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provided by Elsevier - Publisher Connector Pediatrics and Neonatology (2011) 52, 214e218

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ORIGINAL ARTICLE Intestinal Angiodysplasia: An Uncommon Cause of Gastrointestinal in Children

Feng-Ju Chuang a,b, Jen-Shyang Lin a, Chun-Yan Yeung b, Wai-Tao Chan b, Chuen-Bin Jiang b, Hung-Chang Lee a,c,*

a Department of Pediatrics, Chia-Yi Christian Hospital, Chiayi, Taiwan b Department of Pediatrics, Mackay Memorial Hospital, Taipei, Taiwan c Department of Pediatrics, Taipei Medical University, Taipei, Taiwan

Received Jul 13, 2009; received in revised form Sep 21, 2010; accepted Sep 24, 2010

Key Words Background: Angiodysplasia of the gastrointestinal (GI) tract is recognized as an important angiodysplasia; cause of lower GI bleeding in elderly. It usually involves the and right colon in adults. lower GI bleeding Unlike the adult group, there has been little experience with the pediatric population. Methods: From July 2004 to October 2008, patients presenting at the Mackay Memorial Hospital with GI hemorrhage diagnosed as angiodysplasia by helical computed tomographic angiography were reviewed. Results: Eighteen patients (14 boys and 4 girls) with mean age of 7.1 years (range, 1 month to 17 years) were diagnosed. The time from initial clinical onset to diagnosis of angiodysplasia ranged from 1 week to 11 years, most around 1e2 weeks. All patients except one had and an average hemoglobin level of 7.9 Æ 2.1 g/dL. The most commonly involved areas were and terminal . Four patients received treatment with resection of affected segments. Conclusions: In pediatric patients, angiodysplasia is a rare cause of GI bleeding and may be delayed in diagnosis. This diagnosis should be considered when patients have recurrent GI bleeding. In this study, the final surgical and pathological diagnosis was made in 6 of 18 patients. In six patients, computed tomographic angiography had 66% diagnostic accuracy for angiodysplasia (four of six patients who received operation were compatible with angiodys- plasia by confirmation of histology). Copyright ª 2011, Taiwan Pediatric Association. Published by Elsevier Taiwan LLC. All rights reserved.

* Corresponding author. Department of Pediatrics, Mackay Memorial Hospital, 92, Section 2, Chung Shan North Road, Taipei 10449, Taiwan. E-mail address: [email protected] (H.-C. Lee).

1875-9572/$36 Copyright ª 2011, Taiwan Pediatric Association. Published by Elsevier Taiwan LLC. All rights reserved. doi:10.1016/j.pedneo.2011.05.002 Intestinal angiodysplasia 215

