How to Perform an Intraoperative Enteroscopy

IOE associates abdominal exploration and intraoperative enteroscopy itself. The challenging question is whether to perform IOE when abdominal exploration discovered a potential cause for GI bleeding. On one hand, abdominal exploration is a good occasion to perform a complete exploration of small bowel by an IOE. On the other hand, when a cause for GI bleeding has been potentially localized during the abdominal exploration, a subsequent negative IOE carries the risks of morbidity due to distension of the mesentery.

Abdominal exploration is usually performed via midline laparotomy even though the laparoscopic approach has been reported in case reports and small series. The former history of abdominal surgery has to be taken into account when an IOE is indicated. Complete adhesiolysis must first be performed carefully to avoid creating iatrogenic lesions during enteroscopy, which could be mistaken for bleeding lesions at endoscopy. A complete surgical exploration of the abdomen is mandatory to exclude macroscopic abnormalities. It includes the exploration of the stomach, duodenum, and the entire length of the large and small intestines using the transillumination technique. When macroscopic lesions are found, the surgeon has to evaluate the probability of whether these lesions are causing GI bleeding and to decide whether to perform IOE.

After the complete surgical exploration, IOE itself has to be prepared. IOE can be performed using the peroral technique, the transanal technique, one or more enterotomies, or combined techniques ( Fig. 1 ; see Table 2 ). Standard enteroscopy with or without overtube might be preferred instead of use of an adult colonoscope because the enteroscope is thinner and probably less traumatic for the small bowel. CO ₂ insufflation during endoscopic procedure instead of air insufflation is also recommended to avoid too much intestinal wall distension. When peroral technique is considered, the Kocher maneuver is recommended to divide the hepatoduodenal ligament and separate the head of the pancreas from the right retroperitoneum. Then, mobilization of the duodenojejunal junction, that is, division of the ligament of Treitz, has also to be performed. When the transanal approach is considered, the extended mobilization of the colon (ie, ileocecal junction, right colon, and hepatic flexure mobilization) is recommended.

View of the different approaches that may be combined to perform an intraoperative enteroscopy. ( A ) Transoral approach. ( B ) Transanal approach. ( C ) Enterotomy approach to explore the proximal small bowel, for example, when an additional enterotomy is performed to complete a transanal approach. ( D ) Enterotomy approach to explore the distal small bowel, for example, when an additional enterotomy is performed to complete a transoral approach. When an exclusive enterotomy approach is used, ( C ) and ( D ) are combined. ( Asterisk ) The endoscope is introduced in a mid-small bowel enterotomy through a sterile laparoscopic plastic sheath temporarily sutured to the borders of the enterotomy. The black arrow represents the direction of endoscope insertion.

( From Bonnet S, Douard R, Malamut G, et al. Intraoperative enteroscopy in the management of obscure gastrointestinal bleeding. Dig Liver Dis 2013;45:281; with permission.)

The transoral approach is the least invasive procedure, but it is often difficult to reach the terminal ileum. In these cases, another approach is needed, either an enterotomy or a transanal approach. The advantage of combining the transoral and the transanal approach when the transoral approach only does not allow access to the terminal ileum, is that performing an enterotomy during surgery can be avoided. In return, this combined approach is time consuming and could generate a large distension of the small bowel and the colon, which may lead to difficulties in closing the abdominal wall. To avoid these difficulties, an enterotomy can be conducted to explore the previously unexplored small bowel during the transoral approach.

The systematic enterotomy approach is currently used in laparoscopically assisted IOE. The question of whether to perform an enterotomy only for complete small bowel exploration is a rare event. In most cases, the great part of the small bowel has been explored by the peroral approach, and some lesions have been marked for further small bowel resection. These resection sites can be used as enterotomies for complete small bowel exploration. In some rare cases, when IOE by peroral approach is negative, the transanal approach could be used to avoid the risks for an enterotomy but with the problems of major intestinal and colonic distension.

