Dra. Begoña González Suárez
Hospital Universitari Clínic. Barcelona
ENTEROSCOPY IN THE DIAGNOSIS OF CROHN’S DISEASE
Crohn’s disease (CD) is an inflammatory disease with transmural involvement that can damage the entire intestinal tract. The small intestine (SI) is involved in 70% of patients, in most cases (30–40%) in the terminal ileum, which can be diagnosed by ileocolonoscopy. However, in 10% of patients, only the jejunal loops and/or proximal ileum are involved, which can significantly delay diagnosis if appropriate techniques are not available. Ileoscopy can only examine the last few centimetres of the terminal ileum, and push enteroscopy is also limited in its reach of the proximal jejunal loops1. The rest of the SI was examined using conventional radiological techniques such as bowel transit. The appearance of capsule endoscopy (CE, 2001) and balloon enteroscopy (BE, 2004) has constituted a significant advance in the study and treatment of the SI. In parallel, more novel radiological examinations, such as computed enterotomography (CT enterography) and resonance enterography, are also available to help us assess the SI2.
CE is a non-invasive examination that allows us to explore the SI in its entirety in 90% of cases, but one of its main limitations is the inability to take biopsies that could confirm a diagnosis3. The great advantage of enteroscopy over CE is that it allows us to directly observe the lesion, take a sample for histological diagnosis and perform a therapeutic intervention. Therefore, as we will see below, both CE and enteroscopy are complementary techniques, not just in this sense, but also because capsule endoscopy will be a key pre-enteroscopy examination indicating the route of access to reach a specific lesion4.
There is not yet sufficient evidence to recommend performing an enteroscopy to diagnose and study the extention of CD, unless the endoscopic and radiological studies are inconclusive or a therapeutic intervention (dilatation, extraction of a foreign body, treatment for bleeding lesions) must be performed. Enteroscopy is also indicated for evaluation of atypical lesions observed by capsule or with radiological techniques, taking biopsies for cases of suspected CD or verification of mucosal healing if CE is contraindicated (Table I)4,5. It must also be considered that not all ulcerous lesions in the SI are secondary to CD, so if lesions of this type are found, it is very important to evaluate the patient’s clinical symptoms and laboratory data on acute-phase reactants. The chronic use of non-steroidal anti-inflammatory drugs can cause ulcerative intestinal lesions that are indistinguishable from CD ulcers, and the same is true of intestinal lymphoma, complicated coeliac disease or radiation enteritis, among other conditions.
We know that SI involvement in CD patients is an independent risk factor for poor prognosis, and these patients often require intensified medical treatment or even surgery6-8. In recent years, numerous publications have emphasised the role of capsule or enteroscopic study of the SI in CD patients, as well as finding a greater incidence of intestinal lesions than previously reported, between 50 and 90%9,10.
Kondo et al. performed double-balloon enteroscopy (DBE) on 75 CD patients, 25 of whom had been recently diagnosed. Indications for the test included bleeding of unknown origin, clinical obstruction, abdominal pain, persistent diarrhoea and iron-deficiency anaemia; 21 of these patients were asymptomatic with treatment at the time of the examination. Inflammatory lesions such as erosions, sores, ulcers and/or stenoses were detected in 51.2% of patients, and 33% of patients were asymptomatic11. Treatment changed in 53.3% of patients following the DBE. No serious complications occurred in any case. Considering these results and that mucosal healing is the objective to be achieved in order to improve the disease’s prognosis, we could think of DBE as being useful for evaluating the mucosa before and after treatment. We also know that there is a poor clinical-endoscopic correlation in CD, so it would be important to identify those (asymptomatic) patients with a clinical response to treatment who have a higher probability of experiencing intestinal lesions12.
At present, we have no validated endoscopic scoring system for SI lesions in CD patients, so Mensik et al. defined a scale based on levels of severity:
• Grade 0 if there are no lesions.
• Grade 1 (mild) when there are minor lesions such as erythema, oedema and sores (Fig. 1).
• Grade 2 (moderate) when there are ulcers of between 0.5 and 2 cm (Fig. 2).
• Grade 3 (severe) when there are ulcers larger than 2 cm and/or non-significant stenoses.
• Grade 4 (stenotic) when there are significant stenoses with or without an associated inflammatory component13 (Fig. 3).
