Push-and-pull enteroscopy using the double-balloon technique/double-balloon enteroscopy
Article Outline
- Abstract
- 1. Technique of PPE/DBE
- 2. Clinical results
- 3. Indications for PPE/DBE
- 4. Conclusion
- Conflict of interest statement
- References
- Copyright
Abstract
Push-and-Pull enteroscopy/Double balloon enteroscopy (PPE/DBE) allows enteroscopy of the entire small bowel, or at least a substantial part of it. The complication rate is acceptably low. Severe complications such as pancreatitis and perforation were encountered in the literature in approximately 1% of all diagnostic PPE/DBEs. It can be expected that the complication rate of therapeutic PPE/DBEs is higher, comparable with the conventional endoscopy. The diagnostic yield is high, at approximately 75%, as is the therapeutic yield. The option of carrying out endoscopic therapy (in approximately 40%–50% of cases in the Western hemisphere) is an important aspect. Angiodysplasias are the main bleeding source, at least in Western countries. Using the PPE/DBE device, endoscopic treatments such as endoscopic hemostasis using injection and argon plasma coagulation, polypectomy, endoscopic resection, balloon dilation, and foreign-body extraction have become feasible even in the small intestine and can generally be performed safely and without relevant technical problems. Medical therapy can be started in up to 20% of cases—e.g., after a new or changed diagnosis of Crohn's disease. Surgical therapy is required in 10–20% of cases, due to malignant tumors or complex stenoses, for example. The main indication is mid-gastrointestinal bleeding.
Until recently, only indirect procedures using radiographic or magnetic resonance techniques (such as conventional and magnetic resonance enteroclysis, and computed tomography) were available to provide imaging of the small bowel. These procedures can be used to detect larger tumours and are mainly helpful for demonstrating stenoses and fistulas—e.g., in patients with Crohn's disease [1]. However, they do not allow direct intraluminal assessment of the mucosa. Radiographic angiography and scintigraphic methods are also unsatisfactory, as they are only able to identify a bleeding source in some 15% of the cases [2]. In the absence of a better standard method, however, they have been widely used in patients with suspected chronic or acute recurrent mid-gastrointestinal (MGI) bleeding—i.e., those with a bleeding source located in the small bowel [3]. During the 1980s, push enteroscopy, with its facilities for direct inspection of the mucosa, biopsy sampling, and treatment became the established endoscopic method for examining the proximal part of the small bowel. Due to technical limitations, however, it is only possible to visualise approximately 60–100
cm of the postpyloric small bowel with this method [4]. Intraoperative enteroscopy was therefore previously the gold standard, providing the highest diagnostic and therapeutic yield in patients with chronic or acute recurrent MGI bleeding; however, it is associated with a substantial risk of complications and mortality [5], [6].
Capsule endoscopy and push-and-pull enteroscopy (PPE) using the double-balloon technique (double-balloon endoscopy, DBE) have revolutionised imaging procedures in the field of small-bowel diagnosis. Capsule endoscopy was introduced into clinical practice in 2001 and made it possible for the first time to visualise intraluminal conditions throughout the entire small bowel. Initial studies comparing capsule endoscopy with traditional diagnostic procedures showed that capsule endoscopy was clearly superior to all of the other procedures in the diagnostic work-up of acute recurrent or chronic MGI bleeding [2], [6], [7], [8], [9]. Nevertheless, capsule endoscopy does have certain limitations. There are no facilities for air insufflation, rinsing of tissue, taking biopsies or carrying out therapeutic interventions. PPE/DBE, which was developed and first reported in 2001 by H. Yamamoto and his group in Japan, followed by our own group in Germany in 2003, made it possible not only to inspect small-bowel diseases, but also to carry out endoscopic therapeutic interventions [10], [11]. Particularly in cases of MGI bleeding, PPE/DBE allows haemostasis to be carried out using argon plasma coagulation or injection procedures, in addition to diagnostic work-up.
The purpose of this technical review is to describe the technique of PPE/DBE and to report the clinical results to date, including indications and complications.
1. Technique of PPE/DBE
1.1. Endoscopic device
The endoscopy system (Fujinon EN-450P5/20; Fujinon Inc., Japan) 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 overtube with a length of 145
cm (including the balloon) and an outer diameter of 12
mm. The endoscope's working channel has a diameter of 2.2
mm.
