy) before push enteroscopy in the group with recurrent obscure/overt bleeding (average 2.8 endoscopies per patient), compared with 2.4 in the group with obscure/occult bleeding and 2.3 in the group with persistent obscure/overt bleeding (not significant).

The push enteroscope was successfully passed beyond the ligament of Treitz in all patients, and there were no complications associated with the procedure. The overall yield of push enteroscopy - i. e., the presence of any lesion that could account for blood loss - was 47 % (15 of 32 patients) in the group with recurrent obscure/overt bleeding; 66 % (eight of 12 patients) in the group with persistent obscure/overt bleeding; and 63 % (12 of 19 patients) in the group with obscure/occult bleeding. No patients were found who had two different lesions that could account for bleeding (Table [3]).

In the group with recurrent obscure/overt bleeding, proximal lesions were identified in 6 % of cases (two of the 32 patients) - a gastric ulcer in one patient and esophageal varices in another. In the group with persistent obscure/overt bleeding, proximal lesions were identified in 33 % of cases (four of the 12 patients); these included esophageal varices requiring variceal ligation, a gastric ulcer, a duodenal ulcer, and a friable gastric remnant. Seven of the 19 patients (37 %) in the group with obscure/occult bleeding had lesions proximal to the ampulla - two patients with gastric angiectasia, two with Cameron’s erosions, and the remainder with gastric antral vascular ectasia, erosive esophagitis, and duodenal ulcers, respectively.

In patients in whom a lesion was found, the number of proximal lesions was not significantly higher in the group with persistent obscure/overt bleeding (four of eight patients, 50 %) or the group with obscure/occult bleeding (seven of 12 patients, 58 %) in comparison with the group with recurrent obscure/overt bleeding (two of 15, 26 %; not significant). When the total number of push enteroscopies was considered, finding a proximal lesion within the reach of EGD occurred significantly less often in patients with recurrent obscure/overt bleeding in comparison with patients with persistent obscure/overt bleeding (6 % vs. 33 %; P < 0.05) or obscure/occult bleeding (6 % vs. 37 %; P < 0.005) (Table [3]).

After proximal lesions had been excluded, the true yield of push enteroscopy was 41 % (13 of the 32 patients) in the group with recurrent obscure/overt bleeding, 33 % (four of the 12 patients) in the group with persistent obscure/overt bleeding, and 26 % (five of the 19 patients) in the group with obscure/occult bleeding (not significant). Angiectasia was the most frequent cause of gastrointestinal bleeding distal to the ampulla, found in 34 % (11 of the 32 patients) in the group with recurrent obscure/overt bleeding, 33 % (four of the 12 patients) in the group with persistent obscure/overt bleeding, and 21 % (four of the 19 patients) in the group with obscure/occult bleeding. All angiectasias were treated with electrocoagulation. One patient with Rendu-Osler-Weber syndrome (hereditary hemorrhagic telangiectasia) and persistent obscure/overt bleeding died in hospital due to massive bleeding. Other diagnoses included an actively bleeding aortoenteric fistula, a distal duodenal hemorrhagic lipoma in the group with recurrent obscure/overt bleeding, and a jejunal adenocarcinoma in the group with obscure/occult bleeding.

Two lesions were missed on push enteroscopy. In the group with recurrent obscure/overt bleeding, duodenal angiectasias were diagnosed and treated in one patient during a repeat EGD, and in the group with persistent obscure/overt bleeding, a lesion was noted during an enteroclysis after push enteroscopy, which was diagnosed during laparotomy as a jejunal melanoma recurrence after 20 years of remission. There were no known missed lesions in the group with obscure/occult bleeding.

Discussion

In the literature, liberal use of the definitions of ”yield” for each method, the lack of a standardized classification for gastrointestinal bleeding, and a failure to differentiate clearly between occult, persistent, and recurrent bleeding have made it difficult to evaluate obscure gastrointestinal bleeding after negative upper and lower endoscopies. The few randomized trials conducted on this topic have failed to include a group of asymptomatic persons without evidence of obscure bleeding, in order to determine the frequency of lesions that may ultimately have no clinical relevance.

