Spontaneous Intramural Small-Bowel Hematoma: Imaging Findings and Outcome

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1 Maher. bbas 1 Joseph M. Collins 2 Kevin W. Olden 3 Received December 10, 2001; accepted after revision May 20, Department of Surgery, Mayo Clinic, E. Shea lvd., Scottsdale, Z Department of Diagnostic Radiology, Mayo Clinic, E. Shea lvd., Scottsdale, Z ddress correspondence to J. M. Collins. 3 Division of Gastroenterology and Hepatology, Mayo Clinic, Scottsdale, Z JR 2002;179: X/02/ merican Roentgen Ray Society Spontaneous Intramural Small-owel Hematoma: Imaging Findings and Outcome OJECTIVE. Our aim was to review the imaging findings and outcomes of patients with nontraumatic spontaneous intramural small-bowel hematoma. MTERILS ND METHODS. We retrospectively reviewed the records and radiologic studies of 13 patients with known intramural small-bowel hemorrhage. RESULTS. The mean age at presentation was 64 years. Sixty-two percent of patients had warfarin toxicity. The diagnosis was evident on CT performed in all patients. Small-bowel obstruction was present in 85% of patients, and biliary obstruction was present in 8%. single hematoma was present in 85% of patients, and multiple hematomas were present in 15%. The jejunum was the most common site of the hematoma (69%), followed by the ileum (38%) and duodenum (23%). The hematoma extended into the cecum in 15% of patients. The estimated average length of the hematoma was 23 cm, and the shortest segment was 8 cm. Resolution of the hematoma was seen on CT as early as 1 week after onset. Eleven patients (85%) with nonextensive hematomas were dismissed from the hospital without any short- or long-term complications (mean follow-up, 35 months). Two patients with extensive hematomas involving more than half the length of the small intestine died. CONCLUSION. Spontaneous intramural small-bowel hematoma is rare. It occurs in patients who receive excessive anticoagulation with warfarin or who have some other risk factor for bleeding. CT characteristics include circumferential wall thickening, intramural hyperdensity, luminal narrowing, and intestinal obstruction. Early diagnosis is crucial because most patients are treated nonoperatively with a good outcome. N ontraumatic spontaneous intramural small-bowel hematoma, once considered a rare complication of oral anticoagulation therapy, is being reported with increasing frequency [1 12]. Overanticoagulation by warfarin is the most common cause of spontaneous intramural small-bowel hematoma. Other risk factors include hemophilia, idiopathic thrombocytopenic purpura, leukemia, lymphoma, myeloma, chemotherapy, vasculitis, pancreatitis, and pancreatic cancer [13 17]. The presentation of patients who have spontaneous intramural small-bowel hematoma can vary from mild and vague abdominal pain to intestinal tract obstruction and an acute abdomen [1 18]. Often the diagnosis is not suspected clinically and is established only after abdominal imaging or an exploratory laparotomy is performed. ecause of the rarity of spontaneous intramural small-bowel hematoma, no single institution, to our knowledge, has gathered substantial experience treating patients with this condition. Furthermore, the CT and sonographic findings have been reported only rarely [17, 19 22]. The aim of our study was to review the imaging findings and outcomes of patients with spontaneous intramural small-bowel hematoma. With a total of 13 patients gathered from an experience spanning 17 years, we believe this is the largest single series in the medical literature from an institution reviewing this disease. Materials and Methods Thirty-one patients were evaluated at our institution between 1983 and 2000 with the diagnosis of intramural small-bowel hematoma, but only 13 patients were diagnosed with spontaneous and nontraumatic small-bowel hematoma. The study was approved by our institutional review board. The medical records and imaging studies of these 13 patients were reviewed retrospectively. Longterm follow-up information (range, 3 62 months; mean, 35 months) was available for all patients JR:179, December

2 bbas et al. and obtained from the medical records and telephone interviews. Follow-up CT was performed in seven of 13 patients (time interval between original scan and follow-up: range, 2 days 12 months; mean, 3 months). ll initial and follow-up CT examinations were reviewed retrospectively. Results Clinical Presentation and Outcome The mean age at presentation was 64 years (range, years). Risk factors for bleeding were identified in all 13 patients and included overanticoagulation by warfarin in eight patients, hemophilia in one, liver failure after chemotherapy for lymphoma in one, cir- rhosis in one, systemic lupus vasculitis in one, and idiopathic thrombocytopenic purpura in one. ll patients presented with abdominal pain. The average duration of symptoms was 4 days (range, 1 22 days). Eleven