Pediatric Gastroenterology, Hepatology & Nutrition

  • 제25권3호
  • /
  • Pages.180-193
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  • 2022
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  • 2234-8646(pISSN)
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  • 2234-8840(eISSN)
대한소아소화기영양학회 (The Korean Society of Pediatric Gastroenterology, Hepatology and Nutrition)
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Cerebrovascular Events in Pediatric Inflammatory Bowel Disease: A Review of Published Cases

  • Rohani, Pejman (Pediatric Gastroenterology and Hepatology Research Center, Children's Medical Center, Pediatrics Center of Excellence, Tehran University of Medical Sciences) ;
  • Taraghikhah, Nazanin (Research Institute for Gastroenterology and Liver Disease, Shahid Beheshti University of Medical Sciences) ;
  • Nasehi, Mohammad Mehdi (Pediatric Neurology Research Center, Shahid Beheshti University of Medical Sciences, Research Institute for Children Health) ;
  • Alimadadi, Hosein (Pediatric Gastroenterology and Hepatology Research Center, Children's Medical Center, Pediatrics Center of Excellence, Tehran University of Medical Sciences) ;
  • Aghdaei, Hamid Assadzadeh (Research Institute for Gastroenterology and Liver Disease, Shahid Beheshti University of Medical Sciences)
  • 투고 : 2021.09.11
  • 심사 : 2022.03.07
  • 발행 : 2022.05.15
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초록

Pediatric inflammatory bowel disease (PIBD) is a multisystem disorder characterized by intestinal and extraintestinal manifestations and complications. Cerebrovascular events (CVE) are rare extraintestinal complications in patients with PIBD. Statistics show that 3.3% patients with PIBD and 1.3-6.4% adult patients with inflammatory bowel disease (IBD) experience CVE during the course of the disease. Therefore, this study aimed to review the records of children with IBD who developed CVE during the course of the disease. We retrospectively reviewed 62 cases of PIBD complicated by CVE. The mean patient age at the time of thrombotic events was 12.48±4.13 years. The incidence of ulcerative colitis was significantly higher than that of Crohn's disease (43 [70.5%] vs. 13 [21.3%] patients). Most patients (87.93%) were in the active phase of IBD at the time of CVE. The mean time interval between the onset of IBD and CVE was 20.84 weeks. Overall, 11 (26.83%) patients showed neurological symptoms of CVE at disease onset. The most frequent symptom on admission was persistent and severe headaches (67.85%). The most common site of cerebral venous thrombosis was the transverse sinuses (n=23, 53.48%). The right middle cerebral artery (n=3, 33.34%) was the predominant site of cerebral arterial infarction. Overall, 41 (69.49%) patients who were mostly administered unfractionated heparin or low-molecular-weight heparin (56.09%) recovered completely. Patients with IBD are at a risk of thromboembolism. CVE may be the most common type of thromboembolism. Based on these findings, the most common risk factor for CVE is IBD flares. In patients with CVE, anticoagulant therapy with heparin, followed by warfarin, is necessary.

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참고문헌

  1. Katsanos AH, Katsanos KH, Kosmidou M, Giannopoulos S, Kyritsis AP, Tsianos EV. Cerebral sinus venous thrombosis in inflammatory bowel diseases. QJM 2013;106:401-13. https://doi.org/10.1093/qjmed/hcs229
  2. Standridge S, de los Reyes E. Inflammatory bowel disease and cerebrovascular arterial and venous thromboembolic events in 4 pediatric patients: a case series and review of the literature. J Child Neurol 2008;23:59-66. https://doi.org/10.1177/0883073807308706
  3. Awab A, Elahmadi B, Elmoussaoui R, Elhijri A, Alilou M, Azzouzi A. Cerebral venous thrombosis and inflammatory bowel disease: reflections on pathogenesis. Colorectal Dis 2012;14:1153-4.
  4. Barclay AR, Keightley JM, Horrocks I, Garrick V, McGrogan P, Russell RK. Cerebral thromboembolic events in pediatric patients with inflammatory bowel disease. Inflamm Bowel Dis 2010;16:677-83. https://doi.org/10.1002/ibd.21113
  5. Al-Malik H, Green MR. Cerebral venous thrombosis as a complication of Crohn disease: a case report. J Pediatr Gastroenterol Nutr 2001;32:209-11. Erratum in: J Pediatr Gastroenterol Nutr 2001;33:428. https://doi.org/10.1097/00005176-200102000-00023
  6. Al Tahan A, Mageed SA, Al Momen A, Zaidan R, Daif A, Al Tahan F. Cerebral venous thrombosis as a complication of ulcerative colitis associated with protein-S deficiency: case report and review of literature. Saudi J Gastroenterol 1998;4:34-7.