Evaluating and treating the distal small bowel in patients with obscure gastrointestinal bleeding is still a challenge. Endoscopic methods of evaluating the small bowel include sonde enteroscopy, intraoperative enteroscopy, push enteroscopy, and - more recently - capsule endoscopy. Since sonde enteroscopy does not allow simultaneous treatment, is time-consuming for the patient and physician, and provides only suboptimal visualization of the mucosa, it is an unpopular modality for evaluating obscure bleeding [4] [8] [14] [15] [16]. Although intraoperative enteroscopy has a high diagnostic yield, its use is limited by the invasiveness of the procedure [6] [8] [15] [17]. Capsule endoscopy is an effective new diagnostic modality that allows visualization of the majority of the small-bowel mucosa [10] [14] [18] [19] [20]. Higher diagnostic yields with capsule endoscopy in comparison with push enteroscopy have been reported, but overinterpretation of subtle findings may play a role [8] [9] [21] [22] [23] [24] [25]. Although capsule endoscopy has a clear role in the evaluation of patients with obscure bleeding, its place in the diagnostic algorithm has yet to be defined.

Push enteroscopy is the only method that allows nonsurgical treatment of proximal jejunal bleeding, but it is still ineffective for evaluating the distal small bowel [1] [2] [3] [6] [7] [15]. Although using an overtube may increase the depth of insertion, it is not clear whether this affects the diagnostic yield [4] [26] [27]. Push enteroscopy identifies a source of bleeding after negative upper and lower endoscopies in 17 - 75 % of patients, with the highest yield in patients with active bleeding. Lower diagnostic yields are reported when the procedure is carried out for indications such as the evaluation of abnormal radiographic imaging or abdominal pain [2] [5] [6] [14]. The definition of yield in the literature is often inconsistent. With as many as 20 - 75 % of lesions located proximal to the ampullary region, several studies that include these in the calculation of the yield may overestimate the true yield [2] [5] [10] [14]. Zaman et al. reported a significant drop in the yield of push enteroscopy when proximal lesions that could, or should, have been seen during conventional endoscopy were excluded in patients with obscure bleeding [10].

The aim of the present study was to determine whether the rate of proximal lesions varied in three clinically relevant groups of patients with obscure gastrointestinal bleeding. The overall yield was in the higher range of the results reported in the literature - 47 % in the group with recurrent obscure/overt bleeding to 66 % in the group with persistent obscure/overt bleeding. However, the actual or true yield of push enteroscopy, a more accurate representation of push enteroscopy, was between 26 % in the group with obscure/occult bleeding and 41 % in the group with recurrent obscure/overt bleeding.

Interestingly, a difference was found between the groups with regard to the number of proximal lesions. A proximal lesion within the reach of an EGD was significantly less likely to be present in patients who had recurrent obscure/overt bleeding in comparison with patients with persistent obscure/overt or obscure/occult bleeding. Patients with recurrent obscure/overt bleeding may not need a repeat EGD and could proceed to push enteroscopy or capsule endoscopy, in contrast to those with persistent obscure/overt bleeding or obscure/occult bleeding, who may benefit from a repeat EGD before having a more advanced evaluation. This underscores the importance of classifying patients into clinically relevant groups in future studies. The use of a standard definition of gastrointestinal bleeding, as suggested by the American Gastroenterological Association, will allow a better understanding of the accuracy of any particular diagnostic modality [11].

Overall, angiectasias are the most common finding in patients with obscure gastrointestinal bleeding, but small-bowel tumors are more common in patients under the age of 50 [4] [6] [10] [13] [28] [29]. This was confirmed in the present study, as angiectasias were diagnosed in 50 % of cases in the group with persistent obscure/overt bleeding and 73 % of those in the group with recurrent obscure/overt bleeding when a lesion was found during push enteroscopy. There were two small-bowel tumors in this study, both in patients under the age of 50: a jejunal adenocarcinoma in a 40-year-old man in the obscure/occult bleeding group and a bleeding lipoma in a 47-year-old man in the recurrent obscure/overt bleeding group. Due to the lack of a gold standard, the sensitivity of push enteroscopy has not been well defined. In the present study, two lesions were counted as having been missed by push enteroscopy. An abnormal enteroclysis carried out after push enteroscopy identified a jejunal lesion, which was diagnosed as a melanoma recurrence during subsequent laparotomy in a patient with persistent obscure/overt bleeding. This was considered as a missed push enteroscopy lesion, since it was in the jejunum, although it is possible that the lesion may have been beyond the reach of the push enteroscope. Duodenal angiectasias were treated during a subsequent EGD in a patient with recurrent obscure/overt bleeding. This emphasizes the need for a multimodal diagnostic approach and perseverance in patients with obscure gastrointestinal bleeding.