patients had emesis. Gastrointestinal tract hemorrhage was noted clinically in three patients. The mean international normalized ratio (INR) at presentation was 11.6 (normal value, 1) in patients receiving warfarin, which indicated overanticoagulation. Only one patient was anemic (hemoglobin level, <12 g/ dl) at presentation, but 11 patients (85%) became anemic within the first 48 hr after admission. Eleven patients were treated medi- cally. Only two patients underwent surgical exploration, one for peritoneal signs and one for an obstructing duodenal mass (hematoma), but none had a bowel resection. Two patients died during hospitalization. oth of these patients had extensive hematomas and sepsis at presentation. One extensive hematoma involved the duodenum and the entire jejunum. The other extensive hematoma stretched from the proximal jejunum to the ascending colon. The other 11 patients (85%) had nonextensive hematomas with an average length of 23 cm. ll these patients were dismissed from the hospital without short-term complications. t Fig year-old woman with atrial fibrillation who received excessive anticoagulation with warfarin (international normalized ratio, 10)., Contrast-enhanced CT scan shows gastric and biliary obstruction. Dilated stomach (curved arrow), distended gallbladder (large straight arrow), and dilated bile and pancreatic ducts (small straight arrows) are evident., CT scan shows unenhancing, large duodenal hematoma (arrow) causing obstruction. Fig year-old woman with atrial fibrillation who received excessive anticoagulation with warfarin (international normalized ratio, 6.8)., CT scan with oral and IV contrast media shows jejunal hematoma with diffuse thickening of mucosal folds (arrows) with luminal narrowing., CT scan with enteroclysis shows picket fence appearance of hematoma (arrow) JR:179, December 2002

3 Imaging of Spontaneous Intramural Small-owel Hematoma the last follow-up (mean, 35 months), four of these patients had died of causes unrelated to the previous spontaneous intramural smallbowel hematoma, and seven patients were alive and well. None of the patients had recurrence of intestinal tract hematoma, abdominal pain, or intestinal tract obstruction. Imaging Findings t presentation, CT was performed in all patients; upper gastrointestinal tract studies with follow-through of the small bowel, in two patients; and enteroclysis, in one patient. Follow-up CT was performed in seven patients, and upper gastrointestinal tract studies were performed in one patient. Diagnosis was evident on CT performed in all patients. Figures 1 8 represent the findings observed in some patients. CT characteristics included circumferential bowel wall thickening, luminal narrowing, and intestinal tract obstruction. Intramural hyperdensity was noted in five pa- tients. stacked-coin appearance was also noted on upper gastrointestinal tract or enteroclysis studies in these five patients. None of our patients had pneumatosis intestinalis or air in the portal circulation. Small-bowel obstruction was present in 11 patients (85%); it was partial in 64% and complete in 36% of this group. iliary obstruction was present in only one patient with a large duodenal hematoma that obstructed the ampulla of Vater. single hematoma was noted in 11 patients (85%), and multiple hematomas (involving separate segments of bowel) were noted in two patients. The jejunum was most commonly involved with the hematoma (69%), followed by the ileum (38%) and the duodenum (23%). The small-bowel hematoma extended into the cecum in two patients. The small bowel was extensively involved with the hematoma in two patients. Intraperitoneal fluid was seen in seven patients. The length of the involved segment (mean, 23 cm) could be estimated from CT per- formed in eight patients. The shortest involved small-bowel segments measured 8 cm and affected the duodenum and the jejunum separately. Follow-up CT scans in seven patients showed resolution of the hematoma without evidence of intestinal obstruction. Resolution of the hematoma was noted on CT as early as 1 week after onset. Discussion In 1904, Sutherland [13] reported a case of a nontraumatic intramural small-bowel hematoma in a child with Henoch-Schönlein purpura presenting with intussusception. few years later, von Khautz [14] diagnosed this condition in a patient with hemophilia. ecause of these early reports, spontaneous intramural small-bowel hematoma has become increasingly recognized as a complication of anticoagulation therapy, bleeding disorders, malignancies, and vasculitis [13 Fig year-old woman with jejunal hematoma due to lupus vasculitis., Contrast-enhanced CT scan shows circumferential thickening in cross-section of jejunal wall with adjacent stranding of mesentery (arrow)., Longitudinal CT scan of jejunal segment shows thickened mucosal folds (arrow). Fig year-old woman with atrial fibrillation who received excessive anticoagulation with warfarin (international normalized ratio, 17.7). Contrast-enhanced CT scan shows jejunal hematoma with circumferential thickening of intestinal wall (arrow) and adjacent mesenteric stranding. Fig year-old man with atrial fibrillation, previous cerebrovascular accident, and deep venous thrombosis who received excessive anticoagulation with warfarin (international normalized ratio, 12). Contrast-enhanced CT scan shows cross-sectional and longitudinal image of thickened wall of jejunum due to intramural hematoma (arrows). 4 JR:179, December