The transoral approach starts by the introduction of the enteroscope in the duodenum through the pylorus under visual control and manual guidance. It is then guided by the surgeon through the third and fourth portions of duodenum until it crosses the duodenojejunal flexure.

For some investigators, it is best to perform this step of the procedure before completion of the midline laparotomy because the adhesions facilitate the passage of enteroscope through the duodenum. The critical point of this step in the procedure is then to avoid an intragastric loop, which is possible by using an overtube to prevent the endoscope from curving along the great curvature of the stomach.

When the transoral approach does not allow exploration of the last portion of the small bowel, endoscopists can combine this approach with the transanal approach or with use of intraoperative enterotomy performed by the surgeon.

Several technical refinements have been described to minimalize intraoperative contamination, such as a circular suture surrounding the bowel, the use of a sterile laparoscopic plastic sheath that is temporarily sutured to the borders of the enterotomy, or the use of a laparoscopic 15-mm trocart to introduce the endoscope through the enterotomy. This approach divides the small bowel into 2 shorter segments. The insertion and removal of the endoscope is performed by a surgeon, with other maneuvers usually performed by an endoscopist.

During intraoperative enteroscopy, the small bowel has to be explored completely to avoid missing some lesions. For this purpose, a dual examination is performed, both internally and directly by the endoscopist through the enteroscope, but also externally by the surgeon with the transilluminated bowel. In the literature and in the authors’ experience, insufflation is performed using the nonsterile air of the operating room. For optimal small bowel mucosa visualization, the “air-trapping” technique is the most suitable and consists of pinching a segment of the bowel with fingers to trap sufficient air to keep the lumen open. This technique minimizes mucosal trauma and avoids the use of traumatic clamps and excessive insufflations. Noncrushing occluding clamps can be used and positioned at the ileocecal valve and the duodenojejunal junction, but the authors do not use them due to the risks of intestinal damage. Once a segment has been examined, it is pleated over the endoscope, and the next part of the intestine segment can be examined. This procedure is repeated throughout the entire small bowel, and the surgeon manually advances the endoscope by telescoping the bowel over the tip.

Unlike a colonoscopy, it is essential that the intestinal mucosa be explored during the progression of the enteroscope and not during its withdrawal. Indeed, the progression of the enteroscope, even with the specific “air-trapping” technique described above, may cause trauma of the intestinal mucosa, which may then be considered a vascular lesion during withdrawal of the enteroscope. Lesions identified during intraoperative enteroscopy are then marked with suture stitches on the serosal surface of the small bowel to locate the sites of future segmental resection if endoscopic treatment is unsuitable. Then, careful exsufflation is performed.

Complete enteroscopy depends on several factors, such as the experience of the team or surgical constraints. However, the feasibility rate of complete enteroscopy has been reported to range from 57% to 100%.

Diagnostic and Therapeutic Yield of Intraoperative Enteroscopy in the Management of Obscure Gastrointestinal Bleeding

The literature search identified 16 publications in which intraoperative enteroscopy was assessed. In, total, 468 patients who underwent intraoperative enteroscopy were included. According to the previously published data (see Table 2 ), a site-specific source of bleeding was detected in 371 patients (79.27%), confirming that the source of bleeding in OGIB is often located in the small bowel. The predominant lesions responsible for OGIB and identified by IOE were vascular lesions, which represented 61% (n = 227) of findings, as described previously. The remaining lesion types were as follows: benign ulcers in 19% (n = 70), tumors in 10% (n = 36), and diverticula in 4.0% (n = 15).

Endoscopic or histologic data that distinguished the different types of vascular lesions (ie, angiodysplasias, arteriovenous malformation) were lacking in the published studies. In the case of small bowel resection, histologic confirmation of vascular lesions cannot be regularly obtained. Diagnosis is then usually endoscopic and, therefore, uncertain. Final pathologic examination confirmed the vascular lesions visualized during IOE in 62% to 100% of cases. The complete list of intraoperative findings is summarized in Table 1 .

