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Gastrointestinal Imaging |
1 From the Departments of Radiology (V.J.S., M.S.L., H.H., M.W.), Pathology and Laboratory Medicine (E.E.F.), and Obstetrics and Gynecology (R.W.T.), Hospital of the University of Pennsylvania, 3400 Spruce St, Philadelphia, PA 19104. Received March 5, 1999; revision requested May 28; revision received June 14; accepted June 20. Address reprint requests to M.S.L. (e-mail: levine@oasis.rad.upenn.edu).
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Abstract |
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MATERIALS AND METHODS: A search of radiology files revealed five patients with surgically proved endometriotic implants in the ileum at enteroclysis (three patients), at small-bowel follow-through (one patient), and at double-contrast barium enema study (one patient). The radiographic findings were reviewed retrospectively. Clinical, surgical, and histopathologic findings were also reviewed.
RESULTS: All five patients were nulliparous women (mean age, 34.4 years; age range, 28–41 years). Four patients presented with abdominal and/or pelvic pain, but only one of these four had cyclic pain that coincided with menstruation. Barium studies revealed endometriotic implants in the terminal ileum within 10 cm of the ileocecal valve in four patients and in the midileum in one. The radiographic findings consisted of extrinsic mass effect with variable spiculation and tethering of folds in two patients, annular lesions with spiculated folds and abrupt or tapered borders in two, and a plaquelike lesion in one. In four patients who underwent double-contrast barium enema studies, associated endometriotic implants were found in the rectosigmoid colon.
CONCLUSION: Ileal endometriosis usually involves the terminal ileum within 10 cm of the ileocecal valve and manifests as a spectrum of findings on barium studies. Ileal endometriosis should therefore be considered when these findings are present in young, nulliparous women with abdominal or pelvic pain.
Index terms: Endometriosis, 742.318 • Ileum, 742.1271, 742.318 • Intestines, radiography, 742.1271
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Introduction |
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It is surprising, however, that the radiographic findings of small-bowel endometriosis have not been well documented. To our knowledge, the English-language radiology literature contains only one anecdotal description (2) of an endometriotic implant in the small bowel that was found at enteroclysis.
Since 1984, we have encountered five patients with surgically proved small-bowel endometriosis in whom barium studies were performed. The purpose of our study was to assess the clinical and radiographic findings in a series of patients with ileal endometriosis and to correlate this information with previously reported findings.
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MATERIALS AND METHODS |
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The small bowel was evaluated with enteroclysis (Entero-H; E-Z-Em, Westbury, NY) in three patients, with small-bowel follow-through (Entrobar; E-Z-Em) in one, and with double-contrast barium enema study (Polibar Plus; E-Z-Em) with retrograde filling of the terminal ileum in one. Double-contrast barium enema studies were also performed in two patients who underwent enteroclysis and in one who underwent small-bowel follow-through. The radiographs from all of these examinations were reviewed retrospectively by a consensus panel of three of the authors (V.J.S., M.S.L., H.H.) (all gastrointestinal radiologists).
In the patients with ileal implants, the radiographs were evaluated for extrinsic mass effect, spiculation or tethering, plaquelike lesions, or circumferential narrowing of the bowel. Ileal lesions were classified either as involving the terminal ileum within 10 cm of the ileocecal valve or as involving the more proximal ileum. The diameters of these ileal implants also were measured.
In patients with colonic endometriosis, the radiographs were evaluated for extrinsic mass effect, flattening, tethering, or circumferential narrowing of the rectosigmoid colon, cecum, or other areas of the colon. The radiographic findings were subsequently correlated with the surgical and histopathologic findings by one of the authors (V.J.S.). Medical records were also reviewed to determine the clinical history and presentation in these patients.
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RESULTS |
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Other symptoms with which these four patients presented included nausea and vomiting in one patient, rectal bleeding in one, dysmenorrhea in one, and dyspareunia in two. The remaining patient was found unexpectedly to have ileal endometriosis during a laparoscopic procedure performed because of infertility. All five patients were known to have endometriosis at the time of the barium studies.
Radiographic Findings
Four of the five patients had endometriotic implants that involved the terminal ileum within 10 cm of the ileocecal valve. The remaining patient had an implant that involved the midileum on the left side of the pelvis. These small-bowel implants had a mean diameter of 3.6 cm (range, 3–5 cm).
Ileal endometriosis manifested as extrinsic mass effect at enteroclysis and at small-bowel follow-through in two patients (Figs 1, 2), as annular lesions at double-contrast barium enema studies and at enteroclysis in two (Figs 3, 4a), and as a plaquelike lesion at enteroclysis in one (Fig 5). In the two patients with extrinsic mass effect in the ileum, there was variable spiculation and tethering of folds (Figs 1, 2). One of these patients had a second area of mass effect and tethering on the medial border of the cecum because of a concomitant cecal implant (Fig 1).