On the basis of clinical experience showing that passage through the colon with this thin and flexible scope is more time-consuming and requires greater experience than with the standard colonoscope, a second push-and-pull enteroscope (Fujinon EN-450T5; Fujinon Inc., Japan) has been designed, with an outer diameter of 9.5
mm, for the anal route. This enteroscope also has a larger working channel of 2.8
mm, facilitating therapeutic interventions. The diameter of the overtube for this device is 13
mm. There have not yet been any studies comparing the two types, but initial impressions suggest that the larger working channel is genuinely helpful, especially during endoscopic therapeutic interventions such as polypectomy. On the other hand, advancement into the deep small bowel from the oral route appears to be more difficult with the thicker scope. Passage through the colon appears to be easier with the thicker device, but management of the ileal loops in the pelvis may be more difficult.
1.2. Principle of PPE/DBE
Latex balloons are attached at the tip of the endoscope and the overtube, and are inflated and deflated with air from a pressure-controlled pump system [1], [2], which monitors the pressure during the whole procedure and ensures that a maximum of 6
kPa is not exceeded. The endoscope balloons are single-use products and have to be attached to the tip of the endoscope immediately before the examination is started. The balloon on the overtube is fixed to the overtube.
Using either the oral or anal route, the two balloons are deflated at the beginning of the enteroscopy procedure until the duodenum or terminal ileum is reached. The enteroscope is then advanced further as far as possible, while the inflated balloon on the overtube maintains a stable position. In the next step, after deflation of the balloon on the overtube and inflation of the balloon on the enteroscope, the overtube is inserted along the enteroscope until the tip of the enteroscope is reached. After this ‘push’ procedure has been completed, the ‘pull’ procedure begins, during which both the enteroscope and the overtube are pulled back under endoscopic and if necessary fluoroscopic guidance, with both balloons inflated. The ‘push-and-pull’ procedure is then repeated (Fig. 1).

Fig. 1.
Scheme illustrating the principle of PPE/DBE. Yellow: balloon deflated; orange: balloon inflated.
For anal insertion, it is easier to pass through the colon using the push-and-pull technique with balloons. The balloons can be inflated sufficiently to grip the colon wall while advancing through the colon. As the balloons are very elastic and balloon inflation is controlled by pressure instead of air volume, they can be used safely regardless of the intestinal diameter. During passage through the colon, the balloons are usually used several times, ranging from once (at the splenic flexure) up to three times (at the sigmoid-descending colon junction, splenic flexure and hepatic flexure).
With each alternating step of inflation and deflation of the balloons, alternating insertion of the scope and overtube, and pulling back of the endoscope and overtube, up to 40
cm of the small bowel can be visualised before the instrument is advanced further. Using this double-balloon method, looping caused by the forward movement of the endoscope can be reduced to a minimum as the balloon-blocked endoscope and overtube system are pulled back. PPE/DBE can be carried out from the oral or anal route, or both. Total small-bowel enteroscopy can be achieved with the oral route alone only in a minority of patients, particularly when the examination time is limited. Generally, both routes have to be combined to allow total enteroscopy of the small bowel [12], [13]. As experience is gained, total enteroscopy becomes possible in approximately 80% of the patients in whom it is attempted. This is the case in approximately 20–25% of patients who undergo PPE/DBE. In the majority of the patients, the problem can be resolved without the need for a complete enteroscopy—for example, the bleeding source is found, an unclear ulcer or stenosis is identified to allow biopsies to be taken, or a polyp is resected, etc.
It might be possible to increase the success rate with PPE/DBE if laparoscopy were carried out to lyse adhesions in difficult cases in patients who have previously undergone abdominal surgery. However, there are as yet no data to show whether intraoperative enteroscopy would be more effective in these rare cases.
A remarkable feature of PPE/DBE is that it not only provides excellent access to the distal small intestine, but also allows precise control of the endoscope tip in any part of the intestine, since the movement of the endoscope is controlled from the point gripped by the overtube balloon, which can be set anywhere [14]. The diagnostic and therapeutic options provided by this new technique are listed in Table 1.