  7. Mahmoud Reza A, Firozeh H, Houman A, Mehri NS. Pseudotumor cerebri in a case of ulcerative colitis with sagittal sinus thrombosis. Iran J Pediatr 2013;23:109-12.
  8. Rabeh RB, Othman AB, Bouyahya O, Mrad SM, Boukthir S. P331 Extraintestinal manifestations of pediatric inflammatory bowel disease: a tunisian single-center experience. Arch Dis Child 2019;104 Suppl 3:A290.
  9. Ben Sassi S, Mizouni H, Nabli F, Kallel L, Kefi M, Hentati F. Cerebral venous thrombosis presenting with cerebellar ataxia and cortical blindness. J Stroke Cerebrovasc Dis 2010;19:507-9. https://doi.org/10.1016/j.jstrokecerebrovasdis.2009.09.004
  10. Bridger S, Evans N, Parker A, Cairns SR. Multiple cerebral venous thromboses in a child with inflammatory bowel disease. J Pediatr Gastroenterol Nutr 1997;25:533-6. https://doi.org/10.1097/00005176-199711000-00009
  11. Cognat E, Crassard I, Denier C, Vahedi K, Bousser MG. Cerebral venous thrombosis in inflammatory bowel diseases: eight cases and literature review. Int J Stroke 2011;6:487-92. https://doi.org/10.1111/j.1747-4949.2011.00620.x
  12. Conners LM, Ahad R, Janda PH, Mudasir Z. Cerebral venous sinus thrombosis in a patient with ulcerative colitis flare. Case Rep Neurol Med 2018;2018:5798983. https://doi.org/10.1155/2018/5798983
  13. Calderon A, Wong JW, Becker LE. Multiple cerebral venous thromboses in a child with ulcerative colitis. Clin Pediatr (Phila) 1993;32:169-71. https://doi.org/10.1177/000992289303200310
  14. DeFilippis EM, Barfield E, Leifer D, Steinlauf A, Bosworth BP, Scherl EJ, et al. Cerebral venous thrombosis in inflammatory bowel disease. J Dig Dis 2015;16:104-8. https://doi.org/10.1111/1751-2980.12212
  15. Diakou M, Kostadima V, Giannopoulos S, Zikou AK, Argyropoulou MI, Kyritsis AP. Cerebral venous thrombosis in an adolescent with ulcerative colitis. Brain Dev 2011;33:49-51. https://doi.org/10.1016/j.braindev.2010.04.006
  16. Houissa F, Salem M, Bouzaidi S, Rejeb MB, Mekki H, Debbeche R, et al. Cerebral thrombosis in inflammatory bowel disease: a report of four cases. J Crohn's Colitis 2011;5:249-52. https://doi.org/10.1016/j.crohns.2010.12.010
  17. Jibaly R, Kaddourah A. P-0010: venous sinus thrombosis in a child with ulcerative colitis. Inflamm Bowel Dis 2009;15 Suppl 2:S7. https://doi.org/10.1097/00054725-200912002-00018
  18. Kao A, Dlugos D, Hunter JV, Mamula P, Thorarensen O. Anticoagulation therapy in cerebral sinovenous thrombosis and ulcerative colitis in children. J Child Neurol 2002;17:479-82. https://doi.org/10.1177/088307380201700702
  19. Kalbag RM, Woolf AL. Radiology, prognosis, pathology and treatment. In: Kalbag RM, Woolf AL, eds. Cerebral venous thrombosis: with special reference to primary aseptic thrombosis. London: Oxford University Press, 1967:237-50.
  20. Keene DL, Matzinger MA, Jacob PJ, Humphreys P. Cerebral vascular events associated with ulcerative colitis in children. Pediatr Neurol 2001;24:238-43. https://doi.org/10.1016/S0887-8994(00)00264-2
  21. Kim I, Min KH, Yeo M, Kim JS, Lee SH, Lee SS, et al. Unusual case of cerebral venous thrombosis in patient with Crohn's disease. Case Rep Neurol 2015;7:115-20. https://doi.org/10.1159/000430805
  22. Kupfer SS, Rubin DT. Inflammatory bowel disease and cerebral venous sinus thrombosis. Gastroenterol Hepatol (N Y) 2006;2:914-7.
