About this Journal Submit a Manuscript Table of Contents
Stroke Research and Treatment
Volume 2011 (2011), Article ID 219706, 12 pages
http://dx.doi.org/10.4061/2011/219706
Review Article

Diabetic Ketoacidosis-Associated Stroke in Children and Youth

1Critical Care Medicine and Paediatrics, University of Western Ontario, London, ON, Canada N6A 5W9
2Children's Health Research Institute, London, ON, Canada N6C 2V5
3Centre for Critical Illness Research, London, ON, Canada N6C 2V5
4Clinical Neurological Sciences, University of Western Ontario, London, ON, Canada N6A 3K7
5Physiology and Pharmacology, University of Western Ontario, London, ON, Canada N6A 3K7
6Translational Research Centre, London, ON, Canada N6C 2V5

Received 8 October 2010; Revised 12 November 2010; Accepted 4 December 2010

Academic Editor: Halvor Naess

Copyright © 2011 Jennifer Ruth Foster et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Wolfsdorf, N. Glaser, and M. A. Sperling, “Diabetic ketoacidosis in infants, children, and adolescents: a consensus statement from the American Diabetes Association,” Diabetes Care, vol. 29, no. 5, pp. 1150–1159, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. J. Scibilia, D. Finegold, J. Dorman, D. Becker, and A. Drash, “Why do children with diabetes die?” Acta Endocrinologica. Supplementum, vol. 279, pp. 326–333, 1986.
  3. J. A. Edge, M. E. Ford-Adams, and D. B. Dunger, “Causes of death in children with insulin dependent diabetes 1990-96,” Archives of Disease in Childhood, vol. 81, no. 4, pp. 318–323, 1999. View at Scopus
  4. A. L. Rosenbloom, “Intracerebral crises during treatment of diabetic ketoacidosis,” Diabetes Care, vol. 13, no. 1, pp. 22–33, 1990. View at Scopus
  5. T. F. Roe, T. O. Crawford, K. R. Huff, G. Costin, F. R. Kaufman, and M. D. Nelson, “Brain infarction in children with diabetic ketoacidosis,” Journal of Diabetes and its Complications, vol. 10, no. 2, pp. 100–108, 1996. View at Publisher · View at Google Scholar · View at Scopus
  6. J. Ho, D. Pacaud, M. D. Hill, C. Ross, L. Hamiwka, and J. K. Mah, “Diabetic ketoacidosis and pediatric stroke,” Canadian Medical Association Journal, vol. 172, no. 3, pp. 327–328, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. J. A. Edge, M. M. Hawkins, D. L. Winter, and D. B. Dunger, “The risk and outcome of cerebral oedema developing during diabetic ketoacidosis,” Archives of Disease in Childhood, vol. 85, no. 1, pp. 16–22, 2001. View at Scopus
  8. S. E. Lawrence, E. A. Cummings, I. Gaboury, and D. Daneman, “Population-based study of incidence and risk factors for cerebral edema in pediatric diabetic ketoacidosis,” Journal of Pediatrics, vol. 146, no. 5, pp. 688–692, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. A. L. Rosenbloom, “Hyperglycemic crises and their complications in children,” Journal of Pediatric Endocrinology and Metabolism, vol. 20, no. 1, pp. 5–18, 2007. View at Scopus
  10. S. Likitmaskul, J. Santiprabhob, P. Sawathiparnich, N. Numbenjapon, and K. Chaichanwatanakul, “Clinical pictures of type 2 diabetes in Thai children and adolescents is highly related to features of metabolic syndrome,” Journal of the Medical Association of Thailand, vol. 88, supplement 8, pp. S169–S175, 2005. View at Scopus
  11. R. L. Sacco, “Risk factors and outcomes for ischemic stroke,” Neurology, vol. 45, no. 2, pp. S10–14, 1995. View at Scopus
