Mid-gastrointestinal Bleeding: Capsule Endoscopy and Push-and-pull Enteroscopy Give Rise to a New Medical Term

Capsule endoscopy (CE) and push-and-pull enteroscopy (PPE) using the double-balloon technique have revolutionized imaging procedures in the field of small-bowel diagnosis. CE, which was introduced into clinical practice in 2001, made it possible for the first time to image intraluminal conditions in the entire small bowel with excellent quality [1] [2]. PPE, the prototype stage of which was first reported in 2001 by H. Yamamoto and by our own group in 2003, made it possible not only to inspect small-bowel diseases but also to carry out intraluminal treatment of them [3] [4].

At the end of the 20th century, only indirect procedures using radiographic techniques (conventional enteroclysis or computed tomography) or magnetic resonance techniques (magnetic resonance enteroclysis) were available to provide rough imaging of the small bowel. These procedures were - and today still are - used to detect larger tumors, and they are mainly helpful for demonstrating stenoses and fistulas (e. g., in Crohn’s disease). However, they do not of course allow direct intraluminal assessment of the mucosal situation - although this is a decisive prerequisite for detecting bleeding sources in the small bowel. Nuclear-medicine procedures, including radiographic angiography, also proved unsatisfactory for this, but in the absence of a better standard method were in widespread use in patients with a suspicion of chronic or acute recurrent small-bowel bleeding. Even the initial studies comparing capsule endoscopy with the conventional indirect procedures showed that capsule endoscopy was clearly superior to all of the other procedures for this indication. The same also applied to push enteroscopy, which due to technical limitations only allowed visualization of approximately 60 - 100 cm of the postpyloric small bowel [1] [2] [5] [6].

PPE using the double-balloon technique not only confirmed the results of CE but also extends the range of interventional endoscopy. Particularly in cases of small-bowel bleeding, PPE allows hemostasis to be carried out using injection procedures or argon plasma coagulation, in addition to diagnostic work-up. Precise diagnosis and endoscopic treatment options have in the meantime made many open surgical procedures with intraoperative hemostasis unnecessary. CE and PPE have optimized the diagnosis of small-bowel bleeding and made it more precise. This was confirmed by retrospective and prospective single-center and multicenter studies in Japan and Europe [7] [8] [9] [10]. The studies of PPE published in the current issue of Endoscopy [11] [12] confirm the findings of the initial studies. Both in the series in Magdeburg and in the larger study in the Netherlands, complete endoscopy via the oral route was successful in selected patients. In the Dutch series, the mention of three complications, all involving pancreatitis, should be noted; however, conservative treatment was possible in all of these cases. Both studies underline the tremendous diagnostic potential of the method and its direct implications for treatment in more than half of the patients examined.

The studies in France and Japan provide initial information on the comparative value of capsule endoscopy and PPE [13] [14]. In the study by Gay et al., capsule endoscopy was regarded 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., the diagnostic yield of CE was 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 two studies provide further support for the concept of using CE as a diagnostic procedure for selecting patients for PPE. Further prospective and controlled studies are undoubtedly necessary to establish the value of CE and PPE in the diagnostic setting of small-bowel diseases.

Before the introduction of CE and PPE, the definition of what constitutes bleeding in the small-bowel region was just as unclear as the diagnosis of the condition itself. Only upper gastrointestinal bleeding (UGI) and lower gastrointestinal bleeding (LGI) were known. A standard textbook in gastroenterology, Sleisenger and Fordtran, does not even include a definition of UGI and LGI bleeding or any information regarding landmarks for distinguishing between the two [15]. Other standard reference publications often describe bleeding from lesions above the ligament of Treitz as UGI bleeding and all forms of bleeding from lesions situated below the ligament of Treitz as LGI bleeding. With the optimized diagnostic options in the small-bowel region now available with CE and PPE, it may be suggested that OGI and UGI bleeding should be defined strictly in accordance with their diagnostic accessibility and should be supplemented with a further term - mid-gastrointestinal (MGI) bleeding.

UGI bleeding. All bleeding sites that can be reached during the course of standard upper gastrointestinal endoscopy (esophagogastroduodenoscopy) and which can usually also be treated endoscopically should in the future be described as UGI bleeding. This means that the boundaries between UGI and MGI bleeding created by the equipment and technology lie between the papilla of Vater and the lower bend of the duodenum. However, it is best to set the boundary to the papilla of Vater, as the lower bend of the duodenum is not always reached with standard gastroscopy.

MGI bleeding refers to the actual small bowel, starting distally to the papilla of Vater and reaching as far as the terminal ileum. Bleeding sources that lie in this segment of the digestive tract are best diagnosed with CE and PPE (via the oral or anal routes). Secondary diagnostic procedures for clarifying MGI bleeding include push enteroscopy, technetium scintigraphy, radiographic angiography, and blood-pool scintigraphy. When all of the procedures fail - e. g., with incomplete PPE due to stenoses or adhesions - intraoperative enteroscopy can also be considered as a last resort in MGI bleeding.

LGI bleeding consists of bleeding sources located in the colon or anorectum, which can usually be reached with a standard colonoscope. Bleeding sites located in the terminal ileum that can be identified using intubation with the colonoscope (e. g., bleeding in florid Crohn’s ileitis) should be defined as MGI bleeding, as the terminal ileum, being part of the mid-gastrointestinal tract, belongs to the small bowel; the terminal ileum cannot be examined endoscopically in all cases and if it can, only a short part of it is usually visible.

