Diagnostic and therapeutic yield is not influenced by the timing of small-bowel enteroscopy: morning versus afternoon

ORIGINAL ARTICLE: Clinical Endoscopy

Diagnostic and therapeutic yield is not influenced by the timing of small-bowel enteroscopy: morning versus afternoon Madhusudhan R. Sanaka, MD,1 Udayakumar Navaneethan, MD,1 Bennie R. Upchurch, MD,1 Rocio Lopez, MS,2 Sabrina Vannoy, LPN,1 Milan Dodig, MD,1 Janice M. Santisi, RN,1 John J. Vargo, MD1 Cleveland, Ohio, USA

Background: Small-bowel enteroscopies (BEs) are tedious and prolonged, and their efficacy may be affected by the timing of procedures. Objective: We aimed to evaluate the differences in diagnostic yield, insertion depth, procedure duration, therapeutic yield, and adverse events (AEs) of enteroscopies performed in the morning versus the afternoon. Design: Retrospective cohort study. Setting: Tertiary referral center. Patients: Patients who underwent BE for suspected small-bowel disease at a single institution between January 2008 and August 2009. Main Outcome Measurement: Differences in diagnostic yield, insertion depth, procedure duration, therapeutic yield, and AEs between morning (started before noon) and afternoon (after noon) procedures. Results: A total of 250 enteroscopies were performed on 250 patients, of which 125 patients (50%) underwent a procedure in the morning and 125 patients (50%) underwent the procedure in the afternoon. The diagnostic yield with anterograde enteroscopy was the same in both the morning and afternoon (63.7% and 63.7%, respectively; P ⫽ .99). The procedure durations were also similar (42.4 ⫾ 21.5 minutes vs 46.2 ⫾ 22.4 minutes, respectively; P ⫽ .25). Similarly the diagnostic yield with retrograde enteroscopy was similar in morning and afternoon (44.1% and 35.3%, respectively; P ⫽ .46). However, the procedure durations of retrograde BE were significantly shorter in the morning compared with the afternoon (51.3 ⫾ 21.3 minutes vs 66.6 ⫾ 32.9 minutes, respectively; P ⫽ .03). Therapeutic yield and AEs were similar. Limitations: Retrospective study. Conclusions: The timing of procedure, morning versus afternoon, did not affect the diagnostic and therapeutic efficacy of BE in patients with suspected small-bowel disease. (Gastrointest Endosc 2013;77:62-70.)

Studies on colonoscopy showed lower completion rates and adenoma detection rates in procedures performed in the afternoon compared with the morning.1-4 Fatigue and decreased concentration have been hypothesized as causes for these poorer outcomes in afternoon procedures.1-3 Small-bowel enteroscopy (BE) has revolu-

tionized the evaluation and management of small-bowel disease because of its dual diagnostic and therapeutic capabilities.5 Balloon-assisted enteroscopy is composed of double-balloon enteroscopy (DBE) and single-balloon enteroscopy (SBE). The third type of enteroscopy system is spiral enteroscopy (SE), which uses rotational force to

Abbreviations: APC, argon plasma coagulation; AE, adverse event; BE, small-bowel enteroscopy; DBE, double-balloon enteroscopy; SBE, singleballoon enteroscopy; SE, spiral enteroscopy.

Current affiliations: Departments of Gastroenterology (1) and Quantitative Sciences (2), Digestive Disease Institute, The Cleveland Clinic, Cleveland, Ohio, USA.

DISCLOSURE: The authors disclosed no financial relationships relevant to this publication.

Reprint requests: Madhusudhan R. Sanaka, MD, Digestive Disease Institute, Desk Q3, The Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, OH 44195.

Copyright © 2013 by the American Society for Gastrointestinal Endoscopy 0016-5107/$36.00 http://dx.doi.org/10.1016/j.gie.2012.08.032

If you would like to chat with an author of this article, you may contact Dr Sanaka at [email protected].

Received July 2, 2012. Accepted August 27, 2012.

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create linear insertion capability.6 Enteroscopy procedures are tedious and prolonged and could be tiring. Enteroscopy is also one of the highly operator-dependent procedures performed by gastroenterologists.7 We therefore hypothesized that physician fatigue, which increases as the day progresses, may decrease the efficacy of enteroscopies. The aims of this study were to evaluate the differences in efficacy of enteroscopies (both antegrade and retrograde) performed in the morning versus the afternoon in terms of diagnostic yield, insertion depth, procedure duration, therapeutic yield, and adverse events (AEs).

Enteroscopy and the small bowel

Take-home Message ●

●

The timing of procedures, AM versus PM, does not affect the diagnostic and therapeutic efficacy of small-bowel enteroscopy in patients with suspected small-bowel disease. Retrograde enteroscopies performed in the afternoon might take longer to complete the procedure than morning procedures.

