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American Journal of Gastroenterology ISSN 0002-9270


C 2006 by Am. Coll. of Gastroenterology doi: 10.1111/j.1572-0241.2006.00745.x
Published by Blackwell Publishing

Prospective Comparison of Push Enteroscopy and


Push-and-Pull Enteroscopy in Patients with Suspected
Small-Bowel Bleeding
Andrea May, M.D., Ph.D., Lars Nachbar, M.D., Marion Schneider, M.D., and Christian Ell, Ph.D.
Department of Internal Medicine II, HSK Wiesbaden, Teaching Hospital of the University of Mainz,
Wiesbaden, Germany

BACKGROUND The management of patients with suspected mid-gastrointestinal bleeding has in the past been
AND AIMS: difficult, as push enteroscopy (PE) only allows limited endoscopic access for diagnosis and
treatment. Recently published uncontrolled data on push-and-pull enteroscopy (PPE) using the
double-balloon technique suggest that this new method has a high diagnostic yield and therapeutic
efficacy. A prospective controlled study was therefore carried out to compare PPE with PE as the
common nonsurgical gold standard method.
METHODS: The diagnostic yield, complications, and various examination parameters were compared in 52
consecutive patients with suspected mid-gastrointestinal bleeding who were evaluated with both
enteroscopy methods.
RESULTS: No relevant complications were observed with either method. Sedoanalgesia, examination times,
and X-ray exposure were lower with PE. The insertion depth was significantly greater with PPE than
with PE (230 cm vs 80 cm, p < 0.0001). The overall diagnostic yield with PPE (38 of 52 patients,
73%) and the results of oral PPE only (33 of 52 patients, 63%) were superior to those with PE (23
of 52 patients, 44%; p < 0.0001). PPE identified additional lesions in deeper parts of the small
bowel in PE-positive patients in 78% of cases (18 of 23 patients).
CONCLUSIONS: For endoscopic examination of the small bowel in patients with suspected mid-gastrointestinal
bleeding, PPE is superior to PE with regard to the length of small bowel visualized, as well as the
diagnostic yield. As the method also allows endoscopic treatment to be carried out, PPE should
always be considered before open surgery and intraoperative endoscopy in patients with
mid-gastrointestinal bleeding.
(Am J Gastroenterol 2006;101:2016–2024)

INTRODUCTION enteroscopy in a similar way as capsule endoscopy, while si-


multaneously providing an ability to take biopsies and carry
Since the introduction of wireless capsule endoscopy in 2001, out endoscopic interventions in the small bowel as in PE
much more effective detection of bleeding sources in the and intraoperative enteroscopy, which were the endoscopic
small bowel has become possible in patients with chronic or methods of choice for examining the small bowel before the
acute recurrent gastrointestinal bleeding in whom the loca- introduction of PPE. To date, however, there have been no
tion of the bleeding source is unclear (1–5). However, the prospective trials comparing the new push-and-pull method
capsule is a purely diagnostic device that does not allow of enteroscopy with PE as the usual nonsurgical gold standard
biopsy samples to be taken or treatment to be carried out. method.
Push enteroscopy (PE) became the established endoscopic The prospective study presented here included 52 consec-
method of examining the proximal part of the small bowel utive patients with suspected chronic or acute recurrent mid-
during the 1980s, and with its facilities for biopsy sampling gastrointestinal bleeding and compared PE with PPE using
and treatment it has continued to hold its place. However, the double-balloon technique. The aim of the study was to
the insertion depth is generally limited to the proximal je- evaluate the length of small bowel examined, the diagnostic
junum (6, 7). The new method of push-and-pull enteroscopy yield, complications, examination time, and other parame-
(PPE) using a double-balloon technique was first introduced ters such as the amount of sedoanalgetic medication and X-
in Japan by Yamamoto and colleagues in 2001 (8) and by ray exposure, as well as staffing requirements, with the two
May and colleagues in Europe in 2003 (9). PPE allows total methods.

