Imaging of Meckel’s Diverticulum in Adults: Pictorial Essay James K. Clark, David A. Paz, Gary G. Ghahremani PII: DOI: Reference:

S0899-7071(14)00121-1 doi: 10.1016/j.clinimag.2014.04.020 JCT 7622

To appear in:

Journal of Clinical Imaging

Received date: Revised date: Accepted date:

31 August 2013 26 February 2014 28 April 2014

Please cite this article as: Clark James K., Paz David A., Ghahremani Gary G., Imaging of Meckel’s Diverticulum in Adults: Pictorial Essay, Journal of Clinical Imaging (2014), doi: 10.1016/j.clinimag.2014.04.020

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ACCEPTED MANUSCRIPT Imaging of Meckel’s Diverticulum in Adults: Pictorial Essay

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James K. Clark, M.D.1, David A. Paz, M.D.1, Gary G. Ghahremani, M.D.2

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Department of Radiology, Naval Medical Center San Diego, 34800 Bob Wilson Drive, San Diego, CA 92134 2.

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Department of Radiology, University of California San Diego, 200 West Arbor Drive, San Diego, CA 92103

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Correspondence to J. Clark; email: [email protected]

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Tel: (619) 453-6244 Reprint Address: James Clark, M.D.

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Department of Radiology Naval Medical Center San Diego

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34800 Bob Wilson Drive San Diego, CA 92134

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ABSTRACT: Meckel’s diverticulum is the most common congenital abnormality of the gastrointestinal tract. It is usually asymptomatic but may present with complications of acute diverticular inflammation, ulceration, hemorrhage, small bowel obstruction, perforation, retained foreign

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ACCEPTED MANUSCRIPT bodies, enterolith formation and neoplasm development. Thus, the preoperative radiological diagnosis is crucial for proper management of the patients. This article reviews the anatomic and

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clinical features of Meckel’s and describes the role of imaging in the detection of Meckel’s and

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evaluation of its associated pathological processes.

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Keywords: Meckel’s diverticulum, radiography, small bowel obstruction, enteroliths, computed

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tomography, radionuclide scintigraphy.

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ACCEPTED MANUSCRIPT EMBRYOLOGIC ANATOMY AND PATHOLOGY: Meckel’s diverticulum is the vestigial remnant of the vitelline or omphalomesenteric

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duct, which connects the yolk sac to the midgut of the developing fetus. This structure is usually obliterated by the eighth week of gestational age. In 2-3% of cases, however, the proximal part

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of it remains patent as a tubular or saccular out pouching on the antimesenteric side of distal

of Meckel’s diverticulum to the umbilicus (1).

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ileum. The rest of involuted vitelline duct may persist as a fibrous band connecting the blind end

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Meckel’s diverticulum in adults is usually located 30 to 60 cm from the ileocecal valve, but it is much closer to it in infants since their intestinal maturation and elongation has not yet

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completed. Both the size and shape of Meckel’s diverticulum are also variable. Most of them appear as a 3-5 cm finger-like structure, but occasionally present as a larger saccular lesion with

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5-10 cm diameter (1-4). The wall of Meckel’s diverticulum is composed of 3 typical intestinal

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layers of mucosa, muscularis and serosa. Although it is usually lined with ileal mucosa, it may

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also harbor islands of heterotopic gastric epithelium (40-60%) and pancreatic tissue (5-9%). In such cases, the glandular secretions can lead to peptic ulceration within the diverticulum or adjoining ileum, resulting in intestinal hemorrhage, cicatrical stenosis of the diverticular neck, inflammation and even perforation (2-5).

CLINICAL MANIFESTATIONS: The clinical signs and symptoms of Meckel’s are variable and reflect the underlying pathologic process. By far the majority remain clinically silent and detected incidentally during radiologic evaluation or abdominal surgery for unrelated conditions (5-7). Intestinal hemorrhage 3

ACCEPTED MANUSCRIPT is the most common presentation, particularly in the pediatric patients. The bleeding may be painless, slow or intermittent, but may also cause acute onset of bright red rectal bleeding. Such

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cases are usually associated with a Meckel’s diverticulum containing ectopic gastric mucosa with

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peptic ulceration (7-9).

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The classic description of Meckel’s diverticulum by the “Rule of 2’s” refers to its 2% prevalence, 2 feet distance from the ileocecal valve, 2 inches long, containing 1 or 2 types of

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heterotopic gastric or pancreatic tissue and usually symptomatic by the age of 2 years.