In addition to identifying hemorrhagic lesions, IOE allowed treatment in 74.1% of patients. The treatment was mainly surgery in the older studies and then was gradually superseded by endoscopic management alone or combined with surgery, as reported in Table 2 .

These results were observed with the vascular lesions for which the proportions of surgical and endoscopic treatments were reversed between the first and last studies. Indeed, surgical resection of vascular lesions decreased from 96% of cases for the first studies to 12.5% of cases for the more recent studies, whereas endoscopic treatment alone increased from 2% of cases to 54.2% of cases, and combined endoscopic and surgical treatments increased from 2% of cases to 33.3% of cases. The ability of IOE to identify bleeding lesions is good and has been shown to be equal to the VCE diagnostic yield with a higher sensitivity than push-pull enteroscopy.

However, diagnostic yield of the IOE, comparable to noninvasive explorations, does not mean that IOE has to be used as a diagnostic tool. When the bleeding site has not been formally preoperatively localized in the small bowel, IOE might be negative and/or bleeding sites may be discovered outside the small bowel. For these reasons, some investigators decided to avoid IOE when a bleeding site has not been shown preoperatively in the small bowel. IOE has to be used to complete preoperative exploration, not to replace it.

Recurrent Gastrointestinal Bleeding

Recurrence of bleeding after IOE for obscure GI bleeding is reported in 13% to 52% of the cases (see Table 2 ). The yearly bleeding recurrence rate, which is calculated from p = 1 − e(−rt), in which r is the rate and t is the time, ranged from 12% to 60%. This high rate is due to the predominance of vascular lesions in the causes of obscure GI bleeding and high rate of recurrence associated with these lesions.

These lesions are difficult to identify endoscopically because of possible confusion with lesions induced by endoscopy itself, as reported by Douard and colleagues. In addition, part of rebleeding may be explained by the evanescence of these vascular lesions as mentioned by Gerson, leading some investigators to propose an early deep enteroscopy exploration after OGIB. Hartmann and colleagues reported a recurrence rate of 26% after IOE with a single long-term follow-up. This high recurrence rate could be related to (i) the development of new lesions, (ii) the bleeding of missed lesions in the small bowel or other parts of the GI tract, and (iii) the real recurrence of the treated lesions.

This high rebleeding rate is in favor of endoscopic treatment of lesions identified during IOE in order to avoid the morbidity of surgical resection of small bowel with acceptable efficiency. Thus, the endoscopic treatment of angiodysplasia has been shown to reduce blood loss over long-term follow-up. However, these results are disputed by some investigators who did not find any difference between endoscopic treatment and no treatment. These therapeutic difficulties are especially present in elderly individuals with cardiovascular risks who are treated with antiaggregating medications and have higher risks for vascular lesions and bleeding. Nevertheless, the choice between surgical or endoscopic treatments remains debatable. In the authors’ experience, the high recurrence rate of angiodysplasia that is endoscopically treated during IOE suggests that surgical resection of angiodysplasia could be proposed when a bleeding site has been clearly identified for localized lesions that are only reachable under IOE guidance. In such cases, a recurrence at the same bleeding site would necessitate a second IOE to guide re-treatment.

What Is the Morbidity and Mortality of Intraoperative Enteroscopy?

IOE is associated with high morbidity and mortality, which has to be taken into account before proposing such technique. Morbidities of 1% to 50% have been reported in the literature (see Table 2 ). In studies with available data (11 studies that included 328 patients), overall morbidity affects 18% (n = 60) of the patients, including surgical morbidity, 12.5% (n = 41), and medical morbidity, 4.6% (n = 15).

The main causes of surgical morbidity are listed in Table 3 and classified into 3 categories: mechanical causes, infectious causes, and hemorrhagic causes. Among these complications, the most common complication is postoperative ileus that was found in 20 patients (49% of all complications). The observed medical complications were pneumonia (n = 5), heart complications (n = 8), pulmonary embolism (n = 1), and azotemia (n = 1).