2016
Push Enteroscopy versus Push-and-Pull Enteroscopy 2017

PATIENTS AND METHODS blood was seen in the small bowel, without a bleeding source
being identified. No relevant pathological findings had been
Patients identified in six of the 22 patients (27%).
Between December 2003 and October 2004, 69 patients PE examinations were carried out first, followed by oral
with chronic or acute recurrent gastrointestinal bleeding PPE examinations, by experienced investigators for both en-
and a suspected bleeding source in the small bowel (mid- teroscopy techniques (AM, LN). Before the study was started
gastrointestinal bleeding) presented for PPE at our tertiary approximately 50 PPE procedures had been done. Anal PPE
referral center. Mid-gastrointestinal bleeding was defined as was carried out if the oral examination did not identify a
a bleeding source or sources not accessible either with stan- bleeding source or there was a suspicion that some lesions
dard upper gastrointestinal endoscopy (esophagogastroduo- were also located in the distal part of the small bowel (e.g.,
denoscopy) or standard colonoscopy. Fifty-two patients, with angiodysplasias seen with capsule endoscopy). Depending
a mean age of 55 ± 17 yr, were enrolled in the study after on the individual patient’s condition, the anal PPE procedure
providing written consent and underwent both examinations. was conducted on the next day or the day after.
Data for the patients are listed in Table 1. Seventeen patients A standardized form was completed after each examina-
declined to undergo the additional PE. The average lowest tion to record the following data: all information about the
hemoglobin level was 8.0 ± 6.9 g/dL (median 6.9 g/dL, range patients, including age, gender, and examination date; and en-
3.8–11.4 g/dL). Thirty-five of the 52 patients (67%) had re- teroscopy data, including the number of staff required, time
ceived blood transfusions, with a median of 10 blood units required for the examination, amount of sedoanalgetic med-
(range 2–170). The obscure gastrointestinal bleeding had per- ication, X-ray exposure time (min and dGy/cm2 ), insertion
sisted for a median of 21.5 months (range 0.5–288 months) depth, pathological findings, and acute complications. Ther-
(Table 1). All of the patients were suffering from overt or oc- apeutic procedures such as argon plasma coagulation of an-
cult bleeding. Overt bleeding is defined as macroscopically giodysplasias were only carried out in PPE sessions. The en-
visible bleeding—i.e., evidence of melena or hematochezia. doscopic diagnosis obtained with PE was not blinded for the
In occult bleeding, there is no melena or peranal bleeding, endoscopist performing PPE, as only two endoscopists con-
but the fecal occult blood test is positive. No bleeding sources ducted all of the investigations in the study. The intention was
had been identified in any of the diagnostic procedures, such to ensure that the enteroscopies—including parameters that
as upper and lower gastrointestinal endoscopy (with multiple are quite examiner-dependent, such as the assessment of the
procedures in the majority of cases), carried out at external in- insertion depth—were carried out in a standardized way and
stitutions before the patients were admitted to our department. that all aspects of interest were documented prospectively.
Radiological diagnostic procedures (computed tomography,
enteroclysis, and/or angiography) and scintigraphic diagnos-
Push Enteroscopy
tic procedures had been carried out in 32 of the 52 patients
A standard scope (Fujinon EN-410WM, Fujinon Inc.,
(61.5%) without the bleeding source being identified. Cap-
Saitama City, Japan) with a working length of 230 cm and
sule endoscopy had been carried out in 22 of the 52 patients
an outer diameter of 10.5 mm was used for PE (Fig. 1). The
(42%), revealing pathological lesions that were assessed as
reusable overtube is 835-mm long, with an outer diameter
representing a definite, potential, or uncertain bleeding source
of 14.6 mm. The enteroscope’s working channel has a di-
in 14 of the 22 patients (64%). In two patients (9%), only
ameter of 2.8 mm. The overtube was used in all of the PE

Table 1. Patient Data and Bleeding Parameters


Study Group
Parameter (N = 52)
Men/women 32/20
Age (yr)
Mean ± SD 55 ± 17
Range 26–84
Lowest hemoglobin value (g/dL)
Mean ± SD 8.0 ± 6.9
Median 6.9
Range 3.8–11.4
Period of CGB (months)
Median 21.5
Range (0.5–288)
Patients requiring blood transfusion, N (%) 35 (67%)
Units of packed red cells transfused
Median 10
Range (2–170)
Figure 1. A radiological view of push enteroscopy, with an insertion
CGB = chronic gastrointestinal bleeding. depth of 80 cm.
2018 May et al.