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Meckel’s diverticulitis is a complication usually seen in adults (2, 3, 8). These patients experience abdominal pain and tenderness usually centered in the periumbilical region or the

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right lower abdomen, often simulating acute appendicitis. Therefore, it is a recommended surgical practice to search for Meckel’s diverticulum whenever laparotomy fails to confirm a

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suspected appendicitis (8-11).

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Both the pediatric and adult patients with complicated Meckel’s diverticulum may

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develop small bowel obstruction, and present with colicky abdominal pain, vomiting and distention. The mechanism of obstruction can be intussusception of an inverted Meckel’s diverticulum, volvulus or strangulation of distal ileum by the fibrous band connecting the diverticulum and umbilicus, incarceration in the inguinal canal (Littre’s hernia), and rarely by an enlarged diverticulum harboring retained foreign objects, enteroliths or a tumor (2-4,7-9). The latter includes benign lesions such as leiomyomas and lipomas, or malignant neoplasms such as an adenocarcinoma arising from heterotopic gastric mucosa, carcinoids and sarcomas (2, 3, 8). These tumors are seldom diagnosed preoperatively, but may appear as a filling defect or mass

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ACCEPTED MANUSCRIPT within an opacified Meckel’s diverticulum or infiltrate its wall and the adjacent mesenteric fat on CT images (2, 3, 8).

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RADIOLOGICAL FEATURES:

According to a widely quoted statement by Dr. Charles W. Mayo in 1933, “Meckel’s

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diverticulum is a diagnosis that is frequently suspected, often looked for, but seldom found (12).”

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However, more recent experiences indicate that an accurate preoperative diagnosis of Meckel’s diverticulum and its complications can be made with an increasing frequency due to improved

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imaging techniques (2-4, 13-18). Therefore, it is important for practicing physicians to be familiar with the value and limitations of various imaging modalities that are available for

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diagnostic evaluation of this entity.

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This article is based on our experience with 118 cases of Meckel’s diverticulum diagnosed by the senior author during the past three decades at the Evanston Hospital-

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Northwestern University (1980-2000) and University of California Medical Center – San Diego

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(2000-present). This series included 61 men and 57 women ranging in age from 14 to 88 years (mean age of 48). Surgical resection of these diverticula was performed in 84 patients: 64 at Evanston Hospital, 12 at UCSD, and 8 at other institutions. In the remaining 34 cases the Meckel’s diverticulum was an asymptomatic incidental finding or the patients were lost to follow-up. We illustrate the spectrum of presentations on abdominal radiographs, small bowel series, enteroclysis, barium enema with retrograde ileal reflux, radionuclide scintigraphy and computed tomography. A. Abdominal Radiographs.

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ACCEPTED MANUSCRIPT Patients with symptomatic Meckel’s diverticulum often undergo radiography of the abdomen as the initial examination. On occasional instances a large gas-filled diverticulum may

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be visible as a persistent round or oval-shaped radiolucency in the right lower abdomen (Fig. 1).

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This occurs when the narrowed neck of the diverticulum acts as a ball-valve and entraps the intestinal gas within its lumen. Fruit seeds or other exogenous objects may also be retained

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within a Meckel’s diverticulum and serve as a nidus for development of radiopaque or laminated

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enteroliths (Fig. 2). Their limited mobility with changing position of the patient indicates their

obstruction proximal to it (3, 4, 19).

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B. Gastrointestinal Barium Studies.

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confinement within the diverticulum, particularly when there is concomitant small bowel

Opacification of the small bowel with contrast material has been used successfully for

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detection of Meckel’s diverticulum. Three different techniques that can be utilized for this

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purpose are the conventional antegrade small bowel series, enteroclysis, and retrograde ileal

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reflux during barium enema (2, 3, 19-21). If the Meckel’s diverticulum is large and filled with barium, it can be easily visible during a routine small bowel series. However, smaller diverticula maybe obscured by the opacified intestinal loops. Hence, their detection will require a careful fluoroscopic evaluation using graded compression and spot filming (Figs.2B, 3 and 4). The visualization of a suspected Meckel’s diverticulum during conventional small bowel series can be further improved through air-contrast images. This may be achieved by oral administration of effervescent agents or rectal insufflation of air with subsequent ileal reflux, the so-called peroral pneumocolon (22, 23). The characteristic appearance of a Meckel’s diverticulum is a saccular structure attached to the

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ACCEPTED MANUSCRIPT antimesenteric border of distal ileum, thus facing away from the axis of mesenteric root. A triangular plateau with mucosal folds in three opposing directions is usually identified at the

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junction of Meckel’s diverticulum with the ileum. Most Meckel’s diverticula are located in the

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right lower abdomen or in the periumbilical and pelvic regions. However, they may also be situated elsewhere in the abdomen in patients with a long mesentery, intestinal malrotation or

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situs inversus (2, 20, 21). On rare occasions a Meckel’s diverticulum may protrude and

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incarcerate in the inguinal region as the so-called Littre’s hernia.