  12. . The Emerging Risk Factors Collaboration, “Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies,” The Lancet, vol. 375, no. 9733, pp. 2215–2222, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. W. R. Timperley, F. E. Preston, and J. D. Ward, “Cerebral intravascular coagulation in diabetic ketoacidosis,” The Lancet, vol. 1, no. 7864, pp. 952–956, 1974. View at Scopus
  14. R. K. Kanter, M. Oliphant, J. J. Zimmerman, and M. J. Stuart, “Arterial thrombosis causing cerebral edema in association with diabetic ketoacidosis,” Critical Care Medicine, vol. 15, no. 2, pp. 175–176, 1987. View at Scopus
  15. B. Rogers, I. Sills, M. Cohen, and F. G. Seidel, “Diabetic Ketoacidosis: neurologic collapse during treatment followed by severe developmental morbidity,” Clinical Pediatrics, vol. 29, no. 8, pp. 451–456, 1990. View at Scopus
  16. J. Ho, J. K. Mah, M. D. Hill, and D. Pacaud, “Pediatric stroke associated with new onset type 1 diabetes mellitus: case reports and review of the literature,” Pediatric Diabetes, vol. 7, no. 2, pp. 116–121, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Keane, A. Gallagher, S. Ackroyd, M. A. McShane, and J. A. Edge, “Cerebral venous thrombosis during diabetic ketoacidosis,” Archives of Disease in Childhood, vol. 86, no. 3, pp. 204–206, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. A. L. Rosenbloom, “Fatal cerebral infarctions in diabetic ketoacidosis in a child with previously unknown heterozygosity for factor V Leiden deficiency,” Journal of Pediatrics, vol. 145, no. 4, pp. 561–562, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. K. De Keyzer, K. Paemeleire, M. De Clerck, D. Peeters, and J. L. De Reuck, “Diabetic ketoacidosis presenting as a cerebral venous sinus thrombosis,” Acta Neurologica Belgica, vol. 104, no. 3, pp. 117–120, 2004. View at Scopus
  20. M. J. Sasiadek, D. Sosnowska-Pacuszko, M. Zielinska, and T. Turek, “Cerebral venous thrombosis as a first presentation of diabetes,” Pediatric Neurology, vol. 35, no. 2, pp. 135–138, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Zerah, R. Patterson, I. Hansen, M. Briones, J. Dion, and B. Renfroe, “Resolution of severe sinus vein thrombosis with super selective thrombolysis in a pre-adolescent with diabetic ketoacidosis and a prothrombin gene mutation,” Journal of Pediatric Endocrinology and Metabolism, vol. 20, no. 6, pp. 725–731, 2007. View at Scopus
  22. V. L. Atluru, “Spontaneous intracerebral hematomas in juvenile diabetic ketoacidosis,” Pediatric Neurology, vol. 2, no. 3, pp. 167–169, 1986. View at Scopus
  23. S. L. Atkin, A. M. Coady, D. Horton, N. Sutaria, L. Sellars, and C. Walton, “Multiple cerebral haematomata and peripheral nerve palsies associated with a case of juvenile diabetic ketoacidosis,” Diabetic Medicine, vol. 12, no. 3, pp. 267–270, 1995. View at Scopus
  24. F. H. Mahmud, D. A. Ramsay, S. D. Levin, R. N. Singh, T. Kotylak, and D. D. Fraser, “Coma with diffuse white matter hemorrhages in juvenile diabetic ketoacidosis,” Pediatrics, vol. 120, no. 6, pp. e1540–e1546, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. J. J. Lin, K. L. Lin, H. S. Wang, A. M. C. Wong, and S. H. Hsia, “Occult infarct with acute hemorrhagic stroke in juvenile diabetic ketoacidosis,” Brain and Development, vol. 30, no. 1, pp. 91–93, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. W. H. Hoffman, C. L. Burek, J. L. Waller, L. E. Fisher, M. Khichi, and L. B. Mellick, “Cytokine