4 bbas et al. 17]. Overanticoagulation by warfarin is the most common risk factor [1 12, 18], and the development of spontaneous intramural small-bowel hematoma has been reported as early as 10 days after initiation of anticoagulation therapy [2]. lthough spontaneous intramural small-bowel hematoma might be expected to occur with overanticoagulation by heparin, we have not observed this finding and have found no reports describing it. Most patients present with spontaneous intramural small-bowel hematoma after having symptoms for several days [1, 2, 5, 7 9, 12, 16, 23 25]. The hemorrhage is usually located in the submucosal layer of the bowel and originates from a small vessel that produces slow bleeding [7, 8]. In addition to intramural bleeding, intraluminal, intramesenteric, and retroperitoneal hemorrhage can occur, especially when the duodenum is involved [12, 16]. Hemorrhagic ascites can be present and is re- lated to leakage of blood from an engorged, thickened, and inflamed bowel wall with submucosal bleeding extending into all layers [1, 2, 4 6, 8, 9, 24, 25]. In our study, spontaneous small-bowel hematomas most often were single lesions and most commonly involved the jejunum, followed by the ileum and the duodenum. These findings are different from those seen in traumatic small-bowel hematomas, which most commonly affect the duodenum [26]. Furthermore, traumatic hematomas of the small bowel tend to be focal. The involved bowel appears longer in spontaneous hematomas than in traumatic hematomas, as shown in our study and in those of others [2, 4, 19]. We saw no spontaneous intramural small-bowel hematoma that was less than 8 cm in length. The average length of a nonextensive intramural hematoma was 23 cm. We find that measuring the length is useful to help distinguish spontaneous intramural small-bowel hematoma from tumor infiltration by metastasis or lymphoma. We would expect that a neoplasm that involves a length of 23 cm of small bowel would have a prominent extramural mass component, which was conspicuously absent from our series of spontaneous smallbowel hematomas. Small-bowel hematomas can extend into the colon, as seen in two of our patients. However, isolated cases of intramural colonic hematomas without small-bowel involvement are rare, and we noted only two patients in a review of 67 published cases [1 9, 11, 12, 15 17, 19 21, 23 25, 27, 28]. We saw no spontaneous hematoma involving only the colon in any of our 13 patients. efore CT, the diagnosis of intramural smallbowel hematoma was made occasionally on upper gastrointestinal tract series and was more Fig year-old man with lymphoma, postchemotherapy pancytopenia, liver failure, and sepsis., CT scan shows extensive small-bowel intramural and intraluminal hemorrhage and hyperdense intramural and intraluminal hemorrhage in cross-section of jejunum (arrows). Hyperdense intraluminal hemorrhage is shown in longitudinal image of thick-walled jejunum (arrowheads). Neither oral nor IV contrast medium was administered. Hyperdense hemorrhage mimics oral contrast medium in bowel lumen., CT scan shows layering of hemoperitoneum in pelvic cul-de-sac (arrows). Fig year-old man with hemophilia, HIV, hepatitis C, and cirrhosis. Unenhanced CT scan shows circumferential thickening of terminal ileum with luminal narrowing and surrounding intraabdominal fluid. rrow indicates ileal hematoma. Fig year-old man with deep venous thrombosis who received excessive anticoagulation with warfarin (prothrombin time, 60 sec). fter patient underwent left hemicolectomy for colon cancer, small intestine extends into fossa of descending colon. Contrast-enhanced CT scan shows cross-sectional view of jejunal intramural hematoma (white arrow) with adjacent dilated segment of jejunum and normal bowel wall (black arrow) JR:179, December 2002