Table 1. Diagnostic and therapeutic options of PPE/DBE in the small bowel
| Diagnostic options | Therapeutic options |
|---|---|
| High-resolution (HR) video endoscopy | Haemostasis (injection, argon plasma coagulation, clip application) |
| Chromoendoscopy | Polypectomy |
| Biopsy | Endoscopic resection |
| Endoscopic ultrasound with mini probes 15 and 20 | Dilation |
| Selective enteroclysis | Foreign-body extraction |
| Marking with India ink | Implantation of self-expanding enteral metal stents |
No specific preparation is required for the oral approach. Patients should stop eating and drinking in the same way as before upper gastrointestinal endoscopy. For enteroscopy from the anal approach, bowel cleansing is required as in colonoscopy. The examinations can usually be carried out with the patients under conscious sedation, as in colonoscopy and upper gastrointestinal endoscopy—at least in Japan and Europe. Alternatively, sedation with propofol can be administered, especially in young patients undergoing therapeutic interventions—e.g., polypectomies in patients with Peutz–Jeghers syndrome, or in patients in whom it is known that conscious sedation will not ensure satisfactory conditions for a longer endoscopic examination. General anaesthesia is generally not required.
1.3. Measuring the insertion depth during enteroscopy
When the small bowel is being threaded onto the overtube by means of repeated push-and-pull procedures, it is not possible to determine the length of the small bowel that has been visualised, or the location of any pathological findings, without additional assistance. It is therefore necessary to estimate the effective length of insertion of the endoscope by checking the extent to which the instrument has been advanced (the push manoeuvre) and the length of small bowel released during insertion of the overtube and pulling back of the endoscope and overtube (the pull manoeuvre). After each push-and-pull procedure, the endoscopist has to decide whether the advancement was 0, 10, 20, 30, or 40
cm. The amount is noted on a standardised record sheet by the assistant. If pathological findings are seen during enteroscopy, it is possible to locate them by adding up the individual advancement lengths previously noted. At the end of the examination, all of the amounts recorded are added up and the length of small bowel that has been visualised can be estimated.
This measurement technique was evaluated using the Endo-Trainer animal model that is used in enteroscopy training workshops [15]. There is no doubt that the method is highly dependent on the endoscopist's subjective judgment. Particularly in technically difficult procedures or in the deep small bowel (>300
cm), it is quite difficult to obtain an accurate assessment of the insertion depth.
2. Clinical results
Results with PPE/DBE that have been published in original papers are listed in Table 2 [12], [13], [16], [17]. On average, approximately 250
cm is visualised via the oral route and 130
cm via the anal route, with a mean examination time of 75
min. Radiographic exposure time includes selective enteroclysis and imaging for endoscopic therapy such as dilation of Crohn's stenoses. With experience, the radiographic exposure time during diagnostic PPE/DBE in our unit is now generally less than 1
min. Total enteroscopy is not required in the majority of the patients (75–80%), as the purpose of the examination – e.g., identification and treatment of the potential bleeding source – can be attained without it. However, if total enteroscopy is necessary, it can be achieved in 60–86% of cases, depending on the endoscopist's level of experience [12], [13].
Table 2. Results of published clinical studies of PPE/DBE
| Japanese retrospective (Ref. [12]) | Wiesbaden prospective (Ref. [13]) | European retrospective (Ref. [16]) | European prospective (Ref. [17]) | Netherlands prospective (Ref. [20]) | |
|---|---|---|---|---|---|
| Patients (n) | 123 | 137 | 62 | 100 | 275 |
| PPE/DBE procedures (n) | 178 | 248 | 89 | 147 | 316 |
| Main indication | MGI | MGI | MGI | MGI | MGI |
| Insertion depth (cm) | |||||
| No data | 240 | 250 | 220 | 270 | |
| No data | 140 | 180 | 130 | 150 | |
| Radiography exposure | |||||
| No data | 3.6 | No data | 2.1 | 4 | |
| No data | 236 | No data | 155 | No data | |
| Preferred route | Anal | Oral | Oral | Oral | Oral |
| Major PPE-associated complications (%, n/∑) | 1.6% (2/123) | None | None | None | 1.1% (3/275) |
| 1.1% (2/178) | (1/100 propofol-associated) | (1/100 propofol-associated) | |||
| Diagnostic yield | 76% | 79% | 80% | 72% | 73% (MGI) |
| Therapeutic yield | No data | 76% | No data | 62% | No data |
| 20% | 41.5% | 42% | 42% | 55% (MGI) | |
| No data | 20% | No data | 12% | No data | |
| No data | 17.5% | No data | 8% | No data | |
Adhesions due to prior abdominal surgery are a limitation in PPE/DBE. Severe complications such as perforation were reported by Yamamoto et al. [12] in two cases out of 178 PPE/DBE procedures (1.1%). However, surgical treatment was only required in one of the patients, in whom the perforation turned out to be due to necrosis from a malignant lymphoma after chemotherapy. In the other patient, possible mesenteric penetration by an ileal ulcer in Crohn's disease after PPE/DBE caused abdominal pain and fever, which was managed conservatively. These cases suggest that the indication for enteroscopy should be evaluated carefully before the procedure, and when fragile lesions such as deep acute ulcerations in the small intestine are observed, further insertion of the endoscope across the lesion should be avoided [12]. A case of paralytic intestinal ileus was recently reported after PPE/DBE with argon plasma coagulation of angiodysplasias, which was managed conservatively. It remained unclear whether the therapeutic intervention played a role in this complication, or whether the technique of threading the small bowel was the main factor [18]. No severe complications apart from one associated with propofol occurred in the larger European series [16], [17]. However, as in conventional endoscopy, complications can be expected to occur, especially during or after therapeutic interventions—e.g., after polypectomy, as was recently described in a case report [19].