  23. Kutluk G, Hacifazlioglu NE, Horozoglu H, Ertem D, Yilmaz Y. Cerebral venous thrombosis associated with childhood ulcerative colitis. Turk Arch Pediatr 2013;48:160-5. https://doi.org/10.4274/tpa.484
  24. Liu Y, Ren D, Zhou Q, Gao L. Cerebral sinovenous thrombosis in a child with ulcerative colitis: A case report. Medicine (Baltimore) 2020;99:e18649. https://doi.org/10.1097/md.0000000000018649
  25. Macri A, La Spina P, Terranova ML, Longo M, Gallitto G, Scuderi G, et al. Ulcerative colitis complicated by dural sina venous thrombosis. Int J Colorectal Dis 2002;17:61-2. https://doi.org/10.1007/s003840100355
  26. Markowitz RL, Ment LR, Gryboski JD. Cerebral thromboembolic disease in pediatric and adult inflammatory bowel disease: case report and review of the literature. J Pediatr Gastroenterol Nutr 1989;8:413-20. https://doi.org/10.1097/00005176-198904000-00028
  27. Martin-Masot R, Ortiz Perez P, Serrano Nieto J, Martinez Leon M, Pascual Martinez A, Blasco-Alonso J, et al. Central venous sinus thrombosis in a boy with acute severe ulcerative colitis. Front Pediatr 2019;7:19. https://doi.org/10.3389/fped.2019.00019
  28. Marusic E, Ursic A, Despot R, Simunovic M, Doric ML, Zitko V. Cerebral venous thrombosis a rare complication of ulcerative colitis - case report. Eur J Paediatr Neurol 2017;21 Suppl 1:e27.
  29. Mayeux R, Fahn S. Strokes and ulcerative colitis. Neurology 1978;28:571-4. https://doi.org/10.1212/WNL.28.6.571
  30. Patterson M, Castiglioni L, Sampson L. Chronic ulcerative colitis beginning in children and teenagers. A review of 43 patients. Am J Dig Dis 1971;16:289-97. https://doi.org/10.1007/BF02235203
  31. Philips MF, Bagley LJ, Sinson GP, Raps EC, Galetta SL, Zager EL, et al. Endovascular thrombolysis for symptomatic cerebral venous thrombosis. J Neurosurg 1999;90:65-71. https://doi.org/10.3171/jns.1999.90.1.0065
  32. Prasad RS, Michaels LA, Roychowdhury S, Craig V, Sorrell A, Schonfeld S. Combined venous sinus angioplasty and low-dose thrombolytic therapy for treatment of hemorrhagic transverse sinus thrombosis in a pediatric patient. J Pediatr Hematol Oncol 2006;28:196-9. https://doi.org/10.1097/01.mph.0000210408.66803.f2
  33. Rivera-Suazo Y, Arguello Calderon I, Vazquez-Frias R. Cerebral venous sinus thrombosis in a pediatric patient with inflammatory bowel disease: a case report. Rev Gastroenterol Mex (Engl Ed) 2020;85:364-6.
  34. Robison NJ, Dawlabani N, Lastra CR, Dhall G. Cerebral sinus thrombosis in a child with active ulcerative colitis and factor V Leiden. Pediatr Blood Cancer 2009;52:867-9. https://doi.org/10.1002/pbc.21967
  35. Rohani P, Javadzadeh M, Khalili M, Zojaji R. Cerebral venous thrombosis in a child with inflammatory bowel disease. Iran J Child Neurol 2021;15:159-66.
  36. Rosen I, Berkovitz D, Soudack M, Ben Barak A, Brik R. Cerebral vein thrombosis in a child with Crohn's disease. Isr Med Assoc J 2007;9:620-1.
  37. Rousseau B, Belanger C, Lacoursiere Y, Bergeron MG, Saab M, Poncelet P. [Ulcerative colitis and cerebral venous thrombosis]. Union Med Can 1975;104:414-7. French.