All enteroscopy procedures were performed by 1 of 4 experienced endoscopists who had previous experience with BE and/or advanced therapeutic endoscopy training. All endoscopists had a minimum experience of performing 50 BEs as an attending physician, and more than 200 BEs had been performed in our endoscopy unit before the study period. The basic demographic information was entered in the database with supporting laboratory studies before the procedure. Urine pregnancy tests were also performed before the procedure in women of childbearing potential. Enteroscopy either through the antegrade or retrograde initial approach was used based on the clinical presentation. The default approach was to use the anterograde approach for the examination if no clinical features were available to guide the decision. If pathology was not reached with the initial insertion route, a tattoo was placed and the opposite anatomic approach was used, as deemed clinically appropriate.

We had previously described the protocol for doing antegrade and retrograde procedures in our institution.8 Total procedure duration was defined as the period from insertion to withdrawal of the enteroscope. Estimated maximal insertion depth with the anterograde approach was defined as the number of centimeters beyond the ligament of Treitz when no further advancement was possible. From the retrograde approach, this represented the number of centimeters passed into the small bowel proximal to the ileocecal valve. Insertion depth by SBE and DBE was measured in centimeters by using the total number of 40-cm push-and-pull cycles on insertion, as defined by May and Nachbar.9 The insertion depth by SE was estimated by counting the amount of small bowel traversed on withdrawal in 5- or 10-cm increments.10 All of the 4 endoscopists used the same technique for measuring the insertion depth. At the point of maximal insertion, a tattoo could be placed by using SPOT ink (GI Supply, Camp Hill, Pa). Total enteroscopy was defined as visualizing the entire small bowel if the ileocecal valve was reached from the antegrade route or as bidirectional complete visualization of the small bowel verified by reaching the previous tattoo site. Diagnostic yield was defined as proportion of cases in which a significant endoscopic finding consistent with patients’ clinical presentation was found. The clinical significance of the endoscopic diagnosis was further classified as definite and suspicious based on the clinical indication for the enteroscopy and appearance of the endoscopic lesion. For example, a small red spot is considered a suspicious lesion for a patient presenting with GI bleeding, whereas a red spot with pulsatile bleeding is considered a definite lesion. Therapeutic yield was defined as the proportion of cases in which endoscopic intervention such as polypectomy, stricture dilation, foreign-body removal, and endoscopic hemostasis was performed. Information on AEs was obtained. An AE was defined based on the American Society for Gastrointestinal Endoscopy workshop as an event that prevents completion of the planned procedure and/or results in admission to hospital, prolongation of existing hospital stay, another procedure (needing sedation/anesthesia), or subsequent medical consultation.11 AEs were categorized as mild (procedure aborted because of an AE, postprocedure medical consultation, or requiring up to 3 days of

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METHODS Patients A retrospective chart review of the prospectively maintained institutional review board–approved database of patients referred to our hospital for BE from January 2008 to August 2009 was performed. Patient demographics, indications, procedural findings, and AEs were collected.

Inclusion and exclusion criteria We included patients who had negative findings on upper endoscopy and colonoscopy and/or localization of small-bowel pathology suspected on capsule endoscopy or other imaging studies in the small bowel. We excluded patients with known large esophageal varices, severe active inflammatory bowel disease, fresh surgical stoma, severe ulcerative esophagitis, medical instability, and inability to provide an informed consent. Patients who had intraoperative deep enteroscopy were excluded. In addition, individuals with altered GI anatomy or previous small-bowel resection or previous laparotomy were excluded from the study.

Clinical variables

Enteroscopy and the small bowel

hospitalization), moderate (requiring 4-10 days of hospitalization, requiring intensive care unit admission for 1 night, requiring endotracheal intubation for conscious sedation, requiring transfusion, requiring repeat endoscopy, requiring interventional radiology, or requiring interventional treatment), and severe (requiring ⬎10 days of hospitalization, requiring intensive care unit admission for ⬎1 night, requiring surgical intervention, or permanent disability).11 AE data were collected only if these patients were readmitted or presented to our hospital emergency departments after the procedure.

Endoscopes DBE procedures were performed by using the Fujinon endoscope system (EN-450PS/EN– 450 TS; Fujinon Inc, Saitama, Japan). SBE procedures were performed by using the SBE endoscope system (SIF-Q180; Olympus Optical, Tokyo, Japan). SE was performed by using the spiral overtube (Endo-Ease Discovery SB; Spirus Medical, Stoughton, Mass). It was used either with the Fujinon double-balloon enteroscope or the Olympus singleballoon enteroscope without their respective overtubes.