5 Imaging of Spontaneous Intramural Small-owel Hematoma often established only at exploratory laparotomy or autopsy. Several radiographic features were helpful in making the diagnosis. These included a stacked-coin appearance representing a thickening of folds with sharp demarcation and crowding of valvulae conniventes, a picket fence appearance showing spikelike projections of barium between adjacent thickened mucosal folds, abrupt proximal and distal transition points, and luminal narrowing of a rigid and nondistensible segment of intestine [2, 3, 16, 23 25]. However, despite abnormal findings reported in 92.5% of patients with an intramural small-bowel hematoma, findings on barium studies were not necessarily diagnostic or specific for this condition [18, 28]. Several conditions such as lymphoma, inflammatory bowel disease, bowel infarction, and tuberculosis can mimic the findings of intestinal tract hematoma on upper gastrointestinal tract series. Therefore, it is difficult to make a definite diagnosis of this disorder solely from the results of a gastrointestinal tract barium study. dvances in cross-sectional imaging, primarily CT, have contributed to the early and accurate recognition of this condition. Unenhanced CT findings have been reported previously [17] and include homogeneous and symmetric intramural thickening with hyperdense material (30 80 H) in the bowel wall. The hyperdensity of the bowel wall can be seen during the first 10 days after the onset of symptoms and can be helpful in distinguishing this condition from other infiltrative processes that can affect the small bowel, such as malignancy and infection [17]. However, hyperdensity decreases as the hematoma ages and evolves into a hypodense area that can mimic an intramural cystic lesion [17, 22]. In our study, the diagnosis was evident from the CT scans obtained in all patients. Only two patients underwent surgical exploration, and neither of these required bowel resection. s a result, the gold standard of a histologic diagnosis was absent from our patients. The diagnosis of spontaneous intramural small-bowel hematoma is determined from the CT findings of small-bowel wall thickening and obstruction in patients who received excessive anticoagulation or have other increased risks for bleeding and who present with abdominal pain. The diagnosis is confirmed by the spontaneous resolution of the findings on a follow-up CT scan. Complete resolution of the hematoma usually occurs within a few weeks after onset. Imaging studies in the past have documented healing of the intestine within 2 months [2, 19, 25]. In our study, resolution was noted on CT as early as 1 week after onset. Small-bowel lesions persisting for more than 2 months should raise the radiologist s suspicion for other causes. In our opinion, during CT performed on a patient with complete bowel obstruction, it is best to avoid the use of oral contrast material. Water rather than positive oral contrast material can provide detailed images of the gastrointestinal tract. We recommend the use of IV contrast material because it is helpful in the visualization of many gastrointestinal tract disorders (i.e., ischemic or gangrenous gut, Crohn s disease, or malignancy) and does not hinder the ability of the radiologist to make the diagnosis of spontaneous intramural small-bowel hematoma. Despite this recomendaion, many patients in this series received oral contrast material with CT before the diagnosis of bowel obstruction was established. Many patients did not receive IV contrast material because their clinical condition did not allow it. The sonographic appearance of acute intramural small-bowel hematoma has been described and consists of a thickened and echogenic submucosal layer [20, 22]. However, this abnormality is not specific for intestinal tract hematomas and can be seen in a wide spectrum of disorders, including inflammatory bowel disease, pseudomembranous colitis, infectious colitis, ischemic colitis, hemorrhagic infarction, graft-versus-host disease, and mesenteric venous obstruction [22]. Therefore, the utility of sonography for diagnosing this condition is questionable. MR imaging findings of subacute duodenal hematomas have been reported previously [28]. T2-weighted high-signal-intensity ring sign also has been described [28]. However, no data are available on the imaging characteristics of acute intramural hemorrhage or small-bowel hematomas other than those that occur in the duodenum. Furthermore, in view of its higher cost and currently lower temporal resolution, we do not think that MR imaging should be performed as the initial diagnostic study for patients with spontaneous intramural small-bowel hematoma who present with acute abdominal pain. In conclusion, although nontraumatic spontaneous intramural small-bowel hematoma is rare, its incidence is expected to increase as a result of a growing number of patients with hematologic malignancies receiving chemotherapy and an aging population requiring more chronic long-term anticoagulation treatment. Prompt and early recognition of nontraumatic spontaneous intramural small-bowel hematoma by the radiologist is a crucial contribution to patient treatment that may prevent unnecessary exploratory surgery. ll patients with nonextensive intramural hematomas, with an average length of 23 cm, had a good outcome with medical treatment alone and without bowel resection. Patients with extensive intramural hematomas involving more than half the length of the small