14 The Small Bowel:Normal andPathologic Anatomy

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The Small Bowel:

Normal and

Pathologic Anatomy 14

The distinctive course, coiled nature, and position of the small bowel are provided by the mesentery. The most characteristic gross anatomic feature of the jejunum and ileum is their organization into a series of bowel loops, compactly arranged in the midabdomen. In the routine interpretation of small intestinal series, little attention is directed to this unique organization of the bowel. In- deed, the confluence or overlapping of small bowel loops often presents a misleading appearance. Their ser- pentine, undulating course ordinarily poses a diagnostic challenge in identifying the presence of a localized ab- normality.

However, the anatomic relationships inherent in this characteristic arrangement of the small intestine into loops of bowel may provide significant diagnostic infor- mation.^1,2 Pathologically, many disease processes selectively involve the mesenteric or antimesenteric borders of the small intestine. An understanding of their anatomic definition and relationships permits radiologic identification of the specific borders.¹

Anatomic Considerations

The mesentery (Fig. 14–1) suspends the jejunum and il- eum from the posterior abdominal wall. It is composed of fatty extraperitoneal connective tissue, blood vessels, nerves, lymphatics, and an investment of peritoneum that reflects from the posterior parietal peritoneum. Fea- tures associated with the fan-shaped dimensions of the mesentery make it a unique suspensory ligament and contribute to the characteristic nature of small bowel loops.

The attached border, the root of the mesentery, extends obliquely from the point of termination of the duodenum, at the lower border of the pancreas on the left side of the second lumbar vertebra, to the cecum in the right iliac fossa near the right sacroiliac articulation. In that course, the line of attachment passes from the duodenojejunal flexure down over the front of the third part of the duodenum, then obliquely across the aorta, the inferior vena cava, the right ureter, and the psoas major

Fig. 14–1. The small bowel mesentery.

It extends from its line of attachment, or root, in a series of fanlike ruffles to suspend the jejunum and ileum. The undulating course of its intestinal edge constitutes a series of convexities and concavities. Peritoneal recesses extend between the mesenteric reflections.

(Reproduced from Meyers.¹)

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muscle, to the right iliac region. From the root, the mesentery extends in a series of fanlike ruffles to suspend the jejunum and ileum. There are usually six main folds, from the margins of which secondary folds project in all directions, and from those again even a third series may be formed. A series of peritoneal recesses are formed between the ruffles of the small bowel mesentery. The root of the mesentery is only about 15 cm (6 in.) long and is fixed in position. It is much thicker than the part near the gut, since it contains between its layers a considerable amount of fatty fibroareolar extraperitoneal tissue and the large vascular trunks that supply the intestine (Fig. 14–2).

The base, or unattached border, of the mesentery is frilled out to an enormous degree so that, while the root measures only 6–7 in., the free border is extended to 20–22 ft (Fig. 14–3). The great length of the intestinal border is produced by plication of the mesentery along its edge for a depth of from 6–8 cm (2½–3½ in.).

The length of the mesentery (Fig. 14–3), measured from its root to the attached edge of the intestine directly opposite, is usually 20–22 cm (8–9 in.). It is greater at that part that suspends the coils of the intestine lying between 2 and 3 m (6 and 11 ft) from the duodenum, where it may reach a length of 25 cm (10 in.). It tends to increase in length as age advances.

Normal Radiologic Observations

From these basic considerations, several principles may be derived that have practical diagnostic application to radiology of the abdomen.²

Axis of the Root of the Small Bowel Mesentery

The plane of attachment of the small bowel mesentery may be drawn by an imaginary line extending from the midtransverse duodenum or duodenojejunal junction to the ileocecal junction. The root of the mesentery most often inserts at the termination of the ileum with the colon and only rarely on the ascending colon or the distal ileum. On plain films, the line may be drawn from the left of L2 to the right sacroiliac articulation.

The axis of the root may be defined more clearly by barium contrast studies, which then relates more directly to small bowel loops. Figure 14–4 illustrates two differ-

ent cases of nonrotation of the jejunum, a common de- velopmental variant. The root of the small bowel mesentery is shown by the oblique plane providing the medial demarcation of these jejunal loops. The root may also be identified in cases of normal development and fixation of the mesentery. In the small bowel series shown in Figure 14–5, the attached border of the mesentery can be appreciated as the oblique plane from which the loops are suspended. The axis can be readily appreciated by sectional imaging (Fig. 14–6).

It is these normal relationships of small bowel loops to the supporting mesentery that basically determine the radiologic findings in cases of mechanical obstruction.