These authors included 50 patients with CD and suspected intestinal involvement, not demonstrated by conventional techniques, in their prospective study. All patients had abdominal pain, iron-deficiency anaemia and/or hypomagnesaemia and so received an oral and anal DBE to complete the examination of the SI. Biochemical, inflammatory and clinical parameters (Crohn’s Disease Activity Index [CDAI]) were also recorded. Intestinal lesions were found in 70% of the patients in the proximal and distal jejunum and the proximal and distal ileum. Patients with intestinal lesions primarily had more ileocolic involvement and less exclusively colonic involvement, and although the CDAI was indeed higher in patients with intestinal involvement than in those without it, no differences in laboratory parameters were found between the two patient groups. The findings led to a change in treatment in 26/35 patients (74%), including starting immune suppressant drugs (azathioprine or methotrexate, 29%), anti-tumour necrosis factor (anti-TNF) therapy (infliximab or adalimumab, 26%), changing the anti-TNF drug (15%) and surgery (26%). After one year of follow-up, 88% of patients achieved clinical remission with a significant decrease in CDAI. A second DBE was performed in 10 of the patients, showing mucosal healing in 9 (90%), 7 of whom had started anti-TNF therapy (4 patients) or changed from one anti-TNF agent to another (3 patients). From these results, it is inferred that adjusting treatment for patients with intestinal lesions leads to clinical and endoscopic improvement, with enteroscopy also playing an important role in investigating these lesions. Prospective randomised studies must be conducted to determine indicators for intestinal involvement that could provide guidance as to which symptomatic or asymptomatic patients should have their treatment intensified in order to change the course of the disease.
TIPOS DE ENTEROSCOPIA
There are currently three types of enteroscopes on the market that allow for a deeper intubation of the SI than classic push enteroscopy (150 cm) and ileocolonoscopy (30–50 cm):
• Double-balloon enteroscope (DBE, Fujinon, Wayne, NJ).
• Single-balloon enteroscope (SBE, Olympus America).
• Spiral enteroscope (SE, Spirus Medical, Stoughton, MA, 2005).
The DBE was the first to appear on the market, shortly after capsule endoscopy, and most studies have been conducted and published using this device, although in the last 2–3 years publications referencing SBE and SE have increased significantly. We recommend looking at the characteristics of the different types of enteroscopes in Table I of section I.1.4.
The Fujinon DBE system has a 200-cm-long enteroscope (diameter 9.4 mm) and a 140 cm overtube, both with a latex balloon on their distal ends. In contrast, the SBE has the same diameter and length characteristics, but only one balloon, made of silicon, which is part of the overtube. It is advanced through the SI by repeated cycles of inserting and withdrawing the overtube and the enteroscope with inflated balloons, causing the intestinal loops to straighten and fold, which allows it to advance in depth. The SBE uses a single balloon on the overtube, and the overtube and anchored enteroscope are withdrawn by flexing the latter (Video 1). Enteroscopy can be performed orally or antegrade and anally or retrograde, reaching 240–360 cm in the former case and 102–140 cm by the anal route14,15. With the DBE, 16 to 86% of total enteroscopies have been described as being performed orally, although this is not possible in all cases.
Spiral enteroscopy uses a spiral overtube, 118 cm in length and 17 mm in diameter, with a helical design that can be adapted to endoscopes of less than 9.4 mm in diameter, such as any flexible enteroscope or even a paediatric colonoscope. It is advanced through the SI by manual clockwise rotations of the overtube that fold the SI and allow forward motion. The endoscope is withdrawn using the same rotating movements, but in an anticlockwise direction. This device was initially designed for oral enteroscopy (Endo-Ease Discovery SB), but a rectal overtube called the Endo-Ease Vista Retrograde is now also available and can be used for anal enteroscopy or difficult colonoscopies16 (Fig. 4). The learning curve for this technique is comparable to that for balloon enteroscopy, and it can be performed by expert endoscopists without issue. Another advantage of the SE is that none of its components contains latex.
There are several comparative studies that seek to explain which enteroscopy method is the best one to use. Dogmak et al. recently conducted a multicentre, randomised study comparing both techniques, DBE (65 patients) and SBE (65 patients), in 130 patients, finding no significant differences between the two endoscopic methods in terms of insertion depth, duration of the procedure, the number of total enteroscopies, complications, diagnostic capacity and therapeutic impact17.
Also, May et al. compared spiral and double-balloon enteroscopy in 10 patients, finding that the former examination is completed in significantly less time, but reaches a shallower insertion depth18. Later studies comparing these two techniques have recently noted that there are no differences between them, achieving the same examined distance and the same therapeutic impact, with no serious complications in either case19. In the latter study, 80% of indications were in patients with intestinal bleeding of unknown origin, the majority of whom had had a previous total capsule endoscopy study.