Mortality related to the procedure or to postoperative complications has been as high as 18% in some of the studies (see Table 2 ). Analysis of the 15 studies with available data (including 438 patients) showed an overall mortality associated with IOE of 5% (n = 22), which appears to be primarily related to multisystem organ failure with GI bleeding recurrence and septic causes ( Table 4 ). Among the 15 series of significant size and using IOE, there were no laparoscopic series even if laparoscopic series of IOE have been published for other indications.

What Is the Remaining Role of Intraoperative Enteroscopy in the Exploration of Obscure Gastrointestinal Bleeding?

IOE has long been the only technical exploration of the entire small intestine available, especially in cases of digestive occult bleeding. However, due to its high morbidity and mortality, IOE has been gradually replaced by less invasive exploration techniques and/or procedures associated with less morbidity. Among these new techniques, VCE is the least invasive method to explore the entire small bowel and to diagnose hemorrhagic lesions with good accuracy. Thus, in a prospective study that compares VCE and IOE, the sensitivity and specificity of VCE were 95% and 75%, respectively, with positive and negative predictive values of 95% and 86%, respectively. Because of these results, many guidelines recommend performing a VCE as an initial diagnostic test in cases of OGIB after negative upper endoscopy and colonoscopy. However, 20% tumor miss rates and incomplete small bowel visualization rates have been reported with VCE, in addition to other limitations, such as no maneuverability, no therapeutic capabilities, and the risk of retention by strictures.

New techniques of enteroscopy were also developed in order to explore more consistently and specifically all of the parts of the small bowel with the opportunity to combine therapeutic procedure with diagnostic procedure. These techniques include balloon-assisted endoscopy using either 2 balloons (double-balloon enteroscopy), 1 balloon (single-balloon enteroscopy), or balloon-guided enteroscopy and spiral enteroscopy. Compared with single enteroscopy (named also push enteroscopy), the double-balloon enteroscopy technique increases the length of procedure and diagnostic yield. Double-balloon enteroscopy allows visualization of the entire small bowel in 40% to 80% of cases and appears to be superior to the simple enteroscopy that allows a complete visualization of the small bowel in only 5% to 25% of cases. Spiral enteroscopy has recently been described and could reduce the examination time. However, more experience is needed to confirm the safety and potential superiority of spiral enteroscopy to single-balloon enteroscopy. Comparative studies between deep enteroscopy techniques are scarce. Double-balloon enteroscopy appears to allow more bowel to be visualized compared with single-balloon enteroscopy and at least as much as spiral enteroscopy. Moreover, it has been shown that VCE and double-balloon enteroscopy provide similar diagnostic yield results in small bowel disease, including OGIB.

Following all of these publications, it is clear that the VCE and balloon-assisted endoscopy have supplanted simple enteroscopy as first-line exploration method for occult GI bleeding. In addition, balloon-assisted enteroscopy (with 1 or 2 balloons) allows combination of therapeutic treatment with diagnostic exploration. The negative predictive value of these techniques is so high that some investigators recommend repeating conventional upper endoscopy and colonoscopy in the case of negativity of VCE or balloon-assisted endoscopy. This recommendation is supported by cases of gastric Dieulafoy lesions that had been missed in the preoperative endoscopic workup before IOE. When the small bowel lesion cannot be treated during deep enteroscopy, tattoo marks have been proposed to guide surgical treatment. Consequently, IOE is avoided as a first-line localization tool.

In parallel with the development of endoscopic techniques, vascular and radiological studies have evolved to provide additional information in the preoperative staging of occult GI bleeding. Therefore, although endoscopic explorations reveal potential mucosal lesions, contrast studies have low sensitivity to these same lesions such as small angiodysplasia. On the contrary, these techniques of vascular explorations have a high sensitivity to the parietal lesions, such as stenosis caused by inflammatory bowel diseases or neoplasms, which can be surgically treated without any preoperative endoscopic exploration.