procedures, as prospective studies have shown that the inser-


tion depth is significantly greater when an overtube is used
(6, 7). The overtube is positioned just in front of the pylorus
to avoid damage to the small-bowel tissue and the papilla,
as it has been reported that perforation and pancreatitis are
possible complications during PE (10, 11). The enteroscope
is inserted as far as possible into the small bowel (Fig. 1). As
the enteroscope is advanced, the overtube is held in a stable
position, avoiding withdrawal and advancement in order to
reduce the risk of complications. Under fluoroscopic guid-
ance, the position of the enteroscope is checked and looping
within the stomach is avoided. After straightening, the scope
is pulled back until the pylorus is reached again. The distance
in centimeters between the pylorus and the deepest point af-
ter straightening of the scope is documented as the inser-
tion depth. During withdrawal of the enteroscope, hyoscine
butylbromide (butylscopolamine) is administered in order to
reduce peristalsis in the small bowel and thus optimize visu-
alization. No specific preparation was administered for the
oral approach. The examinations were carried out with the
patients under conscious sedation, and there was no need for
general anesthesia. The examinations were all carried out on
an in-patient basis, and the patients were asked about symp-
toms approximately 4 h after the end of the examination and
also the next day.
PPE with the Double-Balloon Technique
The double-balloon enteroscopy system (Fujinon EN-
450P5/20, Fujinon Inc.) consists of a high-resolution video
endoscope with a working length of 200 cm and an outer
diameter of 8.5 mm, and a flexible single-use overtube with
a length of 145 cm (including the balloon) and an outer di-
ameter of 12 mm (Figs. 2 and 3). The enteroscope’s working
channel has a diameter of 2.2 mm. Latex balloons are at-
tached at the tip of the enteroscope and the overtube, and
are inflated and deflated with air from a pressure-controlled
pump system. The small bowel is threaded onto the overtube
by alternating the inflation and deflation of the balloons, al-
ternating the insertion of the scope and overtube, and pulling
back the enteroscope and overtube (Fig. 2A–C). The prin-
ciple of the double-balloon technique has been described in
detail previously (8, 9). During withdrawal, hyoscine butyl-
bromide is administered in order to reduce peristalsis in the
small bowel and thus optimize visualization.
No specific preparation was administered for the oral
approach. For enteroscopy from the anal approach, bowel
cleansing was performed in the same way as in colonoscopy.
The examinations were carried out with the patients under
conscious sedation, in the same way as in colonoscopy and
upper gastrointestinal endoscopy. General anesthesia was not
required. The examinations were all carried out on an in-
patient basis, and the patients were asked about symptoms Figure 2. (A) Radiological view of an oral push-and-pull en-
approximately 4 h after the end of the examination and also teroscopy with an insertion depth from the pylorus of approximately
200 cm. (B) Radiological view of an anal push-and-pull enteroscopy
the next day. with an insertion depth of approximately 350 cm from the ileocecal
The method used to measure the small-bowel segments valve. (C) Radiological view of a complete small-bowel endoscopy
visualized has been described in detail elsewhere previously from the pylorus to the cecum within one oral PPE session.
Push Enteroscopy versus Push-and-Pull Enteroscopy 2019

(12). The endoscopist has to estimate the effective insertion ( = 0.3/0.6) among PE-negatives. A test with 5% type I er-
length of the enteroscope by endoscopic checking of the in- ror rate and 90% power needs 19 patients with negative PE
strument’s advancement, and has to estimate the length of findings. To obtain at least 19 negative PE findings with a
small bowel “released” during insertion of the overtube and probability of 90%, 38 patients are needed. With 38 patients,
pulling back of the enteroscope and overtube. The length of the overall power is at least 81%.
small bowel visualized and threaded on during each push-
and-pull maneuver is noted on a standardized form. At the
RESULTS
end of the examination, all of the individual lengths advanced
are added up. This technique requires some experience, but PE and PPE were carried out successfully in all of the patients
has been evaluated using an animal model (12). without relevant technical problems. No severe enteroscopy-
associated complications (in either PE or PPE), such as per-
Ethical Aspects foration, bleeding induced by mucosal injury, or pancreati-
A standard information pamphlet (proCompliance publish- tis, were observed. In one female patient, a mucosal injury