The proportion of total enteroscopies achieved with one method or the other is another controversial topic, with publications initially stating that DBE was the technique that achieved the greater percentage of total enteroscopies by the oral route20. Recently, Domagk et al. described very similar rates of completed examinations using double- and single-balloon enteroscopes. No complete studies with the spiral enteroscope had been published, and a few months ago Akerman et al. described a new motorised spiral system that could allow to perform oral studies up to the ileocaecal valve in much shorter times than current systems allow17. As such, prospective studies are needed to confirm these results. In any case, this could be seen as a secondary issue considering that only 25% of CD patients will require a complete enteroscopy. The technique currently used to study the entire SI consists of using India ink to tattoo a small mark at the most distal point reached by oral enteroscopy and subsequently trying to locate this tattoo by the anal route21.
Techniques for correctly performing diagnostic enteroscopy
Routes of access, intestinal preparation and complications:
• Enteroscopy should not be the first line of assessment in a patient with suspected CD, although it must be considered for patients with a clinical obstruction4.
• Capsule endoscopy and other radiological examination techniques can be useful and complementary, indicating the best route of access for intubation of the enteroscope (oral or anal) depending on where the lesions to be biopsied or treated are located.
• In patients with CD, oral enteroscopy will be performed following the CE study if the suspicious lesion is located in the proximal 66% seen on the video; the anal access route will be used if the findings are in the distal 33%22.
• The intestinal preparation will be different depending on the route of access for the enteroscopy. As such, oral or antegrade enteroscopy will only require 8–12 hours of fasting, while patients undergoing retrograde enteroscopy must take an evacuant solution equivalent to the washout required for a colonoscopy.
Enteroscopy is performed under deep sedation or anaesthesia, since it is a long and uncomfortable procedure for patients23. In addition, this examination requires an experienced endoscopist, with the learning curve currently being described as 10 supervised examinations for antegrade enteroscopy and 20–30 cases for retrograde enteroscopy24. Recently, Sanaka et al. published a retrospective study that included 250 enteroscopies performed with one of the three available techniques, which showed that a greater intubation distance (231 vs 103 cm, p < 0.001), shorter examination time and better diagnostic and therapeutic results (55% vs 44%, p < 0.001) were achieved with the antegrade route25.
Technically, a balloon enteroscope creates difficulties at several points in the examination:
• To start with, it is very important to lubricate the space between the endoscope and the overtube well with water, as the latter is permeated with a hydrophilic substance to allow sliding, so other lubricating substances need not be used. Also, pyloric intubation can be difficult in the abdominal cavity, as the tubes are very flexible; it is important to avoid having them loop back on themselves, as this would impede the enteroscope from advancing through the SI.
• In the first examinations, radiological monitoring is useful in order to identify the actual movements made by the endoscope in the SI.
• If air insufflation is minimised, we will achieve better progress and less loop formation.
• Posture change manoeuvres, including the prone position, can help in passing the ileocaecal valve, particularly for retrograde enteroscopy.
• Insufflation with carbon dioxide, which rapidly diffuses from the intestines, will also facilitate progress with less abdominal bloating and, according to observations by some authors in comparative studies with air insufflation, greater insertion depth, less need for sedation and, of course, less pain following the examination26,27.
• After several advance/withdrawal manoeuvres or upon reaching the target point, an India ink tattoo is used to mark the maximum depth reached, which will be informative in later examinations or for the surgeon, if a specific lesion must be located28,29.
In retrograde enteroscopies, the percentage of valve intubation failures can reach 20–30% of cases. In these procedures, prior intestinal preparation is important, as is using the balloon system with inflation and anchoring in the colon in order to advance. As previously mentioned, changes in position can promote caecal intubation and the placement of a guide or a dilatation balloon (triple balloon) can also help30.
The appropriate time to perform treatment during the enteroscopy is during withdrawal, with the balloons half-inflated and using antispasmodic agents such as buscapina or glucagon, which will facilitate the procedure.
There are different methods for measuring the length of intestine examined with the enteroscope: the most widely-used is May’s method, which totals the advances of the enteroscope during each cycle (20–40 cm)31. Other measurement systems developed include the withdrawal method, which estimates the distance examined during withdrawal32, and the overtube method, which compares the measurements of the endoscope and the overtube during the test33. López-Albors et al. validated this method in an animal model, showing it to be useful, with less than 10% deviation and allowing dynamic examinations to be performed21.