1. Introduction our knowledge, this study has the largest series of pediatric cases in Taiwan at present. There are many causes of gastrointestinal (GI) bleeding in children. Some span the whole pediatric age range, 2. Materials and Methods whereas others reflect congenital malformations and present with bleeding in early childhood. Unlike anal We retrospectively reviewed patients who had maroon- fissure, necrotizing , intussusception, polyps, colored stool, , hematochasia, and iron-deficiency and Meckel’s diverticulum, angiodysplasia is not typically anemia with positive result of occult blood from 2004 to considered as a cause of GI bleeding in children, and 2008 patients presenting at the Mackay Memorial Hospital. 1 delayed diagnosis has been reported. Angiodysplasia, also Only patients from newborn to 18 years old who had referred to as vascular ectasia, is recognized as an impor- bleeding in the GI tract and were diagnosed with angiodys- 2 tant cause of lower GI bleeding in the elderly. plasia by helical CTA were enrolled (Table 1). We evaluated Angiodysplasia can affect any segment of the GI tract. for clinical manifestation, radiological images, and surgical The right hemicolon and cecum are the most commonly parameters. Data include gender, age of onset of symptoms. 2e6 affected sites in adults. However, there has been little Laboratory studies include conventional hematological tests experience with the pediatric population. Computed (Table 1) and radiological studies of CTA (Table 2). tomographic angiography (CTA) is a sensitive, specific, and All scans were obtained with a Multislice CT (Siemens noninvasive tool for the diagnosis of angiodysplasia. This Somatom Sensation 16 Multislice CT), under the following retrospective study evaluates the clinical manifestations, conditions: 120 kVp; slice width, 0.75e1 mm; scanning time images, and treatments of angiodysplasia in 18 children. To was dependent on the length of the study. In all cases, maximum-intensity projection of the region of interest was used to obtain most highly attenuated structures. Table 1 Patient demographics and clinical outcomes The CTA studies were interpreted according to the criteria used by accumulation of ectatic vessels within the Variables N Z 18 bowel wall; early filling vein, which is the presence of Age (y) a single vein in arterial phase when no other veins are seen; Mean Æ SD 7.1 and enlarged arteries of the target area.7 Operative spec- Median (range) 6.2 (1e17) imens were reviewed for histological confirmation of angiodysplasia. Gender, n (%) Male 14 (77.8) Female 4 (22.2) 3. Results Symptoms, n (%) Eighteen patients (14 boys and 4 girls) with a mean age of Anemia 17 (94.4) 6.6 Æ 5.6 years (range, 1 month to 17 years) were diagnosed Abdominal pain 10 (55.6) 9 (50.0) Melena 9 (50.0) Infection 9 (50.0) Table 2 Location of angiodysplasia by computed tomo- Underlying disease 4 (22.2) graphic angiography Hemoglobin (g/dL) Case No. of Site of involvement Mean Æ SD 7.9 Æ 2.1 no. affected Median (range) 7.35 (4.9e12.9) sites 1 Multiple Ileum Time to diagnosis (wk) 2 Multiple Upper and distal Mean Æ SD 39.3 Æ 133.9 3 Multiple Terminal ileum and ascending colon Median (range) 1.0 (0.6e572) 4 Multiple Terminal ileum and ascending colon , n (%) 5 Multiple Left colon Yes 11 (61.1) 6 Multiple Ileum and ascending colon No 7 (38.9) 7 Multiple Ileum and ascending colon 8 Multiple Terminal ileum and ascending colon Operation, n (%) 9 Multiple Jejunum Yes 6 (33.3) 10 Multiple Terminal ileum and ascending colon No 12 (66.7) 11 Multiple Ileum and ascending colon Location, n (%) 12 Multiple Ileum and proximal ascending colon Terminal ileum 11 (61.1) 13 Multiple Ascending colon Ascending colon 10 (55.6) 14 Multiple Terminal ileum Jejunum 3 (16.7) 15 Multiple Ileum and ascending colon Left colon 2 (11.1) 16 Multiple Jejunum 1 (5.6) 17 Multiple Rectum 18 Multiple Left colon SD Z standard deviation. 216 F.-J. Chuang et al

Figure 1 Symptoms of 18 angiodysplasia cases. with angiodysplasia by CTA from 2004 to 2008. The average Figure 3 Location of 18 angiodysplasia cases. follow-up time was 33 months. The most common symptom was anemia (94.4%), followed by abdominal pain (55.6%), hematochezia (50.0%), melena (50.0%), and infection had Meckel’s diverticulum. The other one had no finding by (50.0%) (Figure 1). Moreover, four patients had other histological studies. Moreover, four of these patients had underlying diseases (3 had GI anomaly and 1 had immuno- recurrent bleeding after operation because of incomplete deficiency). The mean hemoglobin level was 7.9 Æ 2.1 g/dL. resection. Eleven patients had blood transfusion (61.1%). In The median duration between clinical onset and diagnosis patients without surgery, only one needed repeat blood of angiodysplasia was 1 week (ranged from 1 week to 11 transfusion, and the others had normal hemoglobin levels years). Ten patients received nuclear bleeding scan, and and no occult blood in the stools after follow-up (Table 1). only two showed positive findings. Eight patients accepted endoscopic examination. The 4. Discussion results of were as follows: three patients had nonspecific endoscopic findings, four patients had , Angiodysplasia is a thin-walled, dilated, punctuate red and one patient had angiodysplasic lesions (Figure 2); vascular structure in the mucosa or submucosa of the bowel. moreover, showed that one patient had Angiodysplasia is recognized as an important cause of acute edematous changes at terminal ileum and another had and chronic GI bleeding. Most cases of angiodysplasia are many blood clots. In all cases, the lesions were located detected in patients who are older than 60 years and have and identified by CTA (Table 2). no sexual predilection.8,9 Very few pediatric cases of The most common affected areas were the ascending angiodysplasia are available in the English literatures.1 The colon and terminal ileum (61.1%) (Figure 3). Six patients lesions have varied clinical expressions, and lower intestinal (33.3%) underwent operation to reset the affected bleeding is the most common problem. Endoscopy and segments because of recurrent bleeding and unstable angiography still are standard diagnostic modalities for hemodynamic status. Four of them were compatible with angiodysplasia; however, these two modalities seem too angiodysplasia by confirmation of histology. One of them invasive in pediatric populations. As in the adult group, the most commonly involved areas in our children were the ascending colon and terminal ileum. Thus, the lesion in the could be because of a limitation of the endoscope. In previous studies, the sensitivity of colonoscopy was 68e80%, and the specificity was 90%.7 In our study, only one of eight patients was diagnosed by endoscopy. CTA is a sensitive, specific, and minimally invasive tool for the diagnosis of angiodysplasia.7,10 Presence of ectatic, dilated vessels in the wall of intestine, early filling vein, and enlarged ileocolic artery are the diagnostic criteria (Figure 4). Junquera et al7 reported that the sensitivity, specificity, and positive predictive values of CTA for the detection of colonic angiodysplasia were 70%, 100%, and 100%, respectively. In this study, the final surgical and pathological diagnoses were made in 6 of 18 patients. In these six patients, CTA had 66% diagnostic accuracy of angiodysplasia (four of six patients who underwent opera- Figure 2 A 7-year-old boy had tarry stool for days. Pan- tion were compatible with angiodysplasia by confirmation endoscopy showed multiple cherry red flat spots in the gastric of histology) (Table 3). mucosa, compatible with the findings of angiodysplasia in In our study, the mean age at the time of diagnosis was computed tomographic angiography. 7.1 years (range, 1 month to 17 years), and the patients Intestinal angiodysplasia 217