Outcome measurement Time of the procedure for our primary outcome was defined dichotomously as procedures starting before noon as morning procedures (AM group) and procedures starting after noon as afternoon procedures (PM group). Positive diagnostic yield was defined as the presence of any significant positive endoscopic finding consistent with patients’ clinical presentation. The clinical significance of endoscopic diagnosis was further classified into definite and suspicious, as described previously. Positive therapeutic yield is defined as performance of any significant therapy excluding biopsies. Enteroscopies with poor bowel preparation precluding safe and effective enteroscopy were excluded from the analysis.

Statistical analysis Descriptive statistics were computed for all factors. These include means and standard deviations for continuous factors and frequencies and percentages for categorical variables. A univariable analysis was performed to compare the procedures performed in the morning with those performed in the afternoon. A Student t test was used to assess differences in continuous variables and Pearson’s ␹2 test was used for categorical factors. In addition, a multivariable logistic regression analysis was performed to assess factors associated with positive diagnostic yield. An automated stepwise variable selection method was performed on 1000 bootstrap samples to choose the final model. Time of day was forced into the model, and age, sex, type of enteroscope, duration of procedure, depth, time of day, and indication were considered for inclusion; factors with an inclusion rate of 50% or more were kept in the final model. P ⬍ .05 was considered 64 GASTROINTESTINAL ENDOSCOPY Volume 77, No. 1 : 2013

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statistically significant. All analyses were performed by using SAS (version 9.2; SAS Institute, Cary, NC) and R (version 2.13.1; The R Foundation for Statistical Computing, Vienna, Austria).

RESULTS Demographic and clinical characteristics There were a total of 250 enteroscopies performed, of which 182 were antegrade (91 SBE, 52 DBE, and 39 SE) and 68 were retrograde (23 SBE, 37 DBE, and 8 SE). A total of 125 patients (50%) underwent enteroscopy in the morning and 125 patients (50%) underwent enteroscopy in the afternoon. The mean age of the patients was 61.5 ⫾ 15.8 years. There was a total of 21 enteroscopies performed bidirectionally. The indications for small-bowel endoscopy were suspected obscure overt GI bleeding in 83 patients (33.2%), obscure occult GI bleeding in 57 patients (22.8%), abdominal pain or suspected Crohn’s disease in 37 patients (14.8%), abnormal capsule endoscopy results in 45 patients (18.0%), abnormal abdominal imaging study findings in 5 patients (2.0%), weight loss in 3 patients (1.2%), abnormal polyposis in 9 patients (3.6%), and other indications in 11 patients (4.4%). In patients with abnormal capsule endoscopy results, blood was seen in the small bowel in 28 patients, and ulcerations in the small bowel were seen in 2 patients. However, there was no clear localization of the site of bleeding that led to balloon enteroscopy in 28 patients. The remaining 2 patients had balloon enteroscopy done for diagnostic purposes to determine the cause of ulcerations. The remaining 15 patients had vascular lesions diagnosed on capsule endoscopy, and balloon enteroscopy was performed for therapeutic purposes. The AM and PM groups were not statistically different in terms of demographics and previous capsule endoscopies performed. The procedure indications were also no different among the 3 groups (Tables 1-4). Obscure GI bleeding was the most common indication for BE in both of the groups.

Diagnostic yield Enteroscopy data for the AM and PM groups are shown in Table 2. Significant endoscopic findings included vascular lesions in 56 patients (22.4%), ulcers or erosions in 12 patients (4.8%), polyps in 21 patients (8.4%), and strictures in 5 patients (2%), for an overall diagnostic yield of 57.2% (Tables 3 and 4). On classification of the lesions into suspicious and definite, 30 patients had suspicious lesions, whereas the remaining 64 patients had definite lesions on enteroscopy. The diagnostic yield was significantly higher with SBE compared with DBE (71.4% and 48.1%, respectively; P ⫽ .02), but was not significantly different between SBE and SE (71.4% and 66.7%, respectively; P ⫽ .87). The diagnostic yield with anterograde enteroscopy was similar www.giejournal.org

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Enteroscopy and the small bowel

TABLE 1. Patient demographics and procedural details of antegrade enteroscopies

Factor

P AM (n ⴝ 91) PM (n ⴝ 91) value

TABLE 2. Patient demographics and procedural details of retrograde enteroscopies

Factor

P AM (n ⴝ 34) PM (n ⴝ 34) value

Age, y

63.2 (15.5)

60.8 (15.5)

.29

Age, y

59.5 (14.5)

60.9 (18.5)

.74

Male

36 (39.6)

43 (47.3)

.30

Male

17 (50.0)

15 (44.1)

.63

Insertion depth, cm*

224.8 (90.5)