A clear way of defining the location of the bleeding source is required in order to provide a solid foundation for future studies - particularly for questions of bleeding of unclear etiology, comparisons between different imaging modalities in this problem area, and comparisons of the value of different methods. This has not previously been possible, as the example of push enteroscopy shows. For push enteroscopy, the literature reports diagnostic yields ranging from 20 % to 89 % for bleeding of unclear etiology [16]. When one examines the study reporting the highest diagnostic yield in detail, it is found that successful push enteroscopy was recorded for all bleeding sources that could also have been identified using upper gastrointestinal endoscopy. This would not have happened with the definition proposed here - i. e., limiting UGI bleeding to as far as the papilla of Vater, with MGI bleeding starting distal from the papilla of Vater.

In summary, CE and PPE as modern endoscopic procedures for small-bowel diagnosis require - and make possible - a reclassification of the terminology. Upper gastrointestinal, mid-gastrointestinal, and lower gastrointestinal bleeding are easily and logically defined and will also make the diagnostic work-up clearer (Table [1]).

Table 1 Terminology for gastrointestinal bleeding UGIbleeding MGIbleeding LGIbleeding Diagnosis Esophagogastro-duodenoscopy CE and PPE Colonoscopy secondary methods - Push enteroscopyTechnetium scintigraphyAngiographyIntraoperative endoscopy - CE: capsule endoscopy; LGI: lower gastrointestinal; MGI: mid-gastrointestinal; PPE: push-and-pull enteroscopy; UGI: upper gastrointestinal.

References

• 1 Ell C, Remke S, May A, Helou L. et al . The first prospective controlled trial comparing wireless capsule endoscopy with push enteroscopy in chronic gastrointestinal bleeding.  Endoscopy. 2002;  34 685-689
• 2 Mylonaki M, Fritscher-Ravens A, Swain P. Wireless capsule endoscopy: a comparison with push enteroscopy in patients with gastroscopy and colonoscopy negative gastrointestinal bleeding.  Gut. 2003;  52 1122-1126
• 3 Yamamoto H, Sekine Y, Sato Y. et al . Total enteroscopy with a nonsurgical steerable double-balloon method.  Gastrointest Endosc. 2001;  53 216-220
• 4 May A, Nachbar L, Wardak A. et al . Double-balloon enteroscopy: preliminary experience in patients with obscure gastrointestinal bleeding or chronic abdominal pain.  Endoscopy. 2003;  35 985-991
• 5 Hartmann D, Schilling D, Bolz G. et al . Capsule endoscopy versus push enteroscopy in patients with occult gastrointestinal bleeding.  Z Gastroenterol. 2003;  41 377-382
• 6 Saurin J C, Delvaux M, Gaudin J L. et al . Diagnostic value of endoscopic capsule in patients with obscure digestive bleeding: blinded comparison with video push-enteroscopy.  Endoscopy. 2003;  35 576-584
• 7 Yamamoto H, Kita H, Sunada K. et al . Clinical outcomes of double-balloon endoscopy for the diagnosis and treatment of small-intestinal diseases.  Clin Gastroenterol Hepatol. 2004;  2 1010-1016
• 8 May A, Nachbar L, Schneider M, Ell C. Double-balloon enteroscopy (push-and-pull enteroscopy) of the small bowel: feasibility, diagnostic and therapeutic yield in patients with suspected small bowel disease.  Gastrointest Endosc. 2005;  62 62-70
• 9 Ell C, May A, Nachbar L, Cellier C. et al . Push-and-pull enteroscopy in the small bowel using the double-balloon technique: results of a prospective European multicenter trial.  Endoscopy. 2005;  37 613-616
• 10 Di Caro S, May A, Heine G DN. et al . The European experience with double-balloon enteroscopy: indications, methodology, safety and clinical impact.  Gastrointest Endosc. 2005;  62 545-550
• 11 Mönkemüller K, Weigt J, Treiber G. et al . Diagnostic and therapeutic impact of double-balloon enteroscopy.  Endoscopy. 2006;  38 67-72
• 12 Heine G DN, Hadithi M, Groenen M JM. et al . Double-balloon enteroscopy: indications, yield and complications in a series of 272 patients with suspected small-bowel disease.  Endoscopy. 2006;  38 42-48
• 13 Gay G, Delvaux M, Fassler I. Capsule endoscopy to select push-and-pull enteroscopy indications: experience from 42 consecutive cases and validation of a time index to choose the endoscope insertion route.  Endoscopy. 2006;  38 49-58
• 14 Nakamura M, Niwa Y, Ohmiya N. et al . Preliminary comparison of capsule endoscopy and double-balloon enteroscopy in patients with suspected small bowel bleeding.  Endoscopy. 2006;  38 59-66
• 15 Feldman M, Friedman L S, Brandt L J (eds). Sleisenger and Fordtran’s gastrointestinal and liver disease: pathophysiology, diagnosis, management, 8th ed. Philadelphia; Saunders 2006
• 16 Feldman M, Friedman L S, Sleisenger M H (eds). Sleisenger and Fordtran’s gastrointestinal and liver disease: pathophysiology, diagnosis, management, 7th ed. Philadelphia; Saunders 2002