intestine may represent an important subgroup with a poor outcome. oth our patients with extensive intramural hematomas died. Therefore, if extensive intramural smallbowel hematoma is detected on CT, the radiologist should alert the ordering physician to the seriousness of the patient s condition and recommend aggressive medical treatment. CT findings of small-bowel wall thickening and obstruction in patients presenting with abdominal pain who are undergoing anticoagulation therapy or have other increased risks for bleeding should raise suspicion of spontaneous intramural small-bowel hematoma. lthough mural hyperdensity was present in only five of our 13 patients, we consider this condition pathognomonic of spontaneous intramural small-bowel hematoma when the CT findings of mural hyperdensity occur within an area of circumferential thickening of the small bowel with intestinal obstruction in patients who are overanticoagulated with warfarin. CT is the imaging technique of choice in the diagnosis of spontaneous intramural small-bowel hematoma and can be complemented with barium upper gastrointestinal tract studies with enteroclysis or followthrough of the small bowel. The triad of warfarin toxicity, circumferential thickening of the small bowel, and intestinal obstruction is characteristic of spontaneous intramural small-bowel hematoma and was seen in all patients in this series who were overanticoagulated. References 1. eamish RE, McCreath ND. Intestinal obstruction complicating anticoagulant therapy. Lancet 1961;2: Wiot JF, Weinstein S, Felson. Duodenal hematoma induced by coumarin. JR 1961;86: Silbert, Figiel LS, Figiel SJ. Intramural jejunal hematomas secondary to anti-coagulant therapy. m J Dig Dis 1962;7: Segaul I, Mills M, Wertheimer HM. Intramural hematoma of the small intestine as a complication of anticoagulant therapy. m J Surg 1964; 107: Yvars M, Eckert, Kane. Small bowel obstruction following anticoagulant therapy: report JR:179, December

6 bbas et al. of a case and review of the literature. m J Gastroenterol 1965;44: Killian ST, Heitzman EJ. Intramural hemorrhage of small intestine due to anticoagulants. JM 1967;200: Levine S, Whelan TJ Jr. Small-bowel infarction due to intramural hematoma during anticoagulant therapy. rch Surg 1967;95: Herbert DC. nticoagulant therapy and the acute abdomen. r J Surg 1968;55: Leatherman LL. Intestinal obstruction caused by anticoagulants. m Heart J 1968;76: Macon WL, Morton JH, dams JT. Significant complications of anticoagulant therapy. Surgery 1970;68: vent ML, Canaday R, Sawyer WT. Warfarininduced intramural hematoma of the small intestine. Clin Pharm 1992;11: Gutstein DE, Rosenberg S. Nontraumatic intramural hematoma of the duodenum complicating warfarin therapy. Mt Sinai J Med 1997;64: Sutherland G. Intussusception and Henoch s purpura. r J Dis Child 1904;1: von Khautz. Darmstenose durch submucöse Hämatome bei Hämophilie. rch Klin Chir 1908;87: Kahn, Vandenbogaert N, Cremer N, Fondu P. Intramural hematoma of the alimentary tract in two hemophilic children. Helv Paediatr cta 1977;31: irns MT, Katon RM, Keller F. Intramural hematoma of the small intestine presenting with major upper gastrointestinal hemorrhage: case report and review of the literature. Gastroenterology 1979;77: Lane MJ, Katz DS, Mindelzun RE, Jeffrey R Jr. Spontaneous intramural small bowel haemorrhage: importance of non-contrast CT. Clin Radiol 1997;52: Hughes CE 3rd, Conn J Jr, Sherman JO. Intramural hematoma of the gastrointestinal tract. m J Surg 1977;133: althazar EJ, Hulnick D, Megibow J, Opulencia JF. Computed tomography of intramural intestinal hemorrhage and bowel ischemia. J Comput ssist Tomogr 1987;11: Yoshino MT. Duodenal hematoma: CT demonstration of the ring sign. Gastrointest Radiol 1987;12: Plojoux O, Hauser H, Wettstein P. Computed tomography of intramural hematoma of the small intestine: a report of 3 cases. Radiology 1982;144: Frisoli JK, Desser TS, Jeffrey R. Thickened submucosal layer: a sonographic sign of acute gastrointestinal abnormality representing submucosal edema or hemorrhage. JR 2000;175: Culver GJ, Pirson HS, Milch E, erman L, brantes FJ. Intramural hematoma of the jejunum: a case report. Radiology 1961;76: Sears D, Hawkins J, Kilgore, Miller JE. Plain roentgenographic findings in drug induced intramural hematoma of the small bowel. JR 1964;91: Senturia HR, Susman N, Shyken H. The roentgen appearance of spontaneous intramural hemorrhage of the small intestine associated with anticoagulant therapy. JR 1961;86: Jones WR, Hardin WJ, Davis JT, Hardy JD. Intramural hematoma of the duodenum: a review of the literature and case report. nn Surg 1971;173: arnes CG, Duncan GW. naphylactoid purpura simulating acute regional ileitis. r J Surg 1941;29: Hahn PF, Stark DD, Vici LG, Ferrucci JT Jr. Duodenal hematoma: the ring sign in MR imaging. Radiology 1986;159: JR:179, December 2002

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