239.3 (148.8)

.45

Depth of insertion, cm

Procedure duration, min

42.4 (21.5)

46.2 (22.4)

.25

Procedure duration, min

51.3 (24.3)

66.6 (32.9)

.033

Multiple indications

58 (63.7)

51 (56.0)

.29

Multiple indications

26 (76.5)

24 (70.6)

.58

.029

Type of endoscope

Type of endoscope

100.7 (104.4) 106.2 (102.8)

.26

SBE

50 (54.9)

41 (45.1)

SBE

12 (35.3)

11 (32.4)

DBE

18 (19.8)

34 (37.4)

DBE

16 (47.1)

21 (61.8)

SE

23 (25.3)

16 (17.6)

SE

6 (17.6)

2 (5.9)

7 (7.7)

10 (11.0)

5 (14.7)

6 (17.6)

91 (100.0)

91 (100.0)

34 (100.0)

34 (100.0)

Fluoroscopy used Anesthesia Indication

.44

Fluoroscopy used Anesthesia

.18

Indication

28 (30.8)

19 (20.9)

Obscure occult GI bleeding

2 (5.9)

8 (23.5)

Obscure overt GI bleeding

28 (30.8)

24 (26.4)

Obscure overt GI bleeding

16 (47.1)

15 (44.1)

Vascular lesion on capsule endoscopy

10 (11.0)

4 (4.4)

Vascular lesion on capsule endoscopy

0 (0.0)

1 (2.9)

Abdominal pain

12 (13.2)

22 (24.2)

Abdominal pain

2 (5.9)

1 (2.9)

Polyps

3 (3.3)

5 (5.5)

Polyps

0 (0.0)

1 (2.9)

Small-bowel thickening

2 (2.2)

3 (3.3)

12 (35.3)

7 (20.6)

Weight loss

2 (2.2)

1 (1.1)

Abnormal capsule endoscopy (blood in small bowel and ulcers)

3 (3.3)

8 (8.8)

Abnormal capsule endoscopy (blood in small bowel and ulcers)

2 (5.9)

1 (2.9)

Other

3 (3.3)

5 (5.5)

Values presented as mean (SD) with a t test or as number (%) with Pearson’s ␹2 test. AM, Morning; PM, afternoon; SBE, single-balloon enteroscopy; DBE, double-balloon enteroscopy; SE, spiral enteroscopy. *Data not available for all subjects. Missing value: insertion depth ⫽ 19 cm.

.74

.27

Obscure occult GI bleeding

Other

.83

Values presented as mean (SD) with t test or as number (%) with Pearson’s ␹2 test. AM, Morning; PM, afternoon; SBE, single-balloon enteroscopy; DBE, double-balloon enteroscopy; SE, spiral enteroscopy.

Therapeutic yield

when the procedure was done in the morning versus the afternoon (63.7% and 63.7%, respectively; P ⫽ .99). The diagnostic yield with retrograde enteroscopy was also similar in the AM and PM groups (44.1% and 35.3%, respectively; P ⫽ .46).

Tables 3 and 4 summarize the therapeutic yield of morning and afternoon procedures for anterograde and retrograde procedures; the yield of both was similar. In a total of 69 procedures (27.6%), a therapeutic intervention was performed, including argon plasma coagulation (APC) in 59 (23.6%) cases, dilation in 2 (0.8%), polypectomy in 6 (2.4%) cases, and other therapy in 2 (0.8%) cases. Among the 59 patients in whom APC was performed, 56 were for small-bowel vascular lesions, whereas the remaining 3 patients had it after polypectomies. Of the 56 patients who

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TABLE 3. Enteroscopy findings and treatment with antegrade enteroscopy

Factor Positive diagnostic yield

TABLE 4. Enteroscopy findings and treatment with retrograde enteroscopy

AM (n ⴝ 91)

PM (n ⴝ 91)

P value

58 (63.7)

58 (63.7)

.99

Positive diagnostic yield

.82

Findings

Findings

Factor

Normal/negative

33 (36.3)

33 (36.3)

Normal/negative

Vascular lesion

26 (28.6)

25 (27.5)

Ulcer

5 (5.5)

Polyp/mass Stricture Other

AM (n ⴝ 34)

PM (n ⴝ 34)

P value

15 (44.1)

12 (35.3)

.46 .09

19 (55.9)

22 (64.7)

Vascular lesion

0 (0.0)

5 (14.7)

3 (3.3)

Ulcer

2 (5.9)

2 (5.9)

5 (5.5)

8 (8.8)

Polyp/mass

5 (14.7)

3 (8.8)

0 (0.0)

1 (1.1)

Stricture

3 (8.8)

1 (2.9)

22 (24.2)