The shortening of diagnosis time may be the result of the improvement of diagnostic modalities. Angiodysplasia can involve any segment of the intestinal tract,11 but is almost always confined to the cecum or ascending colon, usually in multiple rather than single sites. The exact mechanism of development of angiodysplasia is not known. Angiodysplasia developing in response to chronic low-grade venous obstruction is the predominant hypothesis and is consistent with the high prevalence of these lesions in the right colon where wall tension is the highest.2,12,13 de la Torre Mondragon et al1 reported that the left hemicolon was the most frequently affected and suggested that the pathophysiology appears to be different in pediatric groups. However, in our study, the ascending colon and terminal ileum were the most commonly affected sites, the same as in adult groups. These results are compatible with the hypothesis describing high wall tension of the right colon. Four patients had other underlying diseases (3 had GI anomalies and 1 was immunocompro- mised), which seems to support the other hypothesis that angiodysplasia is a congenital anomaly.14 Clinical managements depend on severity of bleeding, hemodynamic stability, and recurrence of symptoms. Bleeding stops spontaneously in more than 90% of patients but often recurs despite treatment.15e17 Two patients had recurrent bleeding after operation in our study. This has been attributed to incomplete resection, a second, different 3,18e22 Figure 4 A 2-year-old boy had anemia for half a year. lesion, or a new angiodysplasia. In our study, among Computed tomographic angiography showed early filling of the the patients who did not undergo surgery, only one needed left ileocolic vein (arrows). Angiodysplasia was diagnosed. He repeated blood transfusions, and the others had normal underwent operation because of unstable hemodynamic status. hemoglobin level and no occult blood in stools during follow- Pathological findings were compatible with angiodysplasia. up; thus, in patients with stable hemodynamic status, supportive treatment is suggested. Angiodysplasia is a rare but important cause of recurrent were predominantly males. The age of the children in intestinal bleeding in children. Delayed diagnosis has been previously reported cases ranged from newborn to 15 years, reported. Early diagnosis of these rare lesions is important males being more commonly affected.1 to avoid a possible fatal outcome. In our study, CTA had Unlike anal fissures, necrotizing enterocolitis, intussus- 66% diagnostic accuracy for angiodysplasia in six patients ceptions, polyps, and Meckel’s diverticulum, angiodysplasia who underwent operation and had the ability to display the is not considered as a common cause of GI bleeding in aberrant morphology of these common vascular lesions, children. Delayed diagnosis had been reported. In adult providing a choice for diagnosis. This examination is safe, cases, a delay in diagnosis of more than 3 years from onset noninvasive, well tolerated, and widely available. It can be an of symptoms had been reported.2 In our study, one patient, appropriate diagnostic alternative in the study of GI bleeding a 12-year-old girl, had several episodes of tarry stool since 6 when endoscopy fails to establish the diagnosis, avoiding months of age. All imaging studies, including endoscopy and invasive catheter angiography. Thus, CTA may become the nuclear bleeding scan, showed negative findings. Angio- technique of choice for primary diagnosis of GI bleeding. dysplasia was diagnosed by CTA in 2005. There was no more However, one limitation in this study needs to be speci- tarry stool noted after the patient received surgical fied. This study was a retrospective investigation with only resection. The time since clinical onset to diagnosis of a small number of patients; this may have introduced bias into angiodysplasia ranged from 1 week to 11 years in our study. our results. Thus, prospective comparative studies with other