The dilated loops are then each tensely suspended from the mesenteric root as peristalsis persists; the hydrody- namic consequences lead to the classic “stepladder” con- figuration (Fig. 14–7).

Undulating Changeable Nature of Coils of Bowel Loops

A fan-shaped supporting ligament such as the mesentery, with an attachment of only 6 in. and an average length of 8–9 in., must suspend 20–22 ft of small bowel.

This remarkable feat is accomplished by the unique plication or frilling of its intestinal border. The mesentery extends from its root in a series of fanlike ruffles. This geometric arrangement provides an unusually long border to suspend the jejunum and ileum. It is precisely this feature that contributes to the characteristic undulating nature of the coils of small intestine. The mesentery is of such a length that the loops are able to move freely in the abdominal cavity, and consequently the position occupied by any portion of the small bowel, with the usual exception of the beginning of the jejunum and the ending of the ileum, cannot be stated with certainty.

Nevertheless, in general, the jejunum occupies the superior and left portions of the peritoneal cavity below the stomach, and the ileum the inferior and right divi- sions.

The changeable position of jejunal and ileal loops in vivo is most easily documented by comparing portions of the intubated small bowel on sequential films, as in Figure 14–8. These show the loops are movable on the root of the mesentery, but they maintain the convexities of the ruffles. Specific intestinal segments (nos.

1 through 4) can be matched and demonstrate varying positions within the peritoneal cavity. The changeable

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Normal Radiologic Observations 637

Fig. 14–2. Anatomy of the small bowel mesentery.

(a) Coronal anatomic section taken at the level of the third and fourth portions of the duodenum and the duodenojejunal junction (DJ). It demonstrates the fatty elastic nature of the mesentery, which contains the intestinal vessels as it radiates from its root to suspend loops of jejunum (JL) and ileum (I). L = liver.

(Courtesy of Manuel Viamonte, M.D., Mount Sinai Hospital, Miami Beach, FL.; reproduced from Mey- ers.¹)

(b) Transverse section shows fat- laden mesenteric leaves. Each sheath contains numerous vessels (arrow- heads) radiating toward small bowel loops. These vessels can be traced back to the superior mesenteric vessel.

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Fig. 14–3. Dimensions of the small bowel mesentery.

The length of the intestinal border to an extent

approximately 40 times that of its root is brought about by its unique frilled nature. This determines the characteristic formation of the small bowel into loops.

Fig. 14–4. Two different cases of nonrotation of the jejunum in the right abdomen.

The oblique plane that provides the medial demarcation of the loops of bowel identifies the axis of the root of the small bowel mesentery (dashed line).

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Fig. 14–5. The root of the small bowel mesentery.

This is revealed as the oblique plane (arrows) from which the intestinal coils are suspended. In this instance, it provides a line of transition between jejunal loops (shown by their prominent valvulae conniventes), which project to the patient’s left, and ileal loops (with less conspicuous valvulae), which extend to the right.

Fig. 14–6. Axis of the root of the small bowel mesentery.

Two different levels of CT, a 5 cm cephalad to b, in a patient with massive ascites, show rightward movement of the mesenteric root (MR) inferiorly. Consequently, the right infracolic space becomes smaller inferiorly. This favors the dynamics of metastatic seeding in the right lower quadrant in relation to distal ileal loops. AC = ascending colon; DC = descending colon.

(Courtesy of Yong Ho Auh, M.D., Asan Medical Center, Seoul, Korea.)

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Fig. 14–7. Mechanical small bowel obstruction.

(a and b) Erect films in two different cases illustrate the “stepladder” arrangement of dilated obstructed loops. This pattern is related to tension anchored on the root of the mesentery.

It is necessary to recognize the axis of the root of the mesentery and the undulating, changeable nature of the small bowel loops to understand the basis for the radiologic identification of their mesenteric and antimesenteric borders.¹ Figure 14–9 illustrates certain constant geometric properties of the mesentery. The base of the mesentery, from which the jejunum and ileum are suspended, is essentially a series of alternating convexities and concavities connected by intervening limbs. Any single limb is thus shared by a convexity and a concavity on either side. A limb or straight segment of small bowel, therefore, connects one convex loop with the next con-

cave loop. Any curved line presents basically two sur- faces—one convex, the other concave—determined by the point of reference. In the small bowel, the point of reference used is the root of the mesentery. By definition, therefore, the concept of convexity or concavity of bowel loops is determined by the axis of the root of the small bowel mesentery. Figure 14–9, top illustrates that limbs 1 and 2 constitute the convex loop A, limbs 2 and 3 form the concave loop B, and limbs 3 and 4 produce the convex loop C.