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A Meckel’s diverticulum may at times present as an intraluminal polypoid mass causing small bowel obstruction ( 3, 13, 21, 24).This occurs when the diverticulum is inverted into the

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ileum and may serve as a lead point for intussusceptions ( Fig.5). Enteroclysis maybe an optimal technique for the diagnosis of Meckel’s diverticulum and

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various other pathologic processes of the small bowel. This procedure requires peroral or

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transnasal intubation of the duodenum for rapid infusion of barium to opacify and distend the

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small bowel loops. A sufficient volume of air or methylcellulose may also be injected to produce a double-contrast effect. A careful fluoroscopic evaluation of the opacified small bowel loops allows an accurate demonstration of Meckel’s diverticulum and its complications (Fig.6). Maglinte et al. (20) performed enteroclysis in 415 patients and diagnosed Meckel’s diverticulum in 11 symptomatic cases. Salomonowitz et al. (25) found seven Meckel’s diverticula among 400 patients examined by double-contrast enteroclysis. The detection rate of 2.65% and 1.75% in these 2 studies approximates the actual prevalence of Meckel’s diverticulum. Barium enema with retrograde opacification of the ileal loops is another useful approach to the diagnosis of Meckel’s diverticulum (2, 21). Spontaneous reflux into the small bowel

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ACCEPTED MANUSCRIPT occurs in 70-80% of patients undergoing single or double-contrast colon examination. In patients with right lower abdominal pain and/or distal small bowel obstruction, a barium enema

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study can assist in differential diagnosis of appendicitis, cecal diverticulitis, Crohn’s disease, or

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other pathologic processes. If the colon appears normal, however, the radiologist should attempt to visualize the distal ileum and search for Meckel’s diverticulum as the potential source of the

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clinical symptoms. We have used this technique to demonstrate asymptomatic Meckel’s

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diverticula (Fig.7 A and B), as well as its acute Meckel’s diverticulitis causing intestinal

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obstruction. C. Radionuclide Scintigraphy.

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Technetium pertechnetate is known to accumulate in the gastric mucosa, and it is used to visualize symptomatic Meckel’s diverticula which often contain heterotopic gastric epithelium.

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It has been documented that such mucosal islands with diameter of over 1 cm can be detected

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with almost 90% accuracy by high-resolution gamma cameras (2, 3, 18, 21). This technique

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requires serial imaging of the entire abdomen of a fasting patient after intravenous injection of 30 to 50 microCi/kg of the radioactive agent (up to 1mCi adult dose). Anterior views are recorded every 10 minutes for at least one hour to detect any abnormal collection of the isotope beyond the stomach area. A positive study will show the Meckel’s diverticulum as a persistent focal uptake in the right lower or mid abdomen (Fig. 8). In patients with active intestinal bleeding, a suspected Meckel’s diverticulum as its source can be detected by radionuclide scintigraphy. For this purpose, dynamic imaging of the abdomen is performed following injection of Technetium sulfur colloid or isotope labeled red blood cells (18, 21, 26).

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ACCEPTED MANUSCRIPT D. Mesenteric Angiography. Intestinal hemorrhage is usually the presenting symptom of Meckel’s diverticula that

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contain heterotopic gastric mucosa and peptic ulceration. The bleeding is often copious and painless, initially causing melena and later as bright red rectal bleeding. It has been shown that

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selective mesenteric arteriography can localize the source if the rate of active bleeding exceeds

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0.5 mL per minute (2, 7, 14, 21).

The blood supply to Meckel’s diverticulum is through the ileocolic branches of superior

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mesenteric artery, but a persistent vitelline artery may also be present (Fig.3B). This is an elongated vessel originating from the distal ileal artery and crossing the ileum to supply the

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Meckel’s diverticulum on its antimesenteric border (2, 3, 15).

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A bleeding Meckel’s diverticulum is demonstrated by progressive extravasation of contrast material into its lumen and the adjacent ileum, at times outlining their mucosal folds. A

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dense capillary stain of its wall may be seen, particularly in association with ectopic gastric

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mucosa and diverticulitis.