ers, Erlangen, Germany) was used for PE, as this exami- was noted in the proximal esophagus just below the up-
nation is already an established investigation method in the per esophageal sphincter after PE, probably induced by the
small bowel. overtube. The patient suffered from odynophagia for several
All of the patients provided written consent to undergo days, but no severe problems occurred. Six of the 52 patients
PPE, including endoscopic treatments such as argon plasma (11.5%) reported a sore throat after PE. With regard to PPE,
coagulation or polypectomy/mucosal resection, after receiv- minor side effects such as abdominal pain on the day of in-
ing extensive information regarding the experimental nature vestigation and the following day (probably mainly caused
of the procedure. All of the patients were informed that sur- by air insufflation) and sore throat occurred in 11 of the 52
gical laparotomy with intraoperative enteroscopy or small- patients (21%). One patient had a raised temperature (39◦ C)
bowel resection is currently the standard approach if conven- during the night after the PPE, without further symptoms,
tional PE is unable to find the bleeding source or to reach a and the fever dropped spontaneously without antibiotics by
lesion requiring treatment that has previously been identified the next day.
using other methods such as capsule endoscopy. Approval Details of the conscious sedation and investigation param-
for administering PPE in patients with suspected or proven eters such as X-ray exposure time, investigation time, and the
disease of the small bowel was received from the Ethics Com- depth of endoscope advancement in centimeters are listed in
mittee of the State of Hesse, Germany. Tables 2 and 3. Generally, a combination of midazolam and
meperidine (pethidine) and/or fat-soluble diazepam was cho-
Statistical Analysis sen for conscious sedation; propofol was administered alone
Descriptive statistics were calculated for the patients’ data or in combination with meperidine. For PE, 29 patients re-
and clinical parameters and presented as means and medi- ceived a combination of midazolam, fat-soluble diazepam,
ans, as well as standard deviations and ranges (minimum- and meperidine; midazolam and meperidine were adminis-
maximum) for continuous data and absolute and relative tered in 18 patients; four patients received propofol; and one
frequencies for categorical data. For continuous data, com- patient received a combination of propofol and meperidine.
parisons between the two groups were carried out using the For oral PPE, 27 patients received a combination of midazo-
Mann-Whitney U test. A p value of ≤0.05 was considered to lam, fat-soluble diazepam, and meperidine; two patients re-
be statistically significant. The χ 2 test was used for categor- ceived a combination of midazolam and meperidine; and one
ical data. patient received midazolam alone. Propofol was given alone
The null hypothesis of the test was that PPE is equivalent in 13 patients, and a combination of propofol and meperidine
to PE. On the basis of previous experience, it was assumed was administered in nine patients. For anal PPE, a combi-
that 40% of the patients would have positive PE findings. nation of midazolam, fat-soluble diazepam, and meperidine
It was further assumed that under the aforementioned null was chosen in 16 patients; a combination of midazolam and
hypothesis, a PPE procedure subsequent to a PE procedure meperidine was administered in 10 patients; and propofol
would identify 8% more positive cases and would recapture was given in one patient.
all positive PEs. The null hypothesis therefore implies a 48% Statistically significant differences were seen between the
rate of positive PPE findings. Because this is a paired-sample two groups (PE vs oral PPE) with regard to conscious se-
design in which double-positive cases do not contribute to the dation (midazolam p < 0.0001 and propofol p < 0.002)
test statistic, only patients with negative PE findings are rele- and investigation parameters such as X-ray exposure (du-
vant for the comparison. Hence, P0 = 0.133 ( = 0.08/0.60) is ration p < 0.0001 and dGy/cm2 p < 0.006), insertion depth
the null hypothis to be tested by the binomial test against the (p < 0.0001), and investigation time (p < 0.0001). The inser-
alternative of more than 13.3% positive PPEs among nega- tion depth with oral PPE was nearly three times greater than
tive PEs. The number of cases is calculated for the alterna- with PE (230 cm vs 80 cm). Staffing requirements were gen-
tive hypothesis that subsequent PPE provides a 30% rate of erally higher with PPE, with three persons (one doctor and
additional positive findings among all patients or P1 = 0.5 two nurses for endoscopic assistance, or two doctors and one
2020 May et al.