Another phenomenon of the ruffled nature of the mesentery and small bowel loops results, depending on positional relationships to the mesenteric root. If rota- tion occurs toward the left (Fig. 14–9, right), there is no essential change in the convex–concave relationships of bowel loops. However, if rotation on the mesenteric root occurs toward the right (Fig. 14–9, left), there may be a complete reversal of these relationships. Figure 14–

9, left shows that now loop A is concave, B, convex; C, concave; etc. It must also be recognized that in vivo the small bowel loops do not act synchronously in rotating in position on the mesenteric root. One coil may be location is difficult to evaluate during routine contrast

studies of the small intestine, chiefly because of the common inaccuracy in tracing the continuity of opacified, superimposed bowel loops.

Identification of Mesenteric

and Antimesenteric Borders of Small

Bowel Loops

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Fig. 14–8. Changeable position of small bowel loops.

(a and b) Radiographs of the intubated small intestine 1 day apart, demonstrating striking variations in the positions of the bowel loops. (X marks the duodenojejunal junction).

(c and d) Tracings illustrate that changes in position and arcing convexities of some bowel segments are more marked than in others.

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Fig. 14–9. Diagram of the ruffled edge of the mesentery.

This immediately suspends the small bowel loops. (Top) Vertical (sagittal). (Left) Rotation to the right. (Right) Rotation to the left. The dashed line indicates the root of the small bowel mesentery.

horizontal (transverse), the next vertical (sagittal), the next in the coronal plane, and the next obliquely ori- ented between any of these three planes. The variability is further increased by the fact that these mesenteric pro- jections may extend toward the left or toward the right and may alternate. Position of the patient, peristaltic dynamics, and factors of intraabdominal pressure are likely determinants.

Thus, several conclusions can be derived from these observations that can be accurately applied in the radiologic–anatomic identification of small bowel loops.¹ Figure 14–10 illustrates these:

1. The concave margin of a small bowel loop, facing toward the axis of the root of the mesentery is the mesenteric border.

This is true whether the loop is positioned to the left or to the right of the mesenteric root. This is shown in segments 1, 2, 5, and 6 in Figure 14–10.

2. The convex margin of a small bowel loop, facing away from the axis of the root of the mesentery, constitutes the anti- mesenteric border. This is also true, of course, whether the

loop projects to the left or to the right of the mesenteric root.*

3. Even if loops are suspended in the midline, their mes- enteric and antimesenteric borders can be identified similarly if they project in the coronal plane. This is shown in segment 3 in Figure 14–10.

4. The precise distinction between mesenteric and antimesenteric borders can be routinely applied in a de- tailed small bowel series (Fig. 14–11). When viewed in a frontal x-ray, a loop projecting in the sagittal or horizontal plane may not present its mesenteric and antimesenteric borders for definition. This occurs most often near the midline overlying the mesenteric root, as shown in segment 4 of Figure 14–10. Pressure films or radiographs with the patient positioned obliquely may render such a loop convex and allow delineation of its mesenteric and antimesenteric borders. Viewed in the axial or sagittal plane, these intestinal borders are easily appreciable on computed tomography or magnetic res- onance imaging (Figs. 14–12 and 14–13).

* It can further be appreciated that consequent to the fixation of the mesenteric ruffles, the convex margin of a bowel loop facing toward the axis of the root of the mesentery may at times also constitute the mesenteric border of that particular loop (Fig. 14–1 and loops A and C in Fig. 14–9b). However, while this may be anatomically true, its radiologic application would be untrustworthy.

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Fig. 14–10. Variable orienta- tions of small bowel loops to mesenteric root.

The mesenteric border (arrows) constitutes the concave margin of a loop facing the root. The antimesenteric border is the convex margin of a loop facing away from the root.

Fig. 14–11. Biphasic enteroclysis study of the small intestine.

Suspended by the fanlike ruffles of the mesentery, the 20–

22 ft of small bowel course in an undulating pattern, resulting in the variously termed coils of bowel or intestinal loops. Each coil or loop presents a concave mesenteric and convex antimesenteric contour. The normal folds are symmetric.

Fig. 14–12. Intestinal borders.

Computed tomography identifies fat-containing leaf of mesentery with vascular branches extending to the concave mesenteric border of small bowel loop (SB).

Normal Radiologic Features 643

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Fig. 14–13. Intestinal borders.

Two different examples of tuberculous peritonitis illustrate the radiation of thickened vessels coursing through the mesentery to the mesenteric borders of multiple small bowel loops.

(a) Axial CT.

(Courtesy of Emil Balthazar, M.D., Bellevue Hospital, New York University School of Medicine, New York, NY.) (b) Sagittal T1-weighted fat suppressed MR image. The terminal intestinal branches (arrows) fan out to the bowel loops. Ascites is present.