response to diabetic ketoacidosis and its treatment,” Clinical Immunology, vol. 108, no. 3, pp. 175–181, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. C. G. Schalkwijk, D. C. W. Poland, W. Van Dijk et al., “Plasma concentration of C-reactive protein is increased in Type I diabetic patients without clinical macroangiopathy and correlates with markers of endothelial dysfunction: evidence for chronic inflammation,” Diabetologia, vol. 42, no. 3, pp. 351–357, 1999. View at Publisher · View at Google Scholar · View at Scopus
  28. R. R. Dalton, W. H. Hoffman, G. G. Passmore, and S. L. A. Martin, “Plasma C-reactive protein levels in severe diabetic ketoacidosis,” Annals of Clinical and Laboratory Science, vol. 33, no. 4, pp. 435–442, 2003. View at Scopus
  29. W. H. Hoffman, C. D. Cudrici, E. Zafranskaia, and H. Rus, “Complement activation in diabetic ketoacidosis brains,” Experimental and Molecular Pathology, vol. 80, no. 3, pp. 283–288, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Ceriello, D. Giugliano, A. Quatraro, E. Marchi, M. Barbanti, and P. Lefebvre, “Possible role for increased C4b-binding-protein level in acquired protein S deficiency in type I diabetes,” Diabetes, vol. 39, no. 4, pp. 447–449, 1990. View at Scopus
  31. S. K. Jain, R. McVie, and J. A. Bocchini Jr., “Hyperketonemia (ketosis), oxidative stress and type 1 diabetes,” Pathophysiology, vol. 13, no. 3, pp. 163–170, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. W. H. Hoffman, J. P. Locksmith, E. M. Burton et al., “Interstitial pulmonary edema in children and adolescents with diabetic ketoacidosis,” Journal of Diabetes and its Complications, vol. 12, no. 6, pp. 314–320, 1998. View at Publisher · View at Google Scholar · View at Scopus
  33. R. Bonfanti, E. Bognetti, F. Meschi, S. Medaglini, A. D'Angelo, and G. Chiumello, “Disseminated intravascular coagulation and severe peripheral neuropathy complicating ketoacidosis in a newly diagnosed diabetic child,” Acta Diabetologica, vol. 31, no. 3, pp. 173–174, 1994. View at Publisher · View at Google Scholar · View at Scopus
  34. F. Shanahan, G. Mortimer, and M. I. Drury, “Cerebral intravascular coagulation complicating diabetic ketoacidosis,” Irish Journal of Medical Science, vol. 150, no. 5, pp. 156–157, 1981. View at Scopus
  35. N. Ş. Ileri, Y. Büyükaşik, S. Karaahmetoǧlu et al., “Evaluation of the haemostatic system during ketoacidotic deterioration of diabetes mellitus,” Haemostasis, vol. 29, no. 6, pp. 318–325, 2000. View at Scopus
  36. M. Romano, M. Pomilio, S. Vigneri et al., “Endothelial perturbation in children and adolescents with type 1 diabetes: association with markers of the inflammatory reaction,” Diabetes Care, vol. 24, no. 9, pp. 1674–1678, 2001. View at Scopus
  37. N. Doǧruel, B. Kirel, Y. Akgün, and T. Us, “Serum soluble endothelial-cell specific adhesion molecules in children with insulin-dependent diabetes mellitus,” Journal of Pediatric Endocrinology and Metabolism, vol. 14, no. 3, pp. 287–293, 2001. View at Scopus
  38. M. E. Carr, “Diabetes mellitus: a hypercoagulable state,” Journal of Diabetes and its Complications, vol. 15, no. 1, pp. 44–54, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. T. Sakamoto, H. Ogawa, H. Kawano et al., “Rapid change of platelet aggregability in acute hyperglycemia. Detection by a novel laser-light scattering method,” Thrombosis and Haemostasis, vol. 83, no. 3, pp. 475–479, 2000. View at Scopus