The diagnostic yield is high at approximately 75%, but it should be borne in mind that there is strong selection of the patients in the published reports. The same also applies to the high therapeutic yield. Endoscopic therapy is an important aspect of PPE/DBE, and angiodysplasias have been found to be the main source of bleeding, at least in Western countries (Fig. 2). Using the PPE/DBE system, endoscopic treatments such as endoscopic haemostasis using injection and argon plasma coagulation, polypectomy, endoscopic resection, balloon dilation and stent placement have become feasible even in the small intestine [12], [13]. Medical therapy is started in up to 20% of cases—e.g., after a new diagnosis of a Crohn's disease (Fig. 3). Surgical therapy, due to malignant tumours (Fig. 4) or complex stenoses, for example, is required in 10–20% of cases.
2.1. Pancreatitis
Complications involving cases of pancreatitis in Germany, the Netherlands and Japan have been reported in published cases [20], [21] and in personal information provided to the authors, and these should be noted; however, conservative treatment was possible in all of these cases. The risk is estimated at 1%. The aetiology of the pancreatitis is still unclear. Occlusion of the papilla caused by the balloon on the overtube does not appear to be very plausible as a cause of the pancreatitis, since the inflation and deflation of the balloon are carried out very quickly. However, to reduce the risk, we always inflate the overtube balloon once the overtube has passed the papilla. Duodenal reflux into the pancreatic duct caused by duodenal hypertension has also been discussed as a possible cause [21]. Another hypothesis is that traumatic injury or ischaemia may play a role when the small bowel is threaded together onto the overtube, with removal of the loops possibly exerting some torsion on parts of the mesentery. The length of the examination time may also be an important factor. In our own series, now including more than 500 examinations, there have been no cases of pancreatitis and we have a strict limitation of up to 2
h on the examination time. However, the aetiology of pancreatitis after PPE/DBE is not as yet clear.
2.2. Comparison of PPE/DBE with push enteroscopy and capsule endoscopy
With regard to comparisons between push enteroscopy and PPE/DBE, a controlled prospective trial found that oral PPE was superior to push enteroscopy in terms of insertion depth and detection of pathological lesions [22].
Studies in France, Japan and the Netherlands published as full papers provide initial information on the comparative value of capsule endoscopy and PPE [23], [24], [25]. In the study by Gay et al. [23], capsule endoscopy was used as a method of selecting patients capable of benefiting from PPE. The positive predictive value (PPV) of capsule endoscopy for indicating PPE was 95%, with a negative predictive value (NPV) as high as 98%. In the small study by Nakamura et al. [24], the diagnostic yield of capsule endoscopy was found to be significantly higher than that of PPE. This was probably because a complete endoscopic examination of the entire small bowel was only possible in just under two-thirds of the patients. These data were confirmed by the study in the Netherlands, in which capsule endoscopy also showed a higher diagnostic yield than PPE/DBE (80% versus 60%) [25]. However, the authors discuss the possibility that pathologic findings seen with the capsule can in some cases not be confirmed either with PPE/DBE or even with intraoperative endoscopy, so that overestimation of pathologic findings may sometimes occur. These three studies provide further support for an approach using capsule endoscopy as a diagnostic procedure to select patients for PPE, at least in patients with MGI. Further prospective and controlled studies are undoubtedly necessary to establish the value of capsule endoscopy and PPE in the diagnostic settings of different small-bowel diseases.