(Reproduced from Semelka RC, Ascher SM, Reinhold C:

MRI of the Abdomen and Pelvis. Wiley-Liss, New York, 1997.)

Abnormal Radiologic Features

Diverticulosis of the Small Intestine

Many small bowel abnormalities selectively involve either the mesenteric or antimesenteric borders of small intestinal loops solely or predominantly. Precise radiologic distinction between these margins can localize and diagnose a variety of intraabdominal disease states, which otherwise share many common features. Table 14–1 summarizes the characteristic localization of involvement in a variety of conditions. Application of these principles is particularly helpful at any early stage of the lesion or when there may otherwise be an exten- sive differential diagnosis.

Acquired diverticula of the small bowel are usually multiple and are practically limited to the upper part of the jejunum.³ Examination of a specimen (Fig. 14–14a) documents that the diverticula do not arise randomly from the circumference of the small intestine but are strikingly situated at or immediately alongside the mes-

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Fig. 14–14. Gross specimen of diverticulosis of the jejunum.

(a) The loop is opened by cutting along the antimesenteric border. The multiple diverticula arise in a row distinctly from the mesenteric borders, invaginating between the leaves of the mesentery.

(b) Viewed from the mucosal aspect, the elliptical orifices extend along the line of attachment of the mesentery.

(Reproduced from Meyers.²)

Abnormal Radiologic Features 645

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enteric border, pushing their way between the leaves of the mesentery. The long axis of their domes, as well as of their elliptical orifices (Fig. 14–14b), tends to parallel the longitudinal axis of the bowel. Such diverticula of the small intestine are of the “pulsion” mucous mem- brane type. They arise in relation to the sites of pene- tration of the bowel wall by the vasa recta, which enter on the mesenteric border.⁴

This precise localization of small bowel diverticula to the mesenteric border can be identified radiologically in 75% of cases.² The saccules usually are amorphous, without a mucosal pattern, and characteristically extend from the concave (mesenteric) margins of jejunal loops curved away from the axis of the root of the mesentery (Figs. 14–15 and 14–16). Diverticula of the terminal ileum also follow this pattern (Fig. 14–17).

follows the “rule of twos”: it is present in 2% of people, averages 2 in. in length, and is found in the distal ileum about 2 ft proximal to the ileocecal valve.

The radiologic hallmark of a Meckel’s diverticulum^2,9 is thus based on its identification as a saccule extending precisely from the antimesenteric, convex border of a terminal ileal loop (Figs. 14–19 through 14–22), usually in the right lower quadrant. This can be seen in almost two-thirds of instances.² Because of the variability in position of small bowel loops, the segment from which a Meckel’s diverticulum arises may, at times, project within other areas of the abdomen,¹⁰ but its localization nevertheless to the antimesenteric border can be of great diagnostic value (Fig. 14–23).

Fig. 14–15. Acquired diver- ticula of the small intestine.

Multiple diverticula (Div) project from the mesenteric borders of jejunal loops.

(Reproduced from Meyers.²) A Meckel’s diverticulum represents a remnant of the

omphalomesenteric (vitelline) duct.^5,6 This pouchlike persistence had the same anatomic structure as the re- mainder of the intestine, and thus contains all four his- tologic layers. Meckel’s diverticulum is supplied by the remnants of a nonbranching primitive vitelline artery that arises from an ileal artery^7,8 (Fig. 14–18). It generally

In involvement of the small bowel by scleroderma, muscle atrophy results in atonicity and dilatation. Replace- ment of the atrophied muscle by collagen occurs in a patchy fashion, with perivascular accumulation in the submucosa. Accordion-pleating of the mucosal folds occurs in the face of luminal dilatation, resulting in a typical “hidebound” appearance.¹¹ The individual folds are not thickened. At sites without sclerosis, areas of more normal or atrophic bowel may bulge out between the text continues on page 650

Meckel’s Diverticulum

Scleroderma

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Fig. 14–16. Diverticulosis of the small bowel.

Pressure spot film localizes the diverticula (Div) as specifically arising from the concave, mesenteric border of a jejunal loop.

Fig. 14–17. Diverticulosis of the terminal ileum.

Pressure spot film shows the diverticula arising from the mesenteric border. A few cecal diverticula are also present.

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Fig. 14–18. Vitelline artery supply to Meckel’s diverticu- lum.

Intraoperative selective injection of methylene blue into the vitel- line artery stains the artery (ar- rows) and Meckel’s diverticulum (MD) arising from the antimes- enteric border of the ileum.