Table 2. Comparison of Push Enteroscopy and Push-and-Pull Enteroscopy with Regard to Sedoanalgetic Medication
Push Enteroscopy Oral Push-and-Pull
Conscious Sedation (N = 52) Enteroscopy (N = 52) p Value
Midazolam (mg)
Mean ± SD 8±3 11 ± 3 <0.0001
Median 7 12.5
Range 5–15 5–17
Meperidine (pethidine) (mg)
Mean ± SD 50 ± 0 52 ± 12 n.s. (p = 0.202)
Median 50 50
Range 50–50 25–100
Diazepam (mg)
Mean ± SD 9±3 10 ± 3 n.s. (p = 0.349)
Median 10 10
Range 2.5–15 5–20
Propofol (mg)
Mean ± SD 317 ± 137 692 ± 287 <0.002
Median 300 690
Range 80–500 50–1,150
Hyoscine butylbromide (mg)
Mean ± SD 32 ± 11 48 ± 20 <0.0001
Median 40 40
Range 20–60 20–100

nurse for endoscopic assistance) being needed—especially in Table 4. Altogether, pathological lesions were found with PE
case of therapeutic interventions or using propofol sedation— in 23 of the 52 patients (44%) and with PPE in 38 of the 52
in comparison with two persons for PE (one doctor and one patients (73%). The bleeding source was found with oral PPE
nurse for endoscopic assistance). in 32 of the 52 patients (61.5%); the diagnosis was only made
With PPE, the examination time is approximately three with anal PPE in six of the 52 patients (11.5%)—including
times longer than with PE (median 21 min vs 68 min). How- colon cancer (N = 2); ulcerations resulting from nonsteroidal
ever, it should be taken into account that endoscopic treatment
procedures were carried out during the PPE sessions, while
PE was only carried out for diagnostic purposes. Table 4. Diagnostic Yield of Push Enteroscopy and Push-and-Pull
The detailed results with regard to the diagnostic yield of Enteroscopy
PE and PPE and the therapeutic implications are listed in
Push Oral Anal
Pathological Enteroscopy PPE PPE
Table 3. Comparison of Push Enteroscopy and Push-and-Pull En- Findings (N = 52) (N = 52) (N = 27)
teroscopy with Regard to Examination Parameters Small bowel
Angiodysplasias 17 21 2∗
Push Oral Push-and
Diverticulosis 2 2 –
Enteroscopy Pull Enteroscopy p Value
Malignant tumor – 3 –
X-ray exposure Benign polyp – 1 1
time (min) NSAID ulcerations – 1 –
Mean ± SD 1.0 ± 1.2 3.0 ± 3.6 <0.0001 Hypertensive enteropathy 1 1 –
Median 0.60 1.6 Behçet’s disease 1 1 –
Range 0.1–5.1 0.0–17.1 Dieulafoy ulcer – 1
Dosage (dGy/cm2 ) Ulceration of an anastomosis – – 1
Mean ± SD 108 ± 121 206 ± 239 <0.006 Total 21 31 4
Median 68.0 102.0 Outside of the small bowel
Range 10–746 0–1172 Colon cancer – – 2
Insertion depth (cm) NSAID ulceration in – – 1
Mean ± SD 80 ± 18 230 ± 100 <0.0001 the colon
Median 80 220 Angiodysplasias in – – 1†
Range 30–110 0∗ –510 the colon
Examination Ulceration in the stomach 1 2‡ –
time (min)
NSAID = nonsteroidal antiinflammatory drug; PPE = push-and-pull enteroscopy.
Mean ± SD 21 ± 10 68 ± 25† <0.0001 ∗
Angiodysplasias had already been found on oral PPE in one patient.
Median 21 67 †
In this patient, anal PPE revealed one angiodysplasia in the colon, but the diagnosis
Range 0–54 10–120 had been already made with oral PPE, which identified several angiodysplasias in the
proximal part of the small bowel.
∗ ‡
PPE was not performed because of the ulcer seen in the stomach. An ulceration not seen during push enteroscopy was found in the gastric fundus in