3. Indications for PPE/DBE
Clear and possible indications are listed in Table 3. On the basis of the published papers, the main indication is the acute recurrent or chronic MGI bleeding. The main advantage of PPE/DBE in comparison with capsule endoscopy is that it makes it possible to carry out endoscopic therapeutic interventions and take biopsies. Capsule endoscopy may be helpful for selecting the patients and the primary route (oral or anal) for PPE/DBE [26]. However, the more evident the bleeding is, the more it would make sense to carry out PPE/DBE without prior capsule endoscopy.
Table 3. Clear and possible indications
| Small-bowel endoscopy | |
| Mid-gastrointestinal bleeding (MGI) | |
| Crohn's disease | |
| Polyposis syndromes | |
| Malabsorption, chronic iron-deficiency anaemia | |
| Coeliac disease (refractory) | |
| Outside the small bowel | |
| Difficult ileocolonoscopy | |
| ERCP after stomach resection (Billroth II, Roux-en-Y) | |
| ERCP after biliodigestive anastomosis | |
Another possible indication is Crohn's disease in the small bowel. There have been some studies showing that capsule endoscopy is useful for evaluating the small bowel in patients with suspected or known Crohn's disease [1], [27], [28]. However, due to the risk of capsule retention because of unknown strictures, PPE/DBE appears to be superior to the capsule for this indication. In addition, biopsies can be taken with PPE/DBE, allowing histological classification to exclude malignant lesions. If inflammatory Crohn's disease is found, medical treatment can be started or changed. In patients with a short, scarred stenosis, dilation therapy can be carried out [29]. There is still a lack of the comparative studies that are necessary here.
With regard to polyposis syndromes, capsule endoscopy can in our opinion help select patients for PPE/DBE, as the capsule has a high diagnostic yield for detecting small-bowel polyps [30], [31], [32], [33] and can therefore be useful for polypectomy planning, depending on the number and diameter of the polyps. On the basis of their data, Matsumoto et al. [34] prefer PPE/DBE in patients with polyposis, since more polyps were found with PPE/DBE. Generally, however, total enteroscopy is very difficult to achieve in the majority of this group of patients, who often have several previous abdominal operations in their medical history. In our opinion, capsule endoscopy is therefore ideal for completing the diagnostic work-up of the small bowel in these patients. Again, however, larger prospective and controlled series are still missing.
With regard to small-bowel diseases, any type of malabsorption, chronic iron-deficiency anaemia, refractory coeliac disease, etc. is likely to become an indication for PPE/DBE, particularly in view of the option of taking biopsy samples.
Future indications may include difficult ileocolonoscopy in patients in whom standard colonoscopy and even colonoscopy with the paediatric colonoscope have failed [12], [35], [36]. Another highly attractive group would be patients requiring endoscopic retrograde cholangiopancreatography (ERCP) after previous gastric resections (with Billroth II or Roux-en-Y procedures) or after biliodigestive anastomoses. Up to the present, however, only case reports are available suggesting the potential of the new technique for this indication [12], [37]. The same applies to the use of PPE/DBE for regions of the gastrointestinal tract that were formerly inaccessible endoscopically due to altered anatomy after previous surgery [38], [39]. Larger series are still lacking.
4. Conclusion
In summary, PPE allows enteroscopy of the entire small bowel, or at least a substantial part of it. The complication rate is acceptably low. The diagnostic yield is high, at approximately 75%, as is the therapeutic yield. The option of carrying out endoscopic therapy (in approximately 40% of cases in the Western hemisphere) is an important aspect. Angiodysplasias are the main bleeding source, at least in Western countries. Using the PPE device, endoscopic treatments such as endoscopic haemostasis using injection and argon plasma coagulation, polypectomy, endoscopic resection, balloon dilation and foreign-body extraction have become feasible even in the small intestine. Medical therapy can be started in up to 20% of cases—e.g., after a new or changed diagnosis of Crohn's disease. Surgical therapy is required in 10–20% of cases, due to malignant tumours or complex stenoses, for example. The main indication is MGI bleeding.
Conflict of interest statement
None declared.
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PII: S1590-8658(06)00420-8
doi:10.1016/j.dld.2006.07.101
© 2006 Editrice Gastroenterologica Italiana S.r.l. Published by Elsevier Inc All rights reserved.