There is no staining of the ileum and mesentery.

(Reproduced from Okazaki et al.⁷)

Fig. 14–19. Meckel’s diverticulum.

The saccule (MD) extends from the antimesenteric convex border of a terminal ileal loop. (The filling defects within it in this instance are secondary to calculus formation.) (Reproduced from Meyers.²)

The large saccule (MD) extends from the antimesenteric border of a terminal ileal loop, which it indents in the right lower quadrant of the abdomen.

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Fig. 14–21. Meckel’s diverticulum in an 8-year-old boy with cramping pain and melena.

Enteroclysis demonstrates a large Meckel’s diverticulum arising from the antimesenteric border of distal ileum showing typical junctional fold pattern (arrowhead), with large ulceration in an area of ectopic gastric mucosa (arrow).

TI = terminal ileum; C = cecum.

(Reproduced from Maglinte et al.⁹)

CT demonstrates a 5-cm Meckel’s diverticulum (MD) attached to the antimesenteric side of the ileum. The fibrous remnant of the vitelline duct extends between the diverticulum and the umbilical region.

(Courtesy of Gary Ghahremani, M.D., Evanston, IL.)

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The opacified saccule (MD) attached to the antimesenteric border of a midileal loop (curved arrow) occupies the subhepatic region in the right upper quadrant.

(Courtesy of Gary Ghahremani, M.D., Evanston, IL.)

tethered sections, producing sacculations or pseudodiverticula¹³ (Fig. 14–24). In distinction to true diverticula, these are wide-mouthed and occur on the antimesenteric border. Sacculations are typical of scleroderma, though more commonly seen in the colon than in the small bowel.

Intestinal Duplication

The cystic structure of an intestinal duplication (also called “enteric cyst” or “enterogenous cyst”) may, but

usually does not, communicate with the adjacent intestinal lumen. The muscular coats of the duplication are intimately adherent to and, at times, are microscopically an integral part of the muscularis of the alimentary tract.

Ladd and Gross¹⁴ noted that it arises most often in relationship to the ileum and typically from its mesenteric border. Symptomatology in children includes obstruction, pain, and hemorrhage because of interference with the intestinal blood supply, leading to sloughing of the ileal mucosa. Complete extirpation of the mass along with resection of the adjacent portion of the intestine is thus necessary.

Fig. 14–24. Scleroderma with multiple sacculations.

Small bowel series demonstrates jejunal dilatation, compact appo- sition of normal-sized folds, and multiple wide-mouthed sacculations arising from the antimesen- teric border (arrows).

(Reproduced from Herlinger and Maglinte.¹²)

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With an understanding of the radiologic identification of the mesenteric and antimesenteric borders of small bowel loops, barium contrast studies may be of considerable help in the diagnosis. A noncommunicat- ing intestinal duplication may be revealed as an extrinsic soft-tissue mass displacing an ileal loop upon its mesenteric margin. This precise localization may be seen in 60% of cases.² The lumen of a communicating duplication may be opacified to clearly demonstrate it as a tubular or spherical structure, specifically arising in relationship to the mesenteric border (Fig. 14–25).

Seeded Metastases

The distribution of seeded metastases within the abdomen, as discussed in Chapter 4, has been shown to follow the dynamic pathways of the circulation of ascitic fluid.^15–17 The malignant cells are shed by the primary neoplasm and then transported by the ascites. They are then deposited and subsequently grow as seeded metastases at the sites of stasis or pooling of the ascitic fluid.

In the midabdomen, pooling occurs within the peritoneal recesses of the mesenteric ruffles.¹⁸ Flow occurs in a series of rivulets or cascades from one mesenteric recess to the next lower, with the largest and most consistent pool formed at the termination of the small bowel mesentery at the ileocolic junction. The seeded metastases lodge and grow, therefore, on the mesenteric borders and involve distal ileal loops in over 40% of all cases.¹⁶

The distinctive radiologic feature lies in the localization of changes to the mesenteric border of distal ileal loops, evident in over 75% of seeded metastases in the right lower quadrant of the abdomen.² Mass changes and associated desmoplastic tethering of mucosal folds constitute the basic characteristics. Figure 14–26 illustrates multiple masses indenting the mesenteric borders of individual distal ileal loops in a case of seeded metastases from carcinoma of the ovary. They are strikingly ori- ented in relation to the axis of the small bowel mesentery. The associated desmoplastic response, another sign highly distinctive of seeded lesions,¹⁸ results in angulated tethering of the mucosal folds on the mesenteric borders only. Angulation of the loops themselves at the sites of the serosal masses on the mesenteric borders (Fig. 14–

27) further indicates the desmoplastic process.