  40. A. Iorio, M. O. Federici, E. Mourvaki et al., “Impaired endothelial antithrombotic activity following short-term interruption of continous subcutaneous insulin infusion in type I diabetic patients,” Thrombosis and Haemostasis, vol. 98, no. 3, pp. 635–641, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. G. F. Carl, W. H. Hoffman, G. G. Passmore et al., “Diabetic ketoacidosis promotes a prothrombotic state,” Endocrine Research, vol. 29, no. 1, pp. 73–82, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. J. M. Worly, J. D. Fortenberry, I. Hansen, C. R. Chambliss, and J. Stockwell, “Deep venous thrombosis in children with diabetic ketoacidosis and femoral central venous catheters,” Pediatrics, vol. 113, no. 1, pp. e57–e60, 2004. View at Scopus
  43. J. A. Gutierrez, R. Bagatell, M. P. Samson, A. A. Theodorou, and R. A. Berg, “Femoral central venous catheter-associated deep venous thrombosis in children with diabetic ketoacidosis,” Critical Care Medicine, vol. 31, no. 1, pp. 80–83, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Beck, J. Dubois, A. Grignon, J. Lacroix, and M. David, “Incidence and risk factors of catheter-related deep vein thrombosis in a pediatric intensive care unit: a prospective study,” Journal of Pediatrics, vol. 133, no. 2, pp. 237–241, 1998. View at Scopus
  45. T. C. Vukovich and G. Schernthaner, “Decreased protein C levels in patients with insulin-dependent type I diabetes mellitus,” Diabetes, vol. 35, no. 5, pp. 617–619, 1986. View at Scopus
  46. G. N. Welch and J. Loscalzo, “Homocysteine and atherothrombosis,” New England Journal of Medicine, vol. 338, no. 15, pp. 1042–1050, 1998. View at Publisher · View at Google Scholar · View at Scopus
  47. G. M. Rodgers and M. T. Conn, “Homocysteine, an atherogenic stimulus, reduces protein C activation by arterial and venous endothelial cells,” Blood, vol. 75, no. 4, pp. 895–901, 1990. View at Scopus
  48. M. Greaves, C. Pickering, and G. Knight, “Changes in the factor VIII complex in diabetic ketoacidosis: evidence of endothelial cell damage?” Diabetologia, vol. 30, no. 3, pp. 160–165, 1987. View at Scopus
  49. R. C. Paton, “Haemostatic changes in diabetic coma,” Diabetologia, vol. 21, no. 3, pp. 172–177, 1981. View at Scopus
  50. M. Mirshahi, J. Soria, C. Soria, O. Bertrand, M. Mirshahi, and A. Basdevant, “Glycosylation of human fibrinogen and fibrin in vitro. Its consequences on the properties of fibrin(ogen),” Thrombosis Research, vol. 48, no. 3, pp. 279–289, 1987. View at Scopus
  51. M. E. Carr and B. M. Alving, “Effect of fibrin structure on plasmin-mediated dissolution of plasma clots,” Blood Coagulation and Fibrinolysis, vol. 6, no. 6, pp. 567–573, 1995. View at Scopus
  52. M. R. Adams, C. J. Forsyth, W. Jessup, J. Robinson, and D. S. Celermajer, “Oral L-arginine inhibits platelet aggregation but does not enhance endothelium-dependent dilation in healthy young men,” Journal of the American College of Cardiology, vol. 26, no. 4, pp. 1054–1061, 1995. View at Publisher · View at Google Scholar · View at Scopus
  53. D. Giugliano, R. Marfella, L. Coppola et al., “Vascular effects of acute hyperglycemia in humans are reversed by L- arginine: evidence for reduced availability of nitric oxide during hyperglycemia,” Circulation, vol. 95, no. 7, pp. 1783–1790, 1997. View at Scopus