The main disadvantages of enteroscopy are that it is an expensive, invasive procedure with a long duration that requires sedation and is only available in some specialised centres4.
The most common complications of enteroscopy include pancreatitis, bleeding and intestinal perforation. The perforation rate described for diagnostic procedures is around 0.8%, but can reach up to 4% if therapeutic procedures such as electrocoagulation, polypectomy or endoscopic dilatation are performed23 (Fig. 5). Mensink et al. described the complications of 2,362 procedures performed in Europe and Japan, which primarily included pancreatitis (0.3%), bleeding (0.8%) and perforation following argon gas treatment or the dilatation of intestinal stenoses (0.3%)34.
In a subsequent retrospective multicentre study conducted in 62 German sites including over 2,000 DBE procedures with 23% total enteroscopies, 1.2% had complications, including 4 cases of pancreatitis (0.3%), 3 perforations following SI polypectomies (1.5% of 137 polypectomies performed), 6 cases of bleeding and 11 complications related to sedation35.
Although there are no contraindications described for balloon enteroscopy other than those for conventional endoscopy, we must consider that intestines previously weakened by an inflammatory or neoplastic process or with an altered anatomy following a surgical intervention can be at a higher risk of complications with balloon inflation at this level. Furthermore, patients with previous abdominal surgeries will have adhesions that will impede the enteroscope from advancing.
The complication rate described for spiral enteroscopy is similar to that for other types of enteroscopy, with 0.3% severe complications and 0.27% perforations. No cases of pancreatitis have been described36.
COMPARISON OF ENTEROSCOPY WITH OTHER DIAGNOSTIC TECHNIQUES
Since its appearance on the market, enteroscopy has been compared with each endoscopic and radiological technique available for studying the SI. The diagnostic capacity of balloon enteroscopy for CD differs in patients suspected of having the disease (5–13%) and those already diagnosed with CD (74–96%)37.
The technique classically used to study the SI was bowel transit (BT), which is now almost unused in CD. In a comparative study of DBE against ileocolonoscopy and BT, it was shown that 60% of patients had intestinal involvement that was not accessible by conventional endoscopy and that DBE was also superior to radiological study for the detection of sores, erosions and small intestinal ulcers38.
CE is a non-invasive examination that allows the entire SI to be visualised, but its disadvantage is that we cannot obtain samples for histology or apply treatments. In a recent meta-analysis comparing CE and DBE, including 11 studies and 375 patients with suspected SI involvement, no differences in diagnostic capacity were observed, so the authors concluded that both examinations are equivalent and complementary for the diagnosis of CD39. If the ileocolonoscopy is negative, it would be very useful to perform a CE, which would allow us to examine the entire SI. Furthermore, enteroscopy would also help us if retained capsules need to be extracted40.
MR enterography and CT enterography are two non-invasive radiological techniques that are accepted for study of the SI and have shown great utility in the study of CD, primarily for detecting extraluminal lesions, fistulae and stenotic complications. Absence of radiation means MR enterography is preferable to CT enterography for CD patients. Resonance imaging allows the full SI to be visualised in a single session, and its main limitation is the difficulty of detecting superficial mucosal lesions in the proximal SI (jejunum and proximal ileum), in relation to insufficient intestinal loop distension41. In a recently-published pilot study, Seiderer et al. enrolled 10 patients with suspected CD and compared the findings from DBE and MR enterography, observing that the enteroscopy and the resonance imaging agreed in the diagnosis of 7 patients (5 with inflammatory lesions and 2 with normal examinations). In the three remaining patients, enteroscopy was normal and resonance imaging detected minimal lesions. Therefore, enteroscopy and MR enterography are very useful complementary techniques, particularly for diagnosing stenotic fistulising CD42 (Video 2 and Fig. 6). Wiarda et al. compared CE and MR enterography in 38 patients with suspected or diagnosed CD, using a panel of experts and DBE as the gold standard. In this study, resonance imaging was the first examination performed in order to detect stenoses. Based on this, one third of the patients could not undergo CE, and the results showed MR enterography to have a higher sensitivity than CE (74% vs 57%, p < 0.05). Regarding the identification of these stenoses, resonance imaging identified 13 stenoses and only 10 were confirmed by enteroscopy43.
The different imaging techniques are vital in the study of the SI in patients with CD. Thus, CE, MR enterography and enteroscopy are complementary techniques that are essential for the benefit of the patient44.
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