Hematogenous Metastases

The vasa recta of the bowel penetrate the wall on the mesenteric border. They then extend intramurally for variable distances before ramifying toward the antimesenteric border to arborize into the rich submucosal plexus.

The most common hematogenous metastasis to the small bowel clinically encountered is metastatic melanoma.¹⁷ Its dissemination can be observed radiologically to follow, at times, the field of a specific arterial distribution.¹⁷ The embolic metastases typically present as

Fig. 14–25. Duplication of terminal ileum.

The intestinal duplication (ID) is identified as a tubular structure without a recognizable mucosal pattern, lying along the mesenteric border of the terminal il- eum (TI) with which it commu- nicates.

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Fig. 14–26. Seeded metastases from ovarian carcinoma.

Multiple masses cause scalloped displacement on the mesenteric borders of ileal loops in the right lower quadrant. Mucosal tethering is also localized to the mesenteric margins.

Note the relationship of these changes to the axis of the small bowel mesentery, indicated by the line of dashes.

submucosal filling defects, often with central ulceration (“bull’s-eye” lesions), within a single or multiple intestinal loops. However, when visualized on one wall of a bowel loop, they are localized precisely to its antimesenteric border (Fig. 14–28) in 80% of cases.² This cor- relates with experimental studies indicating that strictly mechanical and circulatory factors can account for the distribution of some secondary tumors.¹⁹ The radiologic–anatomic observation presumably reflects lodgment and subsequent growth of embolic malignant cells within the smaller arterial arborizations on the antimesenteric border.

Carcinoid Tumors

Almost 90% of intestinal carcinoids occur in the distal ileum.^20,21 Invasion through the intestinal wall may stim- ulate an intense desmoplastic reaction in the surround-

Fig. 14–27. Seeded metastases from carcinoma of the ovary.

Multiple serosal masses indent the mesenteric margins of angulated ileal loops in the right lower quadrant. Luminal narrowing and some desmoplastic angulation result in proximal obstruction.

ing submucosa and mesentery. A characteristic manifes- tation is a mesenteric mass with radiating linear strands²² (Figs. 14–29 and 14–30).

Ileal carcinoids are multiple in approximately one- third of cases.^20,21,25 Most comprise more than three lesions, while in a small percentage dozens of lesions of variable sizes may stud a discrete segment of the bowel.^20,21 Although they may be separated by several centimeters, skip areas are uncommon. These multiple lesions are considered by Warner et al. to be secondary mucosal deposits rather than independent primaries.²⁶ Previously viewed as multicentric neoplastic foci, me- ticulous analysis suggests that the phenomenon reflects mucosal metastases from a dominant parent carcinoid tumor, occurring as a process of retrograde submucosal lymphatic spread. Multiple carcinoid tumors thus show a strong predilection for the antimesenteric border of the small intestine.²⁶

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Fig. 14–28. Hematogenous metastatic melanoma.

A large submucosal mass with a prominent central

ulceration is localized to the convex, antimesenteric margin of a distal jejunal loop.

Fig. 14–29. Carcinoid of the ileum.

CT demonstrates a round 2-cm mesenteric mass with stellate radiation of fibers toward the adjacent mesentery and borders of loops. The wall of the involved loop is thickened and angulated. The mass shows a discrete central calcification, and a small lymph node is present in the adjacent tissue.

(Reproduced from Maccionni et al.²³)

Fig. 14–30. Carcinoid of the ileum.

(a) CT shows a mesenteric mass (arrow) with emanating strands corresponding to thickened neurovascular bundles.

(b) Corresponding gross specimen after surgical resection confirms the mesenteric location of the tumor.

(Reproduced from Pelage et al.²⁴)

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Regional Enteritis

The general radiologic findings of regional enteritis cor- relate closely with the gross pathologic features. The involved bowel, often affected by “skip lesions,” is sharply delimited from contiguous gut and has a narrowed lumen, which is sometimes strictured. The bowel wall is rigid and thick, the mesentery is often markedly thickened and edematous, and the mesenteric lymph nodes are enlarged. The swollen, inflamed mucosa develops a cobblestone appearance as longitudinal and transverse ulcers intersect. As these extend deeply through the wall, sinus tracts and fistulas may be present.