This study is limited by its retrospective nature, which probably underestimates the actual number of diagnostic evaluations before patients undergo push enteroscopy, but all of the patients had at least one EGD and colonoscopy before push enteroscopy and the majority had at least one radiographic study. Although unlikely, it is possible that some lesions were not missed but developed during the interval between the initial endoscopic evaluation and push enteroscopy. The time lapse was only a few days in the group with persistent obscure/overt bleeding, as they had acute and ongoing bleeding. It is possible that the lesions missed in this group during the initial endoscopy may have been due to active bleeding that obscured the lesion, or due to the potentially transient behavior of angiectasias [13] [30]. Estimating the time interval between EGD and push enteroscopy in the other two groups was not possible, as the endoscopy unit is an open-access one, so that some of these patients were referred to the institution specifically for push enteroscopy and then returned to their primary-care physician. Long-term follow-up data to determine the success of the interventions are consequently not available. Even so, the high number of proximal lesions within reach of an EGD found during push enteroscopy supports the recommendation that an EGD should be repeated in patients with obscure gastrointestinal bleeding, especially in the subgroup with persistent obscure/overt bleeding or obscure/occult bleeding.

An appropriate and cost-effective diagnostic algorithm for patients with obscure gastrointestinal hemorrhage needs to be better defined and should take into account whether the patient has recurrent obscure/overt, persistent obscure/overt, or obscure/occult bleeding. The role of capsule endoscopy in the algorithm remains to be defined, but it will probably remain closely related to push enteroscopy, as the capsule may be able to identify a lesion that could be treated during push enteroscopy. Repeating an EGD followed by capsule endoscopy, when available, may be the next-best step in evaluating obscure gastrointestinal bleeding before push enteroscopy. This may reduce the risk of interpreting mucosal artifacts provoked by push enteroscopy as a potential cause of gastrointestinal hemorrhage [25].

In summary, the rate of proximal lesions found during push enteroscopy for the evaluation of obscure gastrointestinal bleeding is higher in the patients with persistent obscure/overt bleeding and obscure/occult bleeding than in those with recurrent obscure/overt bleeding. This suggests that patients in the former two groups should undergo a repeat EGD before advancing to a more complex and potentially costly evaluation with push enteroscopy or capsule endoscopy. The actual diagnostic yield of push enteroscopy decreases when proximal lesions are excluded. This is a more accurate representation of the yield of the procedure. The true yield of diagnostic evaluations and a standardized classification of gastrointestinal bleeding should be reported in all studies comparing diagnostic modalities, including capsule endoscopy, in patients with obscure gastrointestinal bleeding, to allow a better understanding of the applicability of the diagnostic modality and for better cross-comparison of results.

Acknowledgment

Research for this study was previously presented in a poster session at the annual American College of Gastroenterology (ACG) meeting held in Seattle in October 2002.

References

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B. C. Pineau, M. D., M. Sc. (Epid.)