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In four patients, double-contrast barium enema studies revealed associated colonic endometriosis that manifested as extrinsic mass effect, flattening, and spiculation of the anterior border of the rectosigmoid colon (Fig 4b). As discussed previously, one patient also had involvement of the medial border of the cecum at enteroclysis (Fig 1).
Surgical and Histopathologic Findings
Four of the five patients underwent laparotomy; endometriotic implants were found in the ileum in all four. In three of these patients, ileal or ileocecal resection was performed. Histopathologic examination of the resected specimens revealed endometriosis that involved the serosa and the muscularis propria of the diseased ileum in all three patients. In the fourth patient, resection was not performed, but examination of surgical biopsy specimens revealed endometriosis that involved the serosa of the diseased ileum. One of these four patients also underwent resection of the sigmoid colon; a pathologically proved endometriotic implant was found in the resected sigmoid colon.
In the remaining patient, the gross laparoscopic findings were compatible with an endometriotic implant that involved the midileum, but no resection was performed and no biopsy specimens were obtained.
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DISCUSSION |
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The most commonly accepted theory of pathogenesis is that endometriotic tissue refluxes through the fallopian tubes during menstruation and becomes implanted on the serosal surfaces of abdominal and pelvic organs (3,5). Alternatively, extrauterine growth of endometriotic tissue could occur as a result of metaplastic transformation of pluripotential peritoneal mesothelium (3).
Endometriotic implants usually involve the pelvic peritoneum and reproductive organs, which include the ovaries, fallopian tubes, and rectovaginal septum. However, the gastrointestinal tract is involved by endometriosis in approximately 12% of cases (1).
The rectosigmoid colon is the major site of gastrointestinal involvement and accounts for 85% of cases (1). Rectosigmoid endometriosis usually manifests on double-contrast barium enema studies as extrinsic mass effect, flattening, tethering, and/or spiculation of the anterior border of the rectosigmoid colon (Fig 4b) (3,6). Similar findings may be present in the proximal sigmoid colon or even in the cecum. Much less commonly, colonic disease may be manifest as an annular lesion or as a polypoid intraluminal mass (3,6).
Although the rectosigmoid colon is by far the most common site of gastrointestinal involvement, endometriosis may also affect the small bowel. In various series (1,7), endometriotic implants were found in the ileum at surgery in 1%–7% of patients with this disease. As in our series, most cases involved the terminal ileum within 10 cm of the ileocecal valve (8). On occasion, however, endometriotic implants have been documented in the proximal ileum (7) or even in the jejunum as far proximally as 30 cm from the duodenojejunal junction (9).
In previous studies (7,8,10–13), women with ileal endometriosis presented most commonly with signs or symptoms of acute, chronic, or intermittent small-bowel obstruction. In our series, however, only one patient had clinical signs of intestinal obstruction; the most common symptom at presentation instead was abdominal and/or pelvic pain. This discrepancy may be partly related to enteroclysis and to careful fluoroscopic palpation of the ileum, which allowed a radiographic diagnosis to be made before small-bowel obstruction occurred.
In previous studies (14–16), some patients also presented with right-lower-quadrant pain, diarrhea, and/or fever, so that the clinical findings mimicked those of Crohn disease or even of appendicitis.
All five of our patients with ileal endometriosis had a known history of endometriosis at the time of the barium studies. In other series (7,9,13), however, ileal endometriosis was usually diagnosed at surgery in patients who were not suspected previously of having this disease. Furthermore, the classic findings of cyclic pain or of other symptoms that coincide with menses has been seen in only 18%–40% of patients with endometriotic implants in the small bowel (15). As a result, ileal endometriosis has rarely been diagnosed preoperatively in patients with this disease in previous reports.
Although endometriotic implants in the ileum have been well documented at surgery, we are aware of only one anecdotal description (2) in the radiology literature of ileal endometriosis, in which a submucosal mass was found in the terminal ileum at enteroclysis.
In contrast, we describe a series of five patients with ileal endometriosis in whom barium studies revealed a spectrum of findings; these included extrinsic mass effect with spiculation and tethering of folds (Figs 1, 2), annular lesions with spiculated folds and abrupt or tapered borders (Figs 3, 4a), and one plaquelike lesion (Fig 5). In our experience, the radiographic findings caused by endometriotic implants in the ileum are therefore similar to those caused by endometriotic implants in the colon.
The pathologic basis for the findings of ileal endometriosis at barium study has been well documented. Endometriotic tissue in the ileum (like endometrial tissue in the uterus) undergoes cyclic hormonal changes, with periodic hemorrhage. When the muscularis propria is involved, there is marked muscular hypertrophy and a desmoplastic response in the wall of the bowel (10,15). This muscular hypertrophy and fibrotic reaction are presumably responsible for the narrowing, tethering, and/or spiculation of the ileum seen on barium studies.