Other specific, more localized changes of regional enteritis have been observed surgically and pathologically. In their pioneering report in 1932, Crohn, Ginz- burg, and Oppenheimer noted on opening the intestine that a series of small linear ulcerations lying in a groove on the mesenteric side of the intestine is almost always present.²⁷ It has also been observed that there is a close relationship between the destructive changes in the mucosa and the extent of increased mesenteric fat.²⁸ The development of pseudodiverticula, furthermore, is probably related to eccentric skip areas.²⁸

I have directly applied these discrete pathologic observations in regional enteritis to the radiologic altera- tions for a more definite diagnosis.^1,2,29 The process may be identified, particularly in its early stages, as localized predominantly to the mesenteric borders of involved loops. Mesenteric border ulcers are a virtually pathog- nomonic finding in approximately 30% of patients with Crohn’s disease.²⁹ The findings of mucosal irregularities, ulcerations, fixation and rigidity, sinus tracts, and extrinsic mass tumefaction may be confined or most evident on the concave margins (Figs. 14–31 through 14–

35). The linear ulcer along the concave border may extend over a few or many centimeters and can be con- tinuous or interrupted. It may be accentuated by a thin line of radiolucency, which reflects inflammatory reaction and fibrosis underneath the ulcer.²⁹ The fact that the antimesenteric wall may not be symmetrically involved at the same time but, rather, retains some degree of pliability may be revealed by the development of pseudosacculations from the convex border.

In severely involved loops, the segmental, skip nature of the lesions may result in pseudosaccular outpouchings from both the mesenteric and antimesenteric borders.

It follows that pseudosacculations or the appearance

Fig. 14–31. Regional enteritis.

Diffuse involvement of ileum. One loop demonstrates ulcerations and small sinus tracts along the concave,mesenteric border at the site of mesenteric tumefaction.

Pseudosacculations on the convex margin of the loop indicate that the antimesenteric border retains some pliability.

The dashed line indicates the axis of the root of the mesentery.

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Fig. 14–32. Regional enteritis in an 11- year-old male.

Small bowel series (a) with pressure spot film of distal ileum (b) show rigidity from the ul- cerative process clearly limited to the mesenteric borders and pseudosaccular outpouchings from the more pliable antimesenteric margins.

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Fig. 14–33. Regional enteritis in two different cases.

(a and b) Flattening and rigidity are conspicuously localized to the mesenteric border of the terminal ileum. The antimesenteric border retains some pliability as shown by pseudosaccular outpouchings.

Fig. 14–34. Regional enteritis.

(a) A linear ulcer (white arrows) can be clearly identified on the rigid mesenteric border of a diseased ileal loop.

It is accentuated by a thin radiolucent line (black arrows) that reflects underlying inflammatory reaction and fibrosis. Pseudosacculations bulge from the antimesenteric border. The distal ileum is narrowed with the diffuse ulceronodular form of Crohn’s disease.

(b) On another view, the linear ulcer (arrowheads) is seen en face.

(Courtesy of Dean Maglinte, M.D., Indianapolis, IN.)

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Fig. 14–35. Regional enteritis, with postsurgical recurrence.

(a) Striking linear ulcers on mesenteric borders (white arrows and black arrows) with pleated pseudosacculations on antimesenteric border.

(b) Nine years later, after surgical resection, there is evident recurrence. Hallmarks again include mesenteric linear ulceration (arrows) and antimesenteric outpouchings.

of diverticula limited solely to the mesenteric borders are not a feature of regional enteritis.

Another sign highly characteristic of Crohn’s disease is also based on discrete radiologic–pathologic correla- tion. Contrast-enhanced spiral CT scans often show vascular changes in the mesentery, manifested as dilatation, tortuosity, and wide spacing of the vasa recta as they approach the mesenteric border of involved ileum. I have termed these distinctive changes the comb sign or vascular jejunization of the ileum³⁰ (Fig. 14–36). Normally, the distal arterial arcades in the mesentery of the ileum are multitiered, so that the vasa recta that arise from the furthest arcade are numerous, short, and closely spaced.

This arterial architecture is in contrast to the jejunum, where the vasa recta are longer and more widely spaced from each other. Increased mesenteric fat, termed fibrofatty proliferation of the mesentery, accompanies transmural involvement of the bowel by Crohn’s disease.

The markedly dilated vessels pass through the hypertro- phied mesenteric and subserosal fat in which perivascular fibrosis develops³¹ (Fig. 14–37). The prominent vasa recta are seen by CT as elongated, widely spaced vessels. Identification of such hypervascularity indicates active disease and is useful in differentiating regional en-

teritis from lymphoma or metastases, which tend to be hypovascular lesions.³⁰

Lymphoma

Within the small bowel, malignant lymphoma involves the distal ileum most often (Fig. 14–38). Growth may be predominantly away from the intestinal lumen, in an exoenteric fashion. Mass extension into the mesentery may produce extrinsic compression of the bowel lumen.