  38. Selvitop O, Poretti A, Huisman TA, Wagner MW. Cerebral sinovenous thrombosis in a child with Crohn's disease, otitis media, and meningitis. Neuroradiol J 2015;28:274-7. https://doi.org/10.1177/1971400915589688
  39. Shahid R. Case series of two patients presenting with cerebral venous sinus thrombosis in association with ulcerative colitis. JSMC Clin Case Rep 2019;4:4.
  40. Thorsteinsson GS, Magnussson M, Hallberg LM, Wahlgren NG, Lindgren F, Malmborg P, et al. Cerebral venous thrombosis and heparin-induced thrombocytopenia in an 18-year old male with severe ulcerative colitis. World J Gastroenterol 2008;14:4576-9. https://doi.org/10.3748/wjg.14.4576
  41. Zitomersky NL, Levine AE, Atkinson BJ, Harney KM, Verhave M, Bousvaros A, et al. Risk factors, morbidity, and treatment of thrombosis in children and young adults with active inflammatory bowel disease. J Pediatr Gastroenterol Nutr 2013;57:343-7. https://doi.org/10.1097/mpg.0b013e31829ce5cd
  42. Fukuhara T, Tsuchida S, Kinugasa K, Ohmoto T. A case of pontine lacunar infarction with ulcerative colitis. Clin Neurol Neurosurg 1993;95:159-62. https://doi.org/10.1016/0303-8467(93)90013-7
  43. Gormally SM, Bourke W, Kierse B, Monaghan H, McMenamin J, Drumm B. Isolated cerebral thrombo-embolism and Crohn disease. Eur J Pediatr 1995;154:815-8. https://doi.org/10.1007/BF01959788
  44. Lloyd-Still JD, Tomasi L. Neurovascular and thromboembolic complications of inflammatory bowel disease in childhood. J Pediatr Gastroenterol Nutr 1989;9:461-6. https://doi.org/10.1097/00005176-198911000-00012
  45. Nelson J, Barron MM, Riggs JE, Gutmann L, Schochet SS Jr. Cerebral vasculitis and ulcerative colitis. Neurology 1986;36:719-21. https://doi.org/10.1212/WNL.36.5.719
  46. Salloum R, Alhalabi N, Almidani MA. A case of Syrian child with cerebral infarction as an extraintestinal manifestation of ulcerative colitis. Case Rep Gastrointest Med 2019;2019:5984094. https://doi.org/10.1155/2019/5984094
  47. Schneiderman JH, Sharpe JA, Sutton DM. Cerebral and retinal vascular complications of inflammatory bowel disease. Ann Neurol 1979;5:331-7. https://doi.org/10.1002/ana.410050405
  48. Tomomasa T, Itoh K, Matsui A, Kobayashi T, Suzuki N, Matsuyama S, et al. An infant with ulcerative colitis complicated by endocarditis and cerebral infarction. J Pediatr Gastroenterol Nutr 1993;17:323-5. https://doi.org/10.1097/00005176-199310000-00017
  49. Yassinger S, Adelman R, Cantor D, Halsted CH, Bolt RJ. Association of inflammatory bowel disease and large vascular lesions. Gastroenterology 1976;71:844-6. https://doi.org/10.1016/s0016-5085(76)80372-1
  50. Nguyen GC, Sam J. Rising prevalence of venous thromboembolism and its impact on mortality among hospitalized inflammatory bowel disease patients. Am J Gastroenterol 2008;103:2272-80. https://doi.org/10.1111/j.1572-0241.2008.02052.x
  51. Lazzerini M, Bramuzzo M, Maschio M, Martelossi S, Ventura A. Thromboembolism in pediatric inflammatory bowel disease: systematic review. Inflamm Bowel Dis 2011;17:2174-83. https://doi.org/10.1002/ibd.21563
  52. Bernstein CN, Blanchard JF, Houston DS, Wajda A. The incidence of deep venous thrombosis and pulmonary embolism among patients with inflammatory bowel disease: a population-based cohort study. Thromb Haemost 2001;85:430-4. https://doi.org/10.1055/s-0037-1615600
  53. Wakefield AJ, Sawyerr AM, Dhillon AP, Pittilo RM, Rowles PM, Lewis AA, et al. Pathogenesis of Crohn's disease: multifocal gastrointestinal infarction. Lancet 1989;334:1057-62. https://doi.org/10.1016/S0140-6736(89)91078-7
  54. Hommes DW, van Dullemen HM, Levi M, van der Ende A, Woody J, Tytgat GN, et al. Beneficial effect of treatment with a monoclonal anti-tumor necrosis factor-alpha antibody on markers of coagulation and fibrinolysis in patients with active Crohn's disease. Haemostasis 1997;27:269-77.