When ileal endometriosis manifests as extrinsic mass effect and tethering, intraperitoneally seeded metastasis to the ileum should be a leading consideration in the differential diagnosis (17). Acute appendicitis with a periappendiceal abscess may also manifest as an extrinsic mass effect and spiculation of the adjacent terminal ileum (18). However, knowledge of the patient's clinical history is extremely helpful for differentiating these conditions, as intraperitoneal metastases usually occur in women older than 60 years who have known gynecologic cancers, pelvic masses, and/or ascites, whereas acute appendicitis usually occurs in men or women with abdominal pain, tenderness, fever, and/or leukocytosis. In contrast, endometriosis occurs typically in young, nulliparous women with abdominal or pelvic pain.
When endometriotic implants in the small bowel manifest as true annular lesions in the ileum, the differential diagnosis includes various malignant tumors. Primary carcinomas of the small bowel may also appear as annular lesions, but these tumors are usually associated with mucosal destruction and shelflike, overhanging borders and are more commonly located in the proximal part of the small bowel (17). In contrast, annular metastases usually cause marked luminal narrowing and angulation, are often accompanied by high-grade obstruction, and are not confined to the distal ileum (19). Lymphomas and carcinoid tumors that circumferentially encase the small bowel could conceivably produce similar findings (17), but the correct diagnosis may be suggested on the basis of the clinical history and presentation.
Finally, plaquelike lesions in the ileum could be mistaken for plaquelike carcinomas on barium studies. However, the possibility of endometriosis should be considered when this finding is detected in young, nulliparous women with lower abdominal or pelvic pain or with other gastrointestinal symptoms, particularly if these symptoms are exacerbated at the time of menses.
In our study, all four patients with ileal endometriosis who underwent double-contrast barium enema studies had associated endometriotic implants in the rectosigmoid colon. In a review of the literature, however, as many as 75% of patients with ileal endometriosis had isolated small-bowel disease without colonic involvement (20). Therefore, it is important to recognize that ileal endometriosis can occur in the absence of colonic disease.
Unfortunately, our study was limited by the small number of cases in our series. It also was difficult to determine our radiographic sensitivity in diagnosing ileal endometriosis because of the inherent limitations of our retrospective study design. Additional investigation is therefore needed to further delineate the spectrum of radiographic findings associated with ileal endometriosis.
When the diagnosis of ileal endometriosis is established, affected patients may be treated medically with drugs such as danazol, a potent pituitary gonadotropin inhibitor (15). However, patients with obstructive implants in the ileum usually require surgical resection of the involved bowel, with an end-to-end anastomosis (13,15).
In summary, we have reported on four patients with endometriotic implants in the terminal ileum within 10 cm of the ileocecal valve and one patient with an implant in the midileum. Ileal endometriosis may manifest on barium studies as an extrinsic mass effect with spiculation and tethering of folds, as annular lesions with spiculated folds and abrupt or tapered borders, or as plaquelike lesions in the terminal ileum. Ileal endometriosis therefore should be considered when these findings are present in a young, nulliparous woman with abdominal or pelvic pain.
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Footnotes |
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Author contributions: Guarantor of integrity of entire study, M.S.L.; study concepts, V.J.S., M.S.L., H.H.; study design, V.J.S., M.S.L.; definition of intellectual content, V.J.S., M.S.L.; literature research, V.J.S.; clinical studies, M.S.L., H.H.; data acquisition, V.J.S., M.W., E.E.F.; data analysis, V.J.S., M.S.L.; manuscript preparation, V.J.S., M.S.L.; manuscript editing and review, H.H., M.W., E.E.F., R.W.T.
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This article has been cited by other articles:
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  M. S. Levine, S. E. Rubesin, and I. Laufer Pattern Approach for Diseases of Mesenteric Small Bowel on Barium Studies Radiology, November 1, 2008; 249(2): 445 - 460. [Abstract] [Full Text] [PDF]
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 N. Faccioli, R. Manfredi, P. Mainardi, E. D. Chiara, E. Spoto, L. Minelli, and R. P. Mucelli Barium Enema Evaluation of Colonic Involvement in Endometriosis Am. J. Roentgenol., April 1, 2008; 190(4): 1050 - 1054. [Abstract] [Full Text] [PDF]
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M. Macari, A. J. Megibow, and E. J. Balthazar A Pattern Approach to the Abnormal Small Bowel: Observations at MDCT and CT Enterography Am. J. Roentgenol., May 1, 2007; 188(5): 1344 - 1355. [Abstract] [Full Text] [PDF]
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