21 (23.1)

Other

5 (14.7)

1 (2.9)

Therapy

.85

Therapy

None

60 (65.9)

63 (69.2)

None

Argon plasma coagulation

28 (30.8)

24 (26.4)

Dilation

0 (0.0)

Polypectomy Other

.18 31 (91.2)

27 (79.4)

Argon plasma coagulation

1 (2.9)

6 (17.6)

1 (1.1)

Dilation

1 (2.9)

0 (0.0)

2 (2.2)

2 (2.2)

Polypectomy

1 (2.9)

1 (2.9)

1 (1.1)

1 (1.1)

Any therapy

3 (8.8)

7 (20.6)

.17

Any therapy

31(34.1)

28 (30.8)

.63

Multiple therapies

2 (5.9)

4 (11.8)

.39

Multiple therapies

12 (13.2)

6 (6.6)

.14

Adverse events

2 (5.9)

2 (5.9)

.99

4 (4.4)

2 (2.2)

.41

Multiple findings

3 (8.8)

8 (23.5)

.10

Adverse events Multiple findings

21 (23.1)

18 (19.8)

.59

Values presented as number (%) with Pearson’s ␹ test. AM, Morning; PM, afternoon.

Values presented as number (%) with Pearson’s ␹ test. AM, Morning; PM, afternoon. 2

2

received APC, it was done for definite lesions in 37, whereas it was performed for suspicious lesions in 19.

Procedure duration and insertion depth The procedure durations in the AM and PM groups for antegrade enteroscopy were similar (42.4 ⫾ 21.5 minutes vs 46.2 ⫾ 22.4 minutes, respectively; P ⫽ .25). The mean depths of maximal insertion beyond the ligament of Treitz were also similar (224.8 ⫾ 90.5 cm and 239.3 ⫾ 148.8 cm, respectively; P ⫽ .45). Similarly, the depth of maximal insertion proximal to the ileocecal valve for retrograde enteroscopy was similar in the AM and PM groups (104.4 ⫾ 100.7 cm and 106.2 ⫾ 102.8 cm, respectively; P ⫽ .83) (Tables 1 and 2). However, the procedure durations were significantly shorter in the morning compared with afternoon procedures (51.3 ⫾ 21.3 minutes vs 66.6 ⫾ 32.9 minutes, respectively; P ⫽ .03) (Fig. 1). Unsuccessful intubation of the ileocecal valve via the retrograde approach was similar in morning and afternoon procedures (P ⫽ .99), 3 in morning (3.3%, 1 SBE, 1 DBE, 1 SE) compared with 2 in the afternoon (2.2%, 1 SBE, 1 DBE). 66 GASTROINTESTINAL ENDOSCOPY Volume 77, No. 1 : 2013

Subgroup analysis of the type of enteroscopy Because some studies have reported that SE is easier to perform and is relatively quicker than balloon-assisted enteroscopy, we performed additional subgroup analysis according to the type of enteroscopy (DBE, SBE, and SE). The results are summarized in Table 5. There was no significant difference between morning and afternoon based on the type of enteroscopy used. We also compared the insertion depth in the different enteroscopy systems. The mean maximal insertion depth beyond the ligament of Treitz for antegrade SE and DBE was significantly greater than that for SBE (254.5 ⫾ 127.5 cm with SE and 274.0 ⫾ 150.9 cm with DBE vs 189.1 ⫾ 74.2 cm, respectively; P ⬍ .001). For the retrograde route, the mean maximal insertion depth for DBE was 117.3 ⫾ 115.8 cm, whereas it was 83.0 ⫾ 88.7 cm with SBE and 98.1 ⫾ 71.5 cm with SE.

Multivariable analysis for diagnostic yield On logistic regression analysis, SBE (odds ratio 3.2; 95% CI, 1.3-7.8; P ⫽ .011), male sex (odds ratio 2.7, 95% CI, 1.3-5.7; P ⫽ .008), and increase in duration of procedure by every 5 minutes www.giejournal.org

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Enteroscopy and the small bowel

Figure 1. Procedure duration and insertion depth of enteroscopies performed in the morning (AM) and afternoon (PM). Patients who underwent enteroscopies in the afternoon had significantly longer procedure duration than patients who underwent them in the morning.