Table 3 Finding of operation Patient Operative finding Pathology A Large Meckel’s diverticulum Meckel’s diverticulum B of terminal ileum Compatible with angiodysplasia C Angiodysplasia over ascending colon and ileum Compatible with angiodysplasia D Edematous bluish wall of terminal ileum with blood in lumen Compatible with angiodysplasia E Hyperemic serosa and engorged small artery of ileum Compatible with angiodysplasia F None None 218 F.-J. Chuang et al intestinal modalities are required to establish the definitive 11. Whitehouse GH. Solitary angiodysplastic lesions in the ileoce- role of CTA in the evaluation of vascular lesions of the gut. cal region diagnosed by angiography. Gut 1973;14:977e82. 12. Moore JD, Thompson NW, Appleman HD, Foley D. Arteriove- nous malformation of the . Arch Surg References 1976;111:381e8. 13. De Diego JA, Molina LM, Diez M, et al. Intestinal angiodysplasia: 1. de la Torre Mondragon L, Vargas Gomez MA, Mora Tiscarreno MA, retrospective study of 18 cases. Hepatogastroenterology 1988; Ramirez Mayans J. Angiodysplasia of the colon in children. 35:586e93. J Pediatr Surg 1995;30:72e5. 14. Hemingway AP, Allison DJ. Angiodysplasia and Meckel’s diver- 2. Boley SJ, DiBiase A, Brandt LJ, Sammartano RJ. Lower intes- ticulum: congenital association? Br J Surg 1982;69:403e96. tinal bleeding in the elderly. Am J Surg 1979;17:57e64. 15. Hutcheon DF, Kabelin J, Bulkely GB, Smith GW. Effect of 3. Meyer CT, Troncale FJ, Galloway S, Sheahan DG. Arteriovenous therapy on bleeding rates in gastrointestinal angiodysplasia. malformations of the bowel: an analysis of 22 cases and review Am J Surg 1987;53:6e9. of the literature. 1981;60:36e48. 16. Lee EW, Laberge JM. Differential diagnosis of gastrointestinal 4. Baum S, Nusbaum M, Blakemore WS, Finkelstein AK. The bleeding. Tech Vasc Interv Radiol 2004;7:112e22. preoperative radiographic demonstration of intra-abdominal 17. Erdozain Sosa JC, Boixeda de Miquel D, Pe´rez-Herna´ndez F, bleeding from undetermined sites by percutaneous selective et al. Intestinal angiodysplasia: a presentation of 7 cases and celiac and superior mesenteric arteriography. Surgery 1965;58: review of the literature. Rev Esp Enferm Apar Dig 1989;75: 797e805. L661e4. 5. Phillips JF, Yao JS. Congenital vascular malformations. In: 18. Rutgeerts P, Van Gompel F, Geboes K, Vantrappen G, Neiman HL, editor. Angiography of . New York, Broeckaert L, Coremans G. Long term results of treatment NY: Churchill Livingstone; 1985. p. 393e419. of vascular malformations of the gastrointestinal tract by 6. Hemingway AP. Angiodysplasia as a cause of iron deficiency neodymium YAG laser photocoagulation. Gut 1985;25:586e93. anaemia. Blood Rev 1989;3:147e51. 19. Cooperman AM, Kelly KA, Bernatz PE, Huizenga KA. Arterio- 7. Junquera F, Quiroga S, Saperas E, et al. Accuracy of helical venous malformation of the intestine: an uncommon cause of computed tomographic angiography for the diagnosis of colonic gastrointestinal bleeding. Arch Surg 1972;104:284e7. angiodysplasia. 2000;119:293e9. 20. Lau WY, Wong SY, Ngan H, Fan ST, Wong KK. Intra-operative 8. Ponce Gonza´lez JF, Sa´nchez Gil JM, Leo´n Duen˜as E, Rodrı´guez localization of bleeding small intestinal lesions. Br J Surg 1988; Rodrı´guez A. Angiodysplasia of the terminal ileum. Rev Esp 75:249e51. Enferm Apar Dig 1989;75:179e84. 21. Gostout CJ, Bowyer BA, Ahlquist DA, Viggiano TR, Balm RK. 9. Jesudason SR, Devasia A, Mathen VI, Bhaktaviziam A, Khanduri P. Mucosal vascular malformations of the gastrointestinal tract: The pattern of angiodysplasia of the gastrointestinal tract in clinical observations and results of endoscopic neodymium: a tropical country. Surg Gynecol Obstet 1985;161:525e31. yttrium-aluminum-garnet laser therapy. Mayo Clin Proc 1988; 10. Chua AE, Ridley LJ. Diagnostic accuracy of CT angiography in 63:993e1003. acute gastrointestinal bleeding. J Med Imaging Radiat Oncol 22. Monk JE, Smith BA, O’Leary JP. Arteriovenous malformations 2008;52:333e8. of the small intestine. South Med J 1989;82:18e22.