Digestive Health Center, Wake Forest University Health Sciences

Medical Center Boulevard · Winston-Salem, NC 27157 · USA

Fax: +1-336-716-6376

Email: bpineau@wfubmc.edu

References

• 1 Sharma B C, Bhasin D K, Makharia G. et al . Diagnostic value of push-type enteroscopy: a report from India.  Am J Gastroenterol. 2000;  95 137-140
  CrossrefPubMedSearch in Google Scholar
• 2 Landi B, Tkoub M, Gaudric M. et al . Diagnostic yield of push-type enteroscopy in relation to indication.  Gut. 1998;  42 421-425
  PubMedSearch in Google Scholar
• 3 Vakil N, Huilgol V, Khan I. Effect of push enteroscopy on transfusion requirements and quality of life in patients with unexplained gastrointestinal bleeding.  Am J Gastroenterol. 1997;  92 425-428
  PubMedSearch in Google Scholar
• 4 Adrain A L, Krevsky B. Enteroscopy in patients with gastrointestinal bleeding of obscure origin.  Dig Dis. 1996;  14 345-355
  CrossrefPubMedSearch in Google Scholar
• 5 Davies G R, Benson M J, Gertner D J. et al . Diagnostic and therapeutic push type enteroscopy in clinical use.  Gut. 1995;  37 346-352
  PubMedSearch in Google Scholar
• 6 Chak A, Koehler M K, Sundaram S N. et al . Diagnostic and therapeutic impact of push enteroscopy: analysis of factors associated with positive findings.  Gastrointest Endosc. 1998;  47 18-22
  CrossrefPubMedSearch in Google Scholar
• 7 Zwas F R, Bonheim N A, Berken C A, Gray S. Diagnostic yield of routine ileoscopy.  Am J Gastroenterol. 1995;  90 1441-1443
  PubMedSearch in Google Scholar
• 8 Appleyard M, Fireman Z, Glukhovsky A. et al . A randomized trial comparing wireless capsule endoscopy with push enteroscopy for the detection of small-bowel lesions.  Gastroenterology. 2000;  119 1431-1438
  CrossrefPubMedSearch in Google Scholar
• 9 Lewis B S, Swain P. Capsule endoscopy in the evaluation of patients with suspected small intestinal bleeding: results of a pilot study.  Gastrointest Endosc. 2002;  56 349-353
  Search in Google Scholar
• 10 Zaman A, Katon R M. Push enteroscopy for obscure gastrointestinal bleeding yields a high incidence of proximal lesions within reach of a standard endoscope.  Gastrointest Endosc. 1998;  47 372-376
  PubMedSearch in Google Scholar
• 11 Zuckerman G R, Prakash C, Askin M P, Lewis B S. AGA technical review on the evaluation and management of occult and obscure gastrointestinal bleeding.  Gastroenterology. 2000;  118 201-221
  CrossrefPubMedSearch in Google Scholar
• 12 Lewis B S, Kornbluth A, Waye J D. Small bowel tumours: yield of enteroscopy.  Gut. 1991;  32 763-765
  CrossrefPubMedSearch in Google Scholar
• 13 Descamps C, Schmit A, Van Gossum A. ”Missed” upper gastrointestinal tract lesions may explain ”occult” bleeding.  Endoscopy. 1999;  31 452-455
  PubMedSearch in Google Scholar
• 14 Pennazio M, Arrigoni A, Risio M. et al . Clinical evaluation of push-type enteroscopy.  Endoscopy. 1995;  27 164-170
  PubMedSearch in Google Scholar
• 15 Lewis B S, Wenger J S, Waye J D. Small bowel enteroscopy and intraoperative enteroscopy for obscure gastrointestinal bleeding.  Am J Gastroenterol. 1991;  86 171-174
  PubMedSearch in Google Scholar
• 16 Waye J D. Small-intestinal endoscopy.  Endoscopy. 2001;  33 24-30
  Thieme ConnectPubMedSearch in Google Scholar
• 17 Bowden T A, Jr, Hooks V H III, Mansberger A R, Jr. Intraoperative gastrointestinal endoscopy in the management of occult gastrointestinal bleeding.  South Med J. 1979;  72 1532-1534
  PubMedSearch in Google Scholar
• 18 Schmit A, Gay F, Adler M. et al . Diagnostic efficacy of push-enteroscopy and long-term follow-up of patients with small bowel angiodysplasias.  Dig Dis Sci. 1996;  41 2348-2352
  PubMedSearch in Google Scholar
• 19 Rossini F P, Pennazio M. Small-bowel endoscopy.  Endoscopy. 2002;  34 13-20
  Thieme ConnectPubMedSearch in Google Scholar
• 20 Askin M P, Lewis B S. Push enteroscopic cauterization: long-term follow-up of 83 patients with bleeding small intestinal angiodysplasia.  Gastrointest Endosc. 1996;  43 580-583
  PubMedSearch in Google Scholar
• 21 Van Gossum A, Hittelet A, Schmit A. et al . A prospective comparative study of push and wireless-capsule enteroscopy in patients with obscure digestive bleeding.  Acta Gastroenterol Belg. 2003;  66 199-205
  PubMedSearch in Google Scholar
• 22 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
• 23 Hartmann D, Schilling D, Bolz G. et al . Capsule endoscopy versus push enteroscopy in patients with occult gastrointestinal bleeding.  Z Gastroenterol. 2003;  41 377-382
  Search in Google Scholar
• 24 Costamagna G, Shah S K, Riccioni M E. et al . A prospective trial comparing small bowel radiographs and video capsule endoscopy for suspected small bowel disease.  Gastroenterology. 2002;  123 999-1005
  CrossrefPubMedSearch in Google Scholar
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B. C. Pineau, M. D., M. Sc. (Epid.)

Digestive Health Center, Wake Forest University Health Sciences

Medical Center Boulevard · Winston-Salem, NC 27157 · USA

Fax: +1-336-716-6376

Email: bpineau@wfubmc.edu