E. Computed Tomography. Computed tomography (CT) has become the preferred modality for the evaluation of most abdominal disorders. Intravenous injection of iodinated contrast material and peroral bowel opacification are helpful for improved visualization of viscera unless there are contraindications to their usage. On CT, a small Meckel’s diverticulum may be difficult to distinguish from normal small bowel loops. If it is larger than 3 cm in diameter, however, it appears as a blind-ending gas or

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ACCEPTED MANUSCRIPT fluid-filled structure that may also contain foreign bodies or enteroliths (Fig. 9). Its visualization is often enhanced by the modern multi-detector CT, which offers improved spatial resolution and

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image reconstruction in coronal and sagittal planes. This is particularly important in detection of

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associated complications (2-4, 13).

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Nearly 30-40% of symptomatic Meckel’s diverticula manifest with an acute or intermittent small bowel obstruction (Fig. 10). This is often the result of ulceration and cicatrical

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stenosis of the attached ileum due to acid secretions by heterotopic tissue of the diverticulum,

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luminal narrowing by adhesions, or torsion and incarceration of the intestinal loops beneath a fibrous band connecting the diverticulum to the umbilical region. CT can demonstrate the

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underlying process such as Meckel’s diverticulitis (Fig.10). Other complications such as intussusception of an inverted diverticulum or Littre’s hernia can be detected by this technique

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(Fig. 5). Retained foreign bodies and enteroliths can be seen in 5-10% of Meckel’s diverticula.

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The presence of ectopic gastric mucosa is usually demonstrated by the hypervascular soft tissue protruding into the diverticular lumen (Fig.4B). The rare occurrence of neoplasms arising within

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a Meckel’s diverticulum can also be recognized as a sessile or lobulated mass that often enhances with contrast and may infiltrate and thicken the adjacent wall (3, 8, 27). F. Other Imaging Modalities. A few reports concerning the imaging of Meckel’s diverticulum by abdominal sonography or MRI have been published (3, 16, 17). These anecdotal cases do not yet permit a conclusion regarding the actual value of these techniques for evaluation of this entity. However, Baldisserotto et al. reported 10 pediatric patients with Meckel’s diverticulitis that were detected

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ACCEPTED MANUSCRIPT by sonography (16). These lesions appeared as a cyst like structure with thick, irregular internal wall and an external hypoechoic rim corresponding to the muscular layer.

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The experience with MRI for diagnosis of Meckel’s diverticulum has been very limited. In one case, Dujardin et al. (14) reported the CT and MRI diagnosis of an inverted Meckel’s

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diverticulum causing ileoileal intussusception. One of our patients had presented with rectal hemorrhage due to subsequently proven Crohn’s colitis. Both the CT and MR enterography

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disclosed the presence of a giant Meckel’s diverticulum as an unsuspected coexisting finding

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(Fig. 12). It is likely that the wider usage of CT and MRI enterography will improve diagnostic applications of these techniques in the future.

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In the same context, the role of capsule endoscopy for the detection of Meckel’s diverticulum would require further experience because only a few isolated cases have been

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published (28, 29). A potential complication might be the retention of capsule within a Meckel’s

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diverticulum. A recent report from Sweden found that 31 of 2300 patients who underwent capsule endoscopy retained it in their digestive tract (30). The underlying cause was luminal

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narrowing by inflammatory or neoplastic processes, but none involved a Meckel’s diverticulum. Direct visualization of Meckel’s diverticulum by double-balloon enteroscopy has been the subject of several reports. Shinozaki et al. (32) were able to diagnose it by this technique in 5 of their 354 patients. By far the largest experience with pre-operative detection of 74 Meckel’s diverticula by double-balloon enteroscopy has been recently reported from China (33).

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ACCEPTED MANUSCRIPT CLINCAL MANAGEMENT: The recommended treatment of a symptomatic or complicated Meckel’s diverticulum is

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its surgical removal by either a simple diverticulectomy or segmental resection of the attached ileum. This can be achieved through laparoscopic or open approach.

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A significant number of Meckel’s diverticula are discovered incidentally during imaging

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studies or laparotomy performed for unrelated abdominal disorders. In such cases an elective surgery for the removal of an asymptomatic diverticulum may not be warranted. However, some

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surgeons consider it advisable to search for and resect a Meckel’s diverticulum during laparotomy in order to eliminate the risk of future complications. Park and associates reviewed

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the Mayo Clinic series of 1,476 patients with Meckel’s diverticulum. They recommend surgical removal of all incidental diverticula, particularly in male patients younger than 50 years of age,

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CONCLUSION:

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when the lesion is longer than 2 cm and contains ectopic tissue or abnormal features.