TABLE 5. Subanalysis of the diagnostic and therapeutic yield with enteroscopy Antegrade Factor

Retrograde

Scope

AM

PM

P value

AM

PM

P value

Positive diagnostic yield

SBE

35 (70.0)

30 (73.2)

.74

3 (25.0)

4 (36.4)

.55

Therapeutic yield

SBE

31 (62.0)

29 (70.7)

.38

3 (25.0)

5 (45.5)

.3

Positive diagnostic yield

DBE

10 (55.6)

15 (44.1)

.43

9 (56.3)

8 (38.1)

.27

Therapeutic yield

DBE

6 (33.3)

10 (29.4)

.77

8 (50.0)

10 (47.6)

.89

Positive diagnostic yield

SE

13 (56.5)

13 (81.3)

.11

3 (50.0)

0 (0.00)

.21

Therapeutic yield

SE

12 (52.2)

13 (81.3)

.063

3 (50.0)

1 (50.0)

.99

AM, Morning; PM, afternoon; SBE, single-balloon enteroscopy; DBE, double-balloon enteroscopy; SE, spiral enteroscopy.

(OR 1.3; 95% CI, 1.1-1.4; P ⫽ .0004) were associated with increased diagnostic yield. However, morning versus afternoon did not have a significant difference in terms of diagnostic yield (Table 6). Similarly for the retrograde approach, there was no significant difference in terms of diagnostic yield based on morning versus afternoon procedures (Table 6). AEs were seen in 10 patients (4%), and there was no significant difference in AEs between the AM and PM groups using both approaches (Tables 3 and 4). All AEs were mild

and were managed conservatively without the need for surgical intervention or hospitalization for more than 24 hours. Among the 6 patients with AEs after antegrade enteroscopy, 4 patients underwent SBE and 1 patient each underwent DBE and SE, respectively. AEs included postpolypectomy bleeding and bleeding after biopsy, intraprocedural hypoxia requiring discontinuation of the procedure, and postprocedural abdominal pain. All of the patients with postprocedural abdominal pain did not have increased serum amylase or lipase level, suggestive of pancreatitis.

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Adverse events

Enteroscopy and the small bowel

Sanaka et al

This is the first study, to the best of our knowledge, that evaluated the influence of the timing of enteroscopy, morning versus afternoon, on the diagnostic yield, estimated insertion depth, procedure duration, therapeutic yield, and AEs of both antegrade and retrograde enteroscopies. We evaluated the start time as a dichotomous group, morning and afternoon. We observed that the diagnostic and therapeutic yield of BE in patients with suspected small-bowel disease was similar in procedure performed in the morning and afternoon. Similarly, there was no difference in the depth of maximal insertion, completion rates, and overall adverse events. However, findings suggest that retrograde enteroscopies performed in the afternoon might take longer than those performed in the morning. Studies have shown lower completion rates and adenoma detection rates in colonoscopies performed in the later part of the day compared with morning.1-4 Physician fatigue and decreased concentration were hypothesized as possible causative factors for this difference because of prolonged repetitive maneuvering and visual monotony throughout the endoscopist’s workday. The impact of pro-

longed and repetitive work resulting in decreased performance has been reported in various medical and nonmedical professions.12-14 When colonoscopies were performed by physicians in half-day instead of full-day blocks, adenoma detection rates in afternoon procedures did not decrease compared with morning procedures.15 We based our study hypothesis on the fact that BE procedures are prolonged, involving significant endoscope maneuvering along with visual monotony. These factors may lead to physician fatigue. Some of these procedures are very difficult and hence take longer to complete, which may increase the risk of adverse events. Longer procedure durations have been shown to increase the incidence of hyperamylasemia after anterograde DBE.16-18 Prolonged procedures may also potentially lead to deeper levels of sedation and thus increase the risk of sedation-related cardiopulmonary adverse events.19 These procedure-related factors along with prolonged extended workdays may contribute to poorer outcomes with procedures done in the afternoon.12 However, our study results are interesting. Our study results are similar to those of the study on outcomes of ERCP based on timing of procedures, which were similar in both the AM and PM groups.20 There was no difference in cannulation rates, length of procedures, and AEs between the morning and afternoon ERCPs.20 The difference in the efficacy based on timing of procedures between BE and colonoscopy may be influenced by a number of factors. The indications and therapeutic capabilities of various BE systems are heterogeneous. Also BE is usually performed for therapeutic purposes after a diagnostic capsule endoscopy.2 Thus, BE might be more similar to ERCP in terms of diagnostic and therapeutic capability. On the other hand, colonoscopy is more of a screening procedure, and several colonoscopies are performed by an endoscopist in a day, whereas the number of BEs performed by an endoscopist is very small compared with colonoscopies. Because of these factors, physician fatigue, decreased attentiveness, or visual monotony may not be that pertinent to BE compared with screening colonoscopy, which is to an extent more monotonous and repetitive than BE. Our study found that the retrograde BE procedure durations were longer in the afternoon compared with the morning. We excluded patients with poor bowel preparation in our study. However, there is a possibility that bowel preparation could have contributed to prolonged duration of retrograde afternoon procedures. Also, 7 of 34 patients who underwent retrograde enteroscopies in the afternoon received some form of therapy through enteroscopy than 3 of 34 patients in who underwent procedures in the morning. Six patients in the PM group required APC treatment compared with 1 in the morning group. We suspect that because of the bias in the therapeutic requirements in morning compared with afternoon procedures, the procedure duration was likely longer in the PM group.