This form of the disease and primary mesenteric lymphoma are characterized radiologically by the presence of mesenteric masses extrinsically compressing and dis- torting the concave borders of small bowel loops (Fig.

14–39).

Intramural and Mesenteric Bleeding

Bleeding into the wall of the small intestine and into the mesentery may be a consequence of many different dis- orders. It is seen in mesenteric thromboses and emboli, segmental ischemic disease, abdominal trauma, antico- agulation medication, underlying diseases associated with

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Fig. 14–36. CT comb sign of Crohn’s disease in two cases.

(a) Spiral CT demonstrates a distal ileal loop with mural thickening, including a curvilinear zone of fluid.

Increased mesenteric fat is present in the right lower quadrant, within which enhanced vessels show dilatation and tortuosity. The vasa recta approaching the mesenteric side of the diseased loop are pushed apart by the fatty proliferation, resulting in the comb sign.

(b) In another patient, an enlarged view demonstrates the conspicuous features of the comb sign.

Fig. 14–37. Crohn’s disease with fibrofatty proliferation and hypervascularity of the mesentery.

(a) Low magnification of cross-sectioned ileum with transmural Crohn’s disease and mesenteric border ulceration (thick arrow). The serosa (small arrows) is displaced from the muscularis propria by an increased accumulation of fat. Transmural fibroinflammatory changes involve vessels and extend into the fat (medium arrows).

(b) Chronic inflammation with subsequent fibrosis extends in a fanlike perivascular pattern (arrows) into the mesenteric fat from the edge of the muscularis propria (arrowheads). (Trichrome stain,

×

^12.)

(Reproduced from Herlinger et al.³¹)

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Fig. 14–38. Hodgkin’s lymphoma.

CT demonstrates mural thickening of an opacified ileal loop in the left lower quadrant strikingly limited to its mesenteric border (arrow). This is accompanied by retroperitoneal adenopathy and stellate infiltration of the mesentery.

Fig. 14–39. Lymphosarcoma.

The process is revealed as masses discretely separating and pressing on the concave mesenteric borders of distal ileal loops in the right lower quadrant.

coagulation defects (hemophilia, leukemia, multiple my- eloma, lymphoma, and metastatic carcinoma), and the vas- culitis of collagen diseases (polyarteritis nodosa, systemic lupus erythematosus), thromboangiitis obliterans (Buer- ger’s disease), and the Henoch-Schönlein syndrome.

While diffuse intramural fluid results in a compact appearance of prominent mucosal folds, sometimes de- scribed as the “stacked-coin” or “picket-fence” arrange-

ment, coalescence of the submucosal edema and hemorrhage produces the characteristic scalloped or nodular filling defects along the contours of the bowel referred to as “thumbprinting.”

These distinctive thumbprint defects in intramural intestinal bleeding are by far most consistently localized to the mesenteric borders of the loops (Figs. 14–40 through 14–42). In advanced cases, the defects may

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Fig. 14–40. Intramural bleeding, secondary to overanticoagulation.

Rectal bleeding in a 56-year-old male on anticoagulants while recovering from a myocardial infarction prompted this small intestinal series. Note that the thumbprint defects (arrows) of coalescent intramural blood are localized specifically to the concave, mesenteric borders. (The dashed line indicates the mesenteric root.) Diffuse submucosal fluid is also present.

Fig. 14–41. Intramural bleeding in a heroin addict.

The thumbprint filling defects (arrows) of intra- mural bleeding are confined to the concave mes- enteric borders. The dashed line indicates the axis of the root of the mesentery. Intramural fluid is also evident.

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Fig. 14–42. Ischemic enteritis.

(a and b) Small bowel series (45 min and 2 hr, respectively) in a female taking oral contraceptive pills show the features of ischemic enteritis involving several ileal loops, with the changes most prominent on their mesenteric borders.

randomly involve both margins of the involved loops, but in early or limited stages, the nodular masses are clearly localized to the concave borders in 75% of patients.² These defects are typically superimposed on a pattern indicating diffuse intramural fluid. If fibrosis pro- gresses, the antimesenteric border then forms multiple

sacculations or pseudodiverticula. Severe involvement may result in a concentric stricture.

Mesenteric bleeding exaggerates and tends to fix the coiled nature of the small intestine. It is further revealed by mass separation and extrinsic compression on the mesenteric borders of the loops (Fig. 14–43).

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Fig. 14–43. (a and b) Two different cases of mesenteric bleeding secondary to Henoch-Schönlein purpura.

Bleeding into the mesentery has resulted in mass separation and displacement upon the concave, mesenteric borders of small bowel loops.

Accompanying intramural fluid is also evident.

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