Small bowel follow-through has now been superseded by computed tomography enterography, and more recently, by magnetic resonance enterography (MRE) in these indications. Vascular explorations, such as computed tomography angiography and angiography, are used to assess vascular lesions, such as angiodysplasia, that are frequently reported in obscure GI bleeding. Computed tomography angiography and angiography are good methods of locating the bleeding site during an active hemorrhage. In this indication, computed tomography angiography is the first-line examination and could guide a subsequent selective conventional angiography to perform selective embolization. Provocative testing has been recently proposed to increase the diagnostic yield of endoscopic and/or angiographic explorations, but data are lacking on the risks and benefits.

The diagnostic and therapeutic management for OGIB depends on both hemodynamic impact of this bleeding, but also the expertise of endoscopists, radiologists, surgeons, and interventional radiologists of the hospital where the patient is located. Because of the high negative predictive value of deep enteroscopy and/or VCE in the localizing bleeding lesions in the small bowel, the authors think that IOE has to be avoided as a diagnostic tool in the evaluation of obscure GI bleeding.

Nevertheless, apart from obscure GI bleeding exploration, IOE seems to keep a wide indication in inherited polyposis syndromes such as familial adenomatous polyposis (FAP) and Peutz-Jeghers syndrome (PJS).

In the FAP, the reference examination for the proximal small bowel is the conventional forward-viewing and side-viewing endoscopy due to the high cumulative risk of severe duodenal polyposis and high relative risk of duodenal cancer. Nevertheless, jejunal and ileal polyps can be also found in 40% to 70% of FAP patients, specifically in patients with severe duodenal polyposis. In these cases, VCE has demonstrated higher sensitivity to diagnose jejunal and ileal polyp than radiological investigation, and studies comparing push-enteroscopy with VCE have shown conflicting results. However, when a polyp larger than 1 cm is identified by VCE or radiological investigation, an enteroscopy is indicated to obtain targeted biopsies and accomplish endoscopic polypectomy.

Similarly, in PJS patients, there is a high risk of polyp-burden and polyp-related complications, such as intussusception and occult hemorrhage requiring small-bowel surveillance and large polyp resection. In these cases, radiological examinations such as MRE are recommended as first line for small bowel surveillance in order to limit the risk of obstruction by VCE in large polyps. MRE was also shown to be less prone to missing large polyps than VCE. When large polyps (>10–15 mm) are discovered by radiological examination, an enteroscopy with polypectomy is required.

In FAP and PJS, the choice for the type of enteroscopy is especially guided by patient’s surgical history. An IOE will be preferred in patients with FAP in whom a Whipple procedure with a Roux-en-Y anastomosis has been performed. Similarly, in FAP or PJS, completeness of small bowel investigation by balloon-assisted enteroscopy may be compromised by previous laparotomies due to multiple adhesions, and IOE will then be preferred. IOE has been demonstrated to enhance small bowel clearance and to reduce the number of laparotomies.

Overall, when noninvasive techniques are unavailable, are unable to explore the entire small bowel, or have conflicting results, IOE may still have a place. However, IOE may be used to guide surgical or endoscopic treatment when small bowel lesions have been demonstrated preoperatively. In the authors’ opinion, IOE remains indicated in some cases when small bowel lesions (i) have been identified by a preoperative workup (VCE, balloon-assisted endoscopy, and/or other explorations such as angiography), (ii) cannot be definitively managed by angiographic embolization or endoscopic treatment with deep enteroscopy or when surgery is required for other reasons, and (iii) cannot be localized during surgical explorations (ie, no serosal visible lesion and/or no previous tattoo) ( Fig. 2 ). In such conditions, IOE allows intraoperative localization of preoperatively determined lesions and appropriate concomitant treatment. For certain indications, laparoscopic-assisted IOE might be proposed to reduce the morbidity of conventional procedures.

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