  54. D. L. Sackett, “Possible risk factors in the development of venous thrombosis. Gastrointestinal disease, infection and dehydration,” The Milbank Memorial Fund quarterly, vol. 50, supplement 2, pp. 105–122, 1972. View at Scopus
  55. L. A. Evan-Wong, R. J. L. Davidson, and J. M. Stowers, “Alterations in erythrocytes in hyperosmolar diabetic decompensation: a pathophysiological basis for impaired blood flow and for an improved design of fluid therapy,” Diabetologia, vol. 28, no. 10, pp. 739–742, 1985. View at Scopus
  56. E. M. Sevick and R. K. Jain, “Effect of red blood cell rigidity on tumor blood flow: increase in viscous resistance during hyperglycemia,” Cancer Research, vol. 51, no. 10, pp. 2727–2730, 1991. View at Scopus
  57. C. M. Isales, L. Min, and W. H. Hoffman, “Acetoacetate and β-hydroxybutyrate differentially regulate endothelin-1 and vascular endothelial growth factor in mouse brain microvascular endothelial cells,” Journal of Diabetes and its Complications, vol. 13, no. 2, pp. 91–97, 1999. View at Publisher · View at Google Scholar · View at Scopus
  58. W. H. Hoffman, R. M. Pluta, A. Q. Fisher, M. B. Wagner, and J. A. Yanovski, “Transcranial Doppler ultrasound assessment of intracranial hemodynamics in children with diabetic ketoacidosis,” Journal of Clinical Ultrasound, vol. 23, no. 9, pp. 517–523, 1995. View at Publisher · View at Google Scholar · View at Scopus
  59. J. S. Roberts, M. S. Vavilala, K. A. Schenkman, D. Shaw, L. D. Martin, and A. M. Lam, “Cerebral hyperemia and impaired cerebral autoregulation associated with diabetic ketoacidosis in critically ill children,” Critical Care Medicine, vol. 34, no. 8, pp. 2217–2223, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. E. Beghi, G. Bogliun, G. Cavaletti et al., “Hemorrhagic infarction: risk factors, clinical and tomographic features, and outcome. A case-control study,” Acta Neurologica Scandinavica, vol. 80, no. 3, pp. 226–231, 1989. View at Scopus
  61. J. K. Lynch, “Cerebrovascular disorders in children,” Current Neurology and Neuroscience Reports, vol. 4, no. 2, pp. 129–138, 2004. View at Scopus
  62. A. B. Muir, R. G. Quisling, M. C. K. Yang, and A. L. Rosenbloom, “Cerebral edema in childhood diabetic ketoacidosis: natural history, radiographic findings, and early identification,” Diabetes Care, vol. 27, no. 7, pp. 1541–1546, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. N. Hoggard, I. D. Wilkinson, and P. D. Griffiths, “The imaging of ischaemic stroke,” Clinical Radiology, vol. 56, no. 3, pp. 171–183, 2001. View at Publisher · View at Google Scholar · View at Scopus
  64. W. Hirsch, R. Beck, C. Behrmann, A. Schobess, and R. P. Spielmann, “Reliability of cranial CT versus intracerebral pressure measurement for the evaluation of generalised cerebral oedema in children,” Pediatric Radiology, vol. 30, no. 7, pp. 439–443, 2000. View at Scopus
  65. B. Husson, G. Rodesch, P. Lasjaunias, M. Tardieu, and G. Sébire, “Magnetic resonance angiography in childhood arterial brain infarcts: a comparative study with contrast angiography,” Stroke, vol. 33, no. 5, pp. 1280–1285, 2002. View at Publisher · View at Google Scholar · View at Scopus
  66. D. S. Atkinson, “Computed Tomography of Pediatric Stroke,” Seminars in Ultrasound, CT and MRI, vol. 27, no. 3, pp. 207–218, 2006. View at Publisher · View at Google Scholar · View at Scopus
  67. B. Franklin, J. Liu, and F. Ginsberg-Fellner, “Cerebral edema and ophthalmoplegia reversed by mannitol in a new case of insulin-dependent diabetes mellitus,” Pediatrics, vol. 69, no. 1, pp. 87–90, 1982. View at Scopus