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A Meckel’s diverticulum is present in about 2% of the general population, and an estimated 5 to 20% of them will develop clinical symptoms during their lifetime. This is usually manifested as intestinal bleeding, acute or intermittent small bowel obstruction and right lower abdominal pain caused by Meckel’s diverticulitis. The widespread utilization of various imaging modalities has led to a marked improvement in preoperative diagnosis of Meckel’s diverticulum and its associated complications. Nearly 80% of our 118 cases had been evaluated by gastrointestinal barium studies and radionuclide scintigraphy. In the most recent 20% of patients, however, their Meckel’s diverticula were detected on abdominal CT examinations. It seems likely that CT and MR enterography, or direct visualization by endoscopic techniques will 12

ACCEPTED MANUSCRIPT be the principal means of diagnosing this entity in the future. Therefore, it is important for the practicing radiologist to be familiar with the spectrum of presentations of Meckel’s diverticula as

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described and illustrated in this article.

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33. He Q, Zhang YL, Xiao B, et al. Double-balloon enteroscopy for diagnosis of Meckel’s diverticulum: comparison with operative findings and capsule endoscopy. Surgery

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ACCEPTED MANUSCRIPT Figure Legend: Figure 1. Gas-filled Meckel’s diverticulum (MD) attached to the lateral aspect of distal ileum (IL) about 25 cm from the cecum (CE). Figures 2 a. and b. a. Meckel’s diverticulum containing 4 enteroliths (arrows) and located above the opacified bladder. b. Spot film of

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the small bowel exam shows the diverticulum and its enteroliths (arrows).

Figures 3 a. and b. a. Meckel’s diverticulum on spot film during small bowel series. b. Intraoperative photo showing the diverticulum

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and its prominent vitelline artery (arrow).

Figures 4 a. and b. a. Meckel’s diverticulum with an island of heterotopic gastric mucosa (arrow). b. Resected Meckel’s diverticulum

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with ulcerated heterotopic gastric mucosa (arrows).

Figures 5 a. and b. Inverted Meckel’s diverticulum causing an ileal intussuception in a 55 year-old woman. a. Note the invaginated antimesenteric wall at the attachment of the Meckel’s diverticulum (arrow). b. The tip of inverted diverticulum and its mesenteric fat

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are visible within the distal ileum on the lower CT image.

Figures 6 a. and b. a. Large Meckel’s diverticulum (arrows) detected by enteroclysis. b. Photograph of the diverticulum shows its

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attachment to the antimesenteric side of ileum.

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Figures 7 a. and b. Two patients with Meckel’s diverticulum (arrow) demonstrated by ileal reflux during barium enema. Figure 8. Meckel’s diverticulum demonstrated by radionuclide scintigraphy (arrow).Note heavy uptake of Tc99m by the gastric

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mucosa and excretion into the urinary bladder.

Figures 9 a. and b. CT images of a Meckel’s diverticulum containing a metallic foreign body (arrow).

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Figures 10 a. and b. Recurrent partial small bowel obstruction in a 45 year-old man. Coronal and sagittal CT images demonstrate a large Meckel’s diverticulum (arrows) at the junction of the markedly distended ileum and its collapsed distal loop. Figures 11 a. and b. CT of Meckel’s diverticulitis in 2 patients. a. Presenting as a thick-walled diverticulum(arrow) with adjacent mesenteric inflammation. b. Presenting as an interloop abscess (arrow) adjacent to the opacified distal ileum. Figures 12 a. and b. Coronal images from CT and MR enterography show a giant Meckel’s diverticulum measuring 5 x 8 cm and containing gas and debris. Note its narrow connection to the adjacent distal ileum (arrow) and the thickened descending colon caused by Crohn’s colitis. Figures 12 c. and d. Images from a follow-up CT enterography reveal the changed position of Meckel’s diverticulum and its attachment to the fluid-filled distal ileum (white arrow). Note the normal appendix (black arrow) as well as the hypervascularity and thickening of the sigmoid colon due to Crohn’s colitis.

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Imaging of Meckel's diverticulum in adults: pictorial essay.

Meckel's diverticulum is the most common congenital abnormality of the gastrointestinal tract. It is usually asymptomatic but may present with complic...
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