Including therapeutic interventions. one patient.
Push Enteroscopy versus Push-and-Pull Enteroscopy 2021

antiinflammatory drugs (NSAIDs) in the colon (N = 1); ul- a combination of injection therapy with diluted epinephrine
ceration in the ileum at the anastomosis after a small-bowel solution in four patients; polypectomy was carried out in 2
resection (N = 1); a polyp (N = 1); and angiodysplasias in of the 38 patients (5%). All of the endoscopic treatments
the ileum (N = 1). PPE thus provided a significantly higher were administered without complications. Medical therapy
diagnostic yield than PE, even when only PE and oral PPE was started or changed in 3 of the 52 patients (6%). Surgi-
were compared (p < 0.0001). cal treatment was found to be indicated by the PPE findings
A significant difference still persists if all the lesions not in 9 of the 52 patients (17%); eight of these patients un-
located in the small bowel are omitted. PE then identified the derwent abdominal surgery, and one received intraoperative
bleeding source in 21 of 47 patients (46%), oral PPE in 31 of enteroscopy with argon plasma coagulation. In the latter pa-
47 patients (66%), and anal PPE in three of 47 patients (6%). tient, total enteroscopy was not possible with PPE because
The lesions found with the anal PPE had not been reachable of multiple prior abdominal operations, and the patient was
with a colonoscope. In all, PPE provided a diagnostic yield for continuing to have bleeding from angiodysplasias.
small-bowel lesions of 72% (34 of 47 patients). Twenty-six Pathological findings were not identified with either PE or
patients had negative PE findings, 11 of whom had positive PPE in only 14 of the 52 patients (27%); in these cases, a wait-
oral PPE findings. The proportion 11/26 = 0.43 is signifi- and-see approach without further measures was chosen.
cantly larger than 0.133 (p <0.0001). The 95% confidence
interval for the conditional probability of achieving a positive
DISCUSSION
oral PPE, given a negative PE, is 0.26–0.61.
Total enteroscopy with a combination of the oral and anal The management of patients with suspected mid-
approaches was carried out in eight of the 52 patients (15%); gastrointestinal bleeding—i.e., with a bleeding source
only a minority of patients required a total enteroscopy. Total suspected in the small bowel after negative upper and lower
enteroscopy was achieved in 8 of the 12 patients in whom gastrointestinal endoscopies—has been problematic for a
it was attempted (67%). All of the lesions found with PE considerable period. The results of uncontrolled studies of
were confirmed on PPE. Additional information (such as the new method of PPE, which allows endoscopic exami-
more angiodysplasias) was obtained with oral PPE in 18 nation of the entire small bowel or at least a large part of
of the 23 PE positive patients (81%), i.e., who had posi- it, have recently been published and have suggested a high
tive findings on PE. diagnostic and therapeutic yield, as well as a low compli-
The bleeding source was found outside of the small bowel cation rate (13–16). However, no data have previously been
in five patients. Two patients were suffering from a colon available comparing this new device with the common non-
carcinoma located in the cecum that had not been detected surgical gold standard method of PE. PE was previously the
during the previous colonoscopy. Passage through the colon method of choice for screening the upper part of the jejunum
had been very difficult in these cases, so that the cecum had in patients with obscure bleeding, and for treating lesions
probably not been reached before. In a third patient, some, in the proximal part of the small bowel. It appears that the
probably NSAID-induced, ulcerations were found in the as- length of the enteroscope does not significantly affect the in-
cending colon during anal PPE. This patient, who had sev- sertion depth (17) and that using an overtube can significantly
eral concomitant diseases, always had problems with colon increase the length of small bowel capable of being visual-
cleansing, which may explain why the ulcerations had not ized endoscopically (6, 7). With an overtube, a postpyloric
been found previously. In addition, he had some angiodys- insertion depth of up to 120 cm was found to be possible in
plasias in the stomach and duodenum, so that further an- two prospective studies (6, 7). A single-center retrospective
giodysplasias in the small bowel were suspected. The fourth analysis even reported average insertion depths of 120 cm
patient was a young man with a history of intensive treat- (18)—lengths that have otherwise only been reported with
ment for scrotal carcinoma; a large ulceration was found in the new type of variable-stiffness enteroscope (19, 20). The
the fundus. The lesion had probably not been identified during examiners’ level of experience is one possible explanation
a previous esophagogastroduodenoscopy because the patient for these divergences, and the use of different measurement
had been investigated in an external institution on an out- methods may also play a role. However, the average inser-
patient basis without any sedation, and he reported having a tion depth of about 70 cm reported in the two prospective
very strong gag reflex. In the fifth patient, in addition to some trials (6, 7) appears to reflect the general situation better and
tiny angiodysplasias, an ulceration in the stomach was found is confirmed by the prospective data obtained in the present
that had probably been the relevant bleeding source. These study, with an average insertion depth of 80 cm. As the use
findings underline the necessity to always check whether an of an overtube is important for effective PE, a system with
upper or lower GI endoscopy has to be repeated before a an overtube was used in the present study. Complications
small-bowel diagnostic is done. such as mucosal stripping, perforation, and pancreatitis that
With regard to the therapeutic implications, the results have been reported with PE were caused by the overtube and
of the enteroscopy influenced the subsequent treatment in mainly located in the duodenum (10, 11, 21). To minimize
38 of the 52 patients (73%). Twenty-six of the 52 patients the risk of complications, it was decided in the present study
(50%) underwent endoscopic therapy: argon plasma coagu- to position the overtube in front of the pylorus and not to pass
lation in 24 of 38 (63%) patients with positive findings, with the pylorus. This is probably the reason why there was only
2022 May et al.