  68. M. Lopez-Vicente, S. Ortega-Gutierrez, C. Amlie-Lefond, and M. T. Torbey, “Diagnosis and Management of Pediatric Arterial Ischemic Stroke,” Journal of Stroke and Cerebrovascular Diseases, vol. 19, no. 3, pp. 175–183, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. D. Eleftheriou and V. Ganesan, “Controversies in childhood arterial ischemic stroke and cerebral venous sinus thrombosis,” Expert Review of Cardiovascular Therapy, vol. 7, no. 7, pp. 853–861, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. R. Belvís, “Thrombolysis for acute stroke in pediatrics,” Stroke, vol. 38, no. 6, pp. 1722–1723, 2007. View at Publisher · View at Google Scholar · View at Scopus
  71. M. I. Shuayto, J. I. Lopez, and F. Greiner, “Administration of intravenous tissue plasminogen activator in a pediatric patient with acute ischemic stroke,” Journal of Child Neurology, vol. 21, no. 7, pp. 604–606, 2006. View at Publisher · View at Google Scholar · View at Scopus
  72. S. L. Benedict, O. K. Ni, P. Schloesser, K. S. White, and J. F. Bale, “Intra-arterial thrombolysis in a 2-year-old with cardioembolic stroke,” Journal of Child Neurology, vol. 22, no. 2, pp. 225–227, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. C. Cognard, A. Weill, S. Lindgren, M. Piotin, L. Castaings, and J. Moret, “Basilar artery occlusion in a child: “Clot angioplasty” followed by thrombolysis,” Child's Nervous System, vol. 16, no. 8, pp. 496–500, 2000. View at Publisher · View at Google Scholar · View at Scopus
  74. A. Kirton, J. H. Wong, J. Mah et al., “Successful endovascular therapy for acute basilar thrombosis in an adolescent,” Pediatrics, vol. 112, no. 3, part 1, pp. e248–e251, 2003. View at Scopus
  75. P. Monagle, E. Chalmers, A. Chan et al., “Antithrombotic therapy in neonates and children: American College of Chest Physicians evidence-based clinical practice guidelines (8th edition),” Chest, vol. 133, no. 6, supplement, pp. 887S–968S, 2008. View at Publisher · View at Google Scholar · View at Scopus
  76. E. S. Roach, M. R. Golomb, R. Adams et al., “Management of stroke in infants and children: a scientific statement from a special writing group of the american heart association stroke council and the council on cardiovascular disease in the young,” Stroke, vol. 39, no. 9, pp. 2644–2691, 2008. View at Publisher · View at Google Scholar · View at Scopus
  77. Paediatric Stroke Working Group, Stroke in Childhood: Clinical Guidelines for Diagnosis, Management and Rehabilitation, Royal College of Physicians, London ,UK, 2004.
  78. J. Burzynski, J. Ho, D. Pacaud, and J. Mah, “DKA and thrombosis,” Canadian Medical Association Journal, vol. 173, no. 2, pp. 132–133, 2005. View at Publisher · View at Google Scholar · View at Scopus
  79. D. B. Dunger, M. A. Sperling, C. L. Acerini et al., “European Society for Paediatric Endocrinology/Lawson Wilkins Pediatric Endocrine Society consensus statement on diabetic ketoacidosis in children and adolescents,” Pediatrics, vol. 113, no. 2, pp. e133–e140, 2004. View at Scopus
  80. M. L. Lawson, D. Pacaud, S. E. Lawrence, D. Daneman, and H. J. Dean, “2003 Canadian clinical practice guidelines for the management of diabetes in children and adolescents,” Paediatrics and Child Health, vol. 10, supplement A, pp. 5A–16A, 2005. View at Scopus