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TABLE 6. Factors associated with positive diagnostic yield on antegrade and retrograde procedures: multivariable logistic regression analysis Odds ratio (95% CI)

P value

1.2 (0.59-2.6)

.56

0.97 (0.96-0.99)

.003

Duration (5-min increase)

1.3 (1.1-1.4)

⬍.001

Male sex

2.8 (1.3-5.8)

.008

SBE vs DBE

3.0 (1.2-7.5)

.017

SE vs DBE

2.4 (0.89-6.2)

.083

AM vs PM

1.6 (0.58, 4.6)

.36

Male sex

0.41 (0.14, 1.2)

.097

SBE vs DBE

0.58 (0.18, 1.8)

.35

SE vs DBE

0.87 (0.16, 4.7)

.87

Factor Antegrade AM vs PM Depth (5-cm increase)

Endoscope

Retrograde

Endoscope

CI, Confidence interval; AM, morning; PM, afternoon; SBE, singleballoon endoscopy; DBE, double-balloon endoscopy; SE, smallbowel enteroscopy.

DISCUSSION

Sanaka et al

All published studies on SE have reported shorter procedure times, which are shorter than those for SBE or DBE.21,22 However, in our study, SBE had shorter procedure duration than SE and DBE, probably because of the fact that patients with a proximal small-bowel source were receiving SBE as their enteroscopy procedure.23 One could argue that the type of BE used might have affected the morning versus afternoon difference. Retrograde procedures are recognized as more technically challenging than antegrade procedures, with failure of terminal ileum intubation occurring in as many as 21% of DBE cases.24 Furthermore, even after stable ileal intubation is achieved, the insertion depths of retrograde DBE and SBE are consistently much lower than those achieved with antegrade DBE and SBE.25-28 DBE was predominantly represented both in the morning and afternoon procedures. Given the trend for increased procedure duration with afternoon procedures with no differences in diagnostic yield, the sample size of 34 patients might have been too small to detect a significant difference in this study. There are several limitations of this study including its retrospective nature. However, the reporting and documentation were done prospectively, and thus possible underreporting of AEs would be similar. There was no automated system of contacting patients after each procedure, and there is a small chance that these patients may have gone to outside hospital emergency departments, which would not have been recorded in our study. The study population was recruited from a subspecialty tertiary care referral center. The sample size of the study, particularly those undergoing retrograde enteroscopy, was small, and given the significance of procedure times, this may have been underpowered to demonstrate significant differences. There was no randomization, and therefore, there could have been a significant bias in patient selection and use of a particular enteroscopy system in individual cases. The depth of maximal insertion was made by estimation of the distance traversed into the small bowel and may not represent accurate scientific measurements. We do not use carbon dioxide insufflation in our institution to perform enteroscopy, and patients with postprocedure abdominal pain might not have had it if they had carbon dioxide insufflation. Also the use carbon dioxide rather than air for insufflation has been reported to possibly enhance the depth of maximal insertion in DBE.29 Although this has not been reported for SE or SBE, the type of gas used for insufflation could be a potential confounding variable affecting the insertion depth in both the AM and PM groups.

Enteroscopy and the small bowel

formed in the afternoon might take longer than morning procedures. This study demonstrates that the influence of timing of procedures on outcomes may not be similar in various endoscopic procedures, ie, screening colonoscopy, ERCP, and BE. REFERENCES

To conclude, the timing of the procedure, morning versus afternoon, does not affect the diagnostic and therapeutic efficacy of BE in patients with suspected smallbowel disease. However, retrograde enteroscopies per-