one minor complication in the proximal part of the esophagus ever, even in cases in which PE did provide a diagnosis, PPE
in this trial, with no problems being encountered in the small was able to identify additional lesions in the deeper part of
bowel and no cases of pancreatitis. the small bowel in nearly 80%, as well as providing the op-
Even when a combination of the oral and anal route is tion of treating them. This advantage comes at the cost of a
used with PE, it is not possible to achieve total enteroscopy significantly longer investigation time, as well as increased re-
of the entire small bowel—partly explaining the low diag- quirements for sedoanalgetic medication, longer X-ray expo-
nostic yield of 26% with PE in this study (18). In previously sure, and higher staffing requirements in comparison with PE.
published data, the reported diagnostic yield with PE in pa- However, it can be assumed that time, staffing, and costs are
tients with obscure gastrointestinal bleeding has ranged from much lower in comparison with intraoperative enteroscopy,
26% to 75% (7, 11, 21–25). Three points are very important although there have not yet been any prospective trials or cost
in interpreting these data: the selection of patients and num- analyses on these issues. In addition, the complication rate of
ber of patients, on the one hand, and the number of lesions in PPE, at about 1% (13–16), appears to be lower than that in
the proximal upper gastrointestinal tract, on the other. Partic- intraoperative enteroscopy, for which complication rates up
ularly in papers reporting a high diagnostic yield, about 50% to about 50% have been reported (29–33). In addition, there
of the findings have been located in the upper gastrointestinal have not yet been any cases of mortality associated with PPE,
tract, accessible with a standard gastroscope; this means that compared with the approximately 2% rate of perioperative
the percentage of pathological findings in the distal duode- mortality associated with intraoperative enteroscopy (5).
num and proximal jejunum in which PE is needed to obtain With regard to the complication rate, no severe complica-
the diagnosis is much lower. In a prospective study including tions occurred in the present study with either PE or PPE.
a large number of patients, Taylor et al. (25) reported a diag- Complication rates of 0.6–2% have been reported in two
nostic yield of 40%, a rate that is quite similar to the present larger series investigating PE (18, 25). The main risks in PE
results at about 45%. One of the reasons for the diagnostic are perforation and pancreatitis; no cases of mortality have
yield of PE being higher in the present study than in trials yet been reported with the method. On the basis of the papers
comparing the results of PE and capsule endoscopy (1, 2, 26– published to date, the complication rates with PE and PPE ap-
28) is the large numbers of angiodysplasias, often scattered pear to be similar (13–16). Fortunately, no complications were
all over the small bowel. The diagnostic yield of PE in these encountered in any of the additional endoscopic interventions
comparative studies varied from 28% to 38% in comparison carried out during PPE in the present trial—illustrating the
with the results of capsule endoscopy, which had figures about easy handling and good control that the system provides.
two times higher. The explanation for this is clear—capsule In summary, in patients with suspected mid-gastroi-
endoscopy allows the examination of the entire small bowel, ntestinal bleeding, PPE is superior to PE for endoscopic ex-
whereas the insertion depth of PE is limited. Intraoperative amination of the small bowel, both with regard to the length
enteroscopy was therefore for a long period the gold stan- of small bowel visualized and to the diagnostic yield. As the
dard for the detection and treatment of lesions in the small method also allows treatment to be carried out, PPE should
bowel, with a diagnostic yield of 70–80% (29–33). Even after always be considered before laparotomy and intraoperative
the introduction of wireless capsule endoscopy, intraopera- endoscopy in patients with mid-gastrointestinal bleeding.
tive enteroscopy continued to be the method of choice for
the treatment of lesions in the deep small bowel that were
not accessible using PE. However, intraoperative enteroscopy ACKNOWLEDGMENT
requires considerable time, staff, and costs, and is associ-
ated with a substantial risk of complications and mortality We are grateful to Michael Robertson for translating and re-
(5, 29–33). vising the manuscript and to Prof. Manfred Berres (Depart-
The new method of PPE with the double-balloon technique ment of Mathematics and Applied Technology, University of
(double-balloon enteroscopy) (9, 8, 13, 14) for the first time Applied Sciences, Koblenz, Germany) for sample size calcu-
allows total enteroscopy and visualization of a large part of lation and assistance in statistical analysis.
the small bowel with a conventional endoscope without the
need for surgical laparotomy. In rare cases, total enteroscopy
STUDY HIGHLIGHTS
can be achieved via the oral route alone, but generally a com-
bination of the oral and anal routes is necessary. Because What Is Current Knowledge
the whole small bowel, or at least a large part of it, can r Insertion depth of push enteroscopy is limited to the
be seen—approximately 250 cm with the oral approach, on
proximal jejunum.
average—a high diagnostic yield can be expected with PPE. r The diagnostic yield of push enteroscopy can be esti-
This assumption has been confirmed by several prospective
mated on approximately 40%.
and retrospective single-center and multicenter trials of PPE, r With the new method of push-and-pull enteroscopy in
reporting diagnostic yields of approximately 70–80% (13–
16). These data correspond to the results of the present trial, double-balloon technique also deeper parts of the small
with an overall diagnostic yield of approximately 70%. How- bowel can be reached.
Push Enteroscopy versus Push-and-Pull Enteroscopy 2023