  55. Brynskov J, Nielsen OH, Ahnfelt-Ronne I, Bendtzen K. Cytokines (immunoinflammatory hormones) and their natural regulation in inflammatory bowel disease (Crohn's disease and ulcerative colitis): a review. Dig Dis 1994;12:290-304. https://doi.org/10.1159/000171464
  56. Miehsler W, Reinisch W, Valic E, Osterode W, Tillinger W, Feichtenschlager T, et al. Is inflammatory bowel disease an independent and disease specific risk factor for thromboembolism? Gut 2004;53:542-8. https://doi.org/10.1136/gut.2003.025411
  57. Solem CA, Loftus EV Jr, Tremaine WJ, Sandborn WJ. Venous thromboembolism in inflammatory bowel disease. Am J Gastroenterol 2004;99:97-101. https://doi.org/10.1046/j.1572-0241.2003.04026.x
  58. Angelberger S, Miehsler W, Novacek G. Colonic involvement does not predispose to thrombosis in IBD. Inflamm Bowel Dis 2009;15:316-7. https://doi.org/10.1002/ibd.20589
  59. Talbot RW, Heppell J, Dozois RR, Beart RW Jr. Vascular complications of inflammatory bowel disease. Mayo Clin Proc 1986;61:140-5. https://doi.org/10.1016/s0025-6196(12)65200-8
  60. Webberley MJ, Hart MT, Melikian V. Thromboembolism in inflammatory bowel disease: role of platelets. Gut 1993;34:247-51. https://doi.org/10.1136/gut.34.2.247
  61. Jackson LM, O'Gorman PJ, O'Connell J, Cronin CC, Cotter KP, Shanahan F. Thrombosis in inflammatory bowel disease: clinical setting, procoagulant profile and factor V Leiden. QJM 1997;90:183-8. https://doi.org/10.1093/qjmed/90.3.183
  62. Liebman HA, Kashani N, Sutherland D, McGehee W, Kam AL. The factor V Leiden mutation increases the risk of venous thrombosis in patients with inflammatory bowel disease. Gastroenterology 1998;115:830-4. https://doi.org/10.1016/S0016-5085(98)70253-7
  63. Bernstein CN, Sargent M, Vos HL, Rosendaal FR. Mutations in clotting factors and inflammatory bowel disease. Am J Gastroenterol 2007;102:338-43. https://doi.org/10.1111/j.1572-0241.2006.00974.x
  64. Spiroski I, Kedev S, Antov S, Arsov T, Krstevska M, Dzhekova-Stojkova S, et al. Association of methylenetetrahydrofolate reductase (MTHFR-677 and MTHFR-1298) genetic polymorphisms with occlusive artery disease and deep venous thrombosis in Macedonians. Croat Med J 2008;49:39-49. https://doi.org/10.3325/cmj.2008.1.39
  65. Marjot T, Yadav S, Hasan N, Bentley P, Sharma P. Genes associated with adult cerebral venous thrombosis. Stroke 2011;42:913-8. https://doi.org/10.1161/strokeaha.110.602672
  66. Gemmati D, Serino ML, Trivellato C, Fiorini S, Scapoli GL. C677T substitution in the methylenetetrahydrofolate reductase gene as a risk factor for venous thrombosis and arterial disease in selected patients. Haematologica 1999;84:824-8.
  67. Turner D, Ruemmele FM, Orlanski-Meyer E, Griffiths AM, de Carpi JM, Bronsky J, et al. Management of paediatric ulcerative colitis, part 2: acute severe colitis-an evidence-based consensus guideline from the European Crohn's and Colitis Organization and the European Society of Paediatric Gastroenterology, Hepatology and Nutrition. J Pediatr Gastroenterol Nutr 2018;67:292-310. https://doi.org/10.1097/MPG.0000000000002036
  68. Ferriero DM, Fullerton HJ, Bernard TJ, Billinghurst L, Daniels SR, DeBaun MR, et al. Management of stroke in neonates and children: a scientific statement from the American Heart Association/American Stroke Association. Stroke 2019;50:e51-96.