1. Sanaka MR, Deepinder F, Thota PN, et al. Adenomas are detected more often in morning than in afternoon colonoscopy. Am J Gastroenterol 2009;104:1659-64. 2. Chan MY, Cohen H, Spiegel BM. Fewer polyps detected by colonoscopy as the day progresses at a Veteran’s Administration teaching hospital. Clin Gastroenterol Hepatol 2009;7:1217-23. 3. Sanaka MR, Shah N, Mullen KD, et al. Afternoon colonoscopies have higher failure rates than morning colonoscopies. Am J Gastroenterol 2006;101:2726-30. 4. Wells CD, Heigh RI, Sharma VK, et al. Comparison of morning versus afternoon cecal intubation rates. BMC Gastroenterol 2007;7:19. 5. Yamamoto H, Sekine Y, Sato Y, et al. Total enteroscopy with a nonsurgical steerable double-balloon method. Gastrointest Endosc 2001;53:216-20. 6. Akerman PA, Agrawal D, Cantero D, et al. Spiral enteroscopy with the new DSB overtube: a novel technique for deep peroral small-bowel intubation. Endoscopy 2008;40:974-8. 7. Mehdizadeh S, Ross A, Gerson L, et al. What is the learning curve associated with double-balloon enteroscopy? Technical details and early experience in 6 U.S. tertiary care centers. Gastrointest Endosc 2006;64:740-50. 8. Sanaka MR, Navaneethan U, Kosuru B, et al. Antegrade is more effective than retrograde enteroscopy for evaluation and management of suspected small-bowel disease. Clin Gastroenterol Hepatol 2012;10:910-6. 9. May A, Nachbar L. Endoscopic interventions in the small bowel using double balloon enteroscopy: feasibility and limitations. Am J Gastroenterol 2007;102:527-35. 10. 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 EndoTrainer. Endoscopy 2005;37:66-70. 11. Cotton PB, Eisen GM, Aabakken L, et al. A lexicon for endoscopic adverse events: report of an ASGE workshop. Gastrointest Endosc 2010;71:446-54. 12. Gaba DM, Howard SK. Patient safety: fatigue among clinicians and the safety of patients. N Engl J Med 2002;347:1249-55. 13. Howard SK, Rosekind MR, Katz JD, et al. Fatigue in anesthesia: implications and strategies for patient and provider safety. Anesthesiology 2002;97:1281-94. 14. Eastridge BJ, Hamilton EC, O’Keefe GE, et al. Effect of sleep deprivation on the performance of simulated laparoscopic surgical skill. Am J Surg 2003;186:169-74. 15. Gurudu SR, Ratuapli SK, Leighton JA, et al. Adenoma detection rate is not influenced by the timing of colonoscopy when performed in halfday blocks. Am J Gastroenterol 2011;106:1466-71. 16. Zepeda-Gómez S, Barreto-Zuñiga R, Ponce-de-León S, et al. Risk of hyperamylasemia and acute pancreatitis after double-balloon enteroscopy: a prospective study. Endoscopy 2011;43:766-70. 17. Matsushita M, Shimatani M, Uchida K, et al. Association of hyperamylasemia and longer duration of peroral double-balloon enteroscopy: present and future. Gastrointest Endosc 2008;68:811. 18. Kopácová M, Rejchrt S, Tachecí I, et al. Hyperamylasemia of uncertain significance associated with oral double-balloon enteroscopy. Gastrointest Endosc 2007;66:1133-8. 19. Patel S, Vargo JJ, Khandwala F, et al. Deep sedation occurs frequently during elective endoscopy with meperidine and midazolam. Am J Gastroenterol 2005;100:2689-95.

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CONCLUSIONS

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20. Mehta PP, Sanaka MR, Parsi MA, et al. Effect of the time of day on the success and adverse events of ERCP. Gastrointest Endosc 2011;74:303-8. 21. Akerman PA, Agrawal D, Chen W, et al. Spiral enteroscopy: a novel method of enteroscopy by using the Endo-Ease Discovery SB overtube and a pediatric colonoscope. Gastrointest Endosc 2009;69:327-32. 22. Khashab MA, Lennon AM, Dunbar KB, et al. A comparative evaluation of single-balloon enteroscopy and spiral enteroscopy for patients with mid-gut disorders. Gastrointest Endosc 2010;72:766-72. 23. Sanaka MR, Upchurch BR, Lopez R, et al. Single balloon enteroscopy might be more effective than double balloon and spiral enteroscopy in the evaluation and management of small bowel disease [abstract]. Gastrointest Endosc 2010;71:AB368-9. 24. Mehdizadeh S, Han NJ, Cheng DW, et al. Success rate of retrograde double-balloon enteroscopy. Gastrointest Endosc 2007;65:633-9.

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25. 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. 26. Heine GD, Hadithi M, Groenen MJ, et al. Double-balloon enteroscopy: indications, diagnostic yield, and complications in a series of 275 patients with suspected small-bowel disease. Endoscopy 2006;38:42-8. 27. Gross SA, Stark ME. Initial experience with double-balloon enteroscopy at a U.S. center. Gastrointest Endosc 2008;67:890-7. 28. Tsujikawa T, Saitoh Y, Andoh A, et al. Novel single-balloon enteroscopy for diagnosis and treatment of the small intestine: preliminary experiences. Endoscopy 2008;40:11-5. 29. Lo SK. Technical matters in double balloon enteroscopy. Gastrointest Endosc 2007;66:S15-8.

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