13. Yamamoto H, Kita H, Sunada K, et al. Clinical outcomes


What Is New Here of double-balloon endoscopy for the diagnosis and treat-
r This is the first prospective study comparing push en-
ment of small-intestinal diseases. Clin Gastroenterol Hepa-
tol 2004;2:1010–6.
teroscopy and push-and pull enteroscopy in double- 14. May A, Nachbar L, Schneider M, et al. Push-and-pull
balloon technique in patients with mid GI bleeding. enteroscopy using the double-balloon technique (double-
r Push-and-pull enteroscopy is superior to push en- balloon enteroscopy): Feasibility, diagnostic and therapeutic
yield in patients with suspected small bowel diseases. Gas-
teroscopy both with regard to the length of small bowel trointest Endosc 2005;62:62–70.
visualized and to the diagnostic yield. 15. Gasbarrini A, di Caro S, May A, et al. The European
experience with double-balloon endoscopy: Indications,
methodology, safety and clinical impact. Gastrointest En-
dosc 2005;62:545–50.
Reprint requests and correspondence: Andrea May, M.D., Ph.D., 16. Ell C, May A, Nachbar L, et al. Push-and-pull enteroscopy in
Department of Internal Medicine II, HSK Wiesbaden, Ludwig- the small bowel using the double-balloon technique: Results
Erhard-Strasse 100, 65199 Wiesbaden, Germany. of a prospective European multicenter study. Endoscopy
Received February 8, 2006; accepted April 11, 2006. 2005;37:613–6.
17. Benz C, Jakobs R, Riemann JF. Does the insertion depth
in push enteroscopy depend on the working length of the
REFERENCES enteroscope? Endoscopy 2002;34:543–5.
18. Landi B, Tkoub M, Gaudric M, et al. Diagnostic yield
1. Ell C, Remke S, May A, et al. The first prospective controlled of push-type enteroscopy in relation to indication. Gut
trial comparing wireless capsule endoscopy with push en- 1998;42:421–5.
teroscopy in chronic gastrointestinal bleeding. Endoscopy 19. Harewood GC, Gostout CJ, Farrell MA, et al. Prospective
2002;34:685–9. controlled assessment of variable stiffness enteroscopy. Gas-
2. Delvaux M, Fassler I, Gay G. Clinical usefulness of the trointest Endosc 2003;58;267–71.
endoscopic video capsule as first intestinal investigation in 20. Keizman D, Brill S, Umansky M, et al. Diagnostic yield
patients with obscure digestive bleeding: Validation of a di- of routine push enteroscopy with a graded-stiffness entero-
agnostic strategy based on patient’s outcome at 12 months. scope without overtube. Gastrointest Endosc 2003;57:877–
Endoscopy 2004;36:1067–73. 81.
3. Pennazio M, Santucci R, Rondonotti E, et al. Outcome of 21. Yang R, Laine L. Mucosal stripping: A complication of push
patients with obscure gastrointestinal bleeding after capsule enteroscopy. Gastrointest Endosc 1995;41:156–8.
endoscopy: Report of 100 consecutive cases. Gastroenterol- 22. Barkin J, Lewis B, Reiner D. Diagnostic and therapeutic
ogy 2004;126:643–53. jejunoscopy with a new, longer enteroscope. Gastrointest
4. May A, Wardak A, Nachbar L, et al. Influence of patient Endosc 1992;38:55–8.
selection on the outcome of capsule endoscopy in patients 23. Linder J, Cheruvattath R, Truss C, et al. Diagnostic yield
with chronic gastrointestinal bleeding. J Clin Gastroenterol and clinical implication of push enteroscopy: Results from
2005;39:684–8. a nonspecialized center. J Clin Gastroenterol 2002;35:383–
5. Hartmann D, Schmidt H, Bolz G, et al. A prospective two- 6.
center study comparing wireless capsule endoscopy with in- 24. Parry SD, Welfare MR, Cobden I, et al. Push enteroscopy
traoperative enteroscopy in patients with obscure GI bleed- in a UK district general hospital: Experience in 51 cases
ing. Gastrointest Endosc 2005;61:826–32. over 2 years. Eur J Gastroenterol Hepatol 2002;14:305–
6. Benz C, Jakobs R, Riemann JF. Do we need the overtube 9.
for push enteroscopy? Endoscopy 2001;33:658–61. 25. Taylor AC, Buttigieg RJ, McDonald IG, et al. Prospective as-
7. Taylor AC, Chen RY, Desmond PV. Use of an overtube for sessment of the diagnostic and therapeutic impact of small-
enteroscopy: Does it increase depth of insertion? A prospec- bowel push enteroscopy. Endoscopy 2003;35:951–6.
tive study of enteroscopy with and without an overtube. En- 26. Saurin JC, Delvaux M, Gaudin JL, et al. Diagnostic value
doscopy 2001;33:227–30. of endoscopic capsule in patients with obscure digestive
8. Yamamoto H, Sekine Y, Sato Y, et al. Total enteroscopy with bleeding: Blinded comparison with video push-enteroscopy.
a nonsurgical steerable double-balloon method. Gastrointest Endoscopy 2003;35:576–84.
Endosc 2001;53:216–20. 27. Mylonaki M, Fritscher-Ravens A, Swain P. Wireless capsule
9. May A, Nachbar L, Wardak A, et al. Double-balloon en- endoscopy: A comparison with push enteroscopy in patients
teroscopy: Preliminary experience in patients with obscure with gastroscopy and colonoscopy negative gastrointestinal
gastrointestinal bleeding or chronic abdominal pain. En- bleeding. Gut 2003;52:1122–6.
doscopy 2003;35:985–91. 28. Lewis BS, Swain P. Capsule endoscopy in the evaluation of
10. Landi B, Cellier C, Fayemendy L, et al. Duodenal perfora- patients with suspected small intestinal bleeding: Results of
tion occurring during push enteroscopy [letter]. Gastrointest a pilot study. Gastrointest Endosc 2002;56:349–53.
Endosc 1996;43:631. 29. Douard R, Wind P, Panis Y, et al. Intraoperative enteroscopy
11. Barkin J, Lewis B, Reiner D, et al. Diagnostic and therapeu- for diagnosis and management of unexplained gastrointesti-
tic jejunostomy with a new, longer enteroscope. Gastrointest nal bleeding. Am J Surg 2000;180:181–4.
Endosc 1992;38:55–8. 30. Desa LA, Ohri SK, Hutton KA, et al. Role of intraoperative
12. May A, Nachbar L, Schneider M, et al. Push-and-pull enteroscopy in obscure gastrointestinal bleeding of small
enteroscopy using the double-balloon technique: Method bowel origin. Br J Surg 1991;78:192–5.
of assessing depth of insertion and training of the en- 31. Lewis BS, Wenger JS, Waye JD. Small bowel enteroscopy
teroscopy technique using the Erlangen endo-trainer. En- and intraoperative enteroscopy for obscure gastrointestinal
doscopy 2005;37:66–70. bleeding. Am J Gastroenterol 1991;86:171–4.
2024 May et al.

32. Lau WY, Fan ST, Chu KW, et al. Intra-operative fibreoptic
enteroscopy for bleeding lesions in the small intestine. Br J CONFLICT OF INTEREST
Surg 1986;73:217–8.
33. Ress AM, Benacci JC, Sarr MG. Efficacy of intraoperative Financial support: The authors received financial support
enteroscopy in diagnosis and prevention of recurrent, occult from Fujinon for the PPE workshops.
gastrointestinal bleeding. Am J Surg 1992;163:94–8.

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