Functional and anatomical evidence of cerebral tissue hypoxia in young sickle cell anemia mice

Journal of Cerebral Blood Flow and Metabolism

Volumn 37, Issue 3, 2017, Pages 994-1005

  Cahill, Lindsay S ^a   Gazdzinski, Lisa M ^a   Tsui, Albert Ky ^b   Zhou, Yu Qing ^a   Portnoy, Sharon ^a   Liu, Elaine ^b   Mazer, C David ^b,c   Hare, Gregory Mt ^b,c   Kassner, Andrea ^a   Sled, John G ^a,c  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b ST MICHAEL'S HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

cerebral hypoxia; cerebrovascular reactivity; continuous arterial spin labelling MRI; Sickle cell anemia mice

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL REACTIVITY; BRAIN BLOOD FLOW; BRAIN HYPOXIA; BRAIN INJURY; BRAIN OXYGEN TENSION; BRAIN REGION; BRAIN SIZE; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; DISEASE ASSOCIATION; EX VIVO STUDY; FEMALE; GRAY MATTER; HYPERCAPNIA; HYPOXEMIA; MOUSE; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SICKLE CELL ANEMIA; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; WHITE MATTER; ANIMAL; BRAIN; BRAIN CIRCULATION; BRAIN ISCHEMIA; CAROTID ARTERY; COMPLICATION; HYPOXIA, BRAIN; METABOLISM; PATHOLOGY; PHYSIOLOGY; STROKE;

ANEMIA, SICKLE CELL; ANIMALS; BRAIN; BRAIN ISCHEMIA; CAROTID ARTERIES; CEREBROVASCULAR CIRCULATION; GRAY MATTER; HYPOXIA, BRAIN; MICE; MICE, TRANSGENIC; STROKE; WHITE MATTER;

EID: 85012190923     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1177/0271678X16649194     Document Type: Article

References (64)

1. Ohene-Frempong K, Weiner SJ, Sleeper LA, et al. Cerebrovascular accidents in sickle cell disease: rates and risk factors. Blood 1998; 91: 288-294.
2. DeBaun MR, Gordon M, McKinstry RC, et al. Controlled trial of transfusions for silent cerebral infarcts in sickle cell anemia. N Engl J Med 2014; 371: 699-710.
3. Gold JI, Johnson CB, Treadwell MJ, et al. Detection and assessment of stroke in patients with sickle cell disease: neuropsychological functioning and magnetic resonance imaging. Pediatr Hematol Oncol 2008; 25: 409-421.
4. Schatz J, Brown RT, Pascual JM, et al. Poor school and cognitive functioning with silent cerebral infarcts and sickle cell disease. Neurology 2001; 56: 1109-1111.
5. Adams RJ, McKie VC, Hsu L, et al. Prevention of a first stroke by transfusions in children with sickle cell anemia and abnormal results on transcranial Doppler ultrasonography. N Engl J Med 1998; 339: 5-11.
6. Adams RJ and Brambilla D. Optimizing primary stroke prevention in sickle cell anemia trial I. Discontinuing prophylactic transfusions used to prevent stroke in sickle cell disease. N Engl J Med 2005; 353: 2769-2778.
7. Kaul DK, Fabry ME and Nagel RL. The pathophysiology of vascular obstruction in the sickle syndromes. Blood Rev 1996; 10: 29-44.
8. Kaul DK, Liu XD, Chang HY, et al. Effect of fetal hemoglobin on microvascular regulation in sickle transgenic-knockout mice. J Clin Invest 2004; 114: 1136-1145.
9. Nur E, Kim YS, Truijen J, et al. Cerebrovascular reserve capacity is impaired in patients with sickle cell disease. Blood 2009; 114: 3473-3478.
10. Reichmuth KJ, Dopp JM, Barczi SR, et al. Impaired vascular regulation in patients with obstructive sleep apnea: effects of continuous positive airway pressure treatment. Am J Respir Crit Care Med 2009; 180: 1143-1150.
11. Kuwabara Y, Sasaki M, Hirakata H, et al. Cerebral blood flow and vasodilatory capacity in anemia secondary to chronic renal failure. Kidney Int 2002; 61: 564-569.
12. Hudetz AG, Wood JD and Kampine JP. 7-Nitroindazole impedes erythrocyte flow response to isovolemic hemodilution in the cerebral capillary circulation. J Cereb Blood Flow Metal 2000; 20: 220-224.
13. Tsui AK, Marsden PA, Mazer CD, et al. Priming of hypoxia-inducible factor by neuronal nitric oxide synthase is essential for adaptive responses to severe anemia. Proc Natl Acad Sci USA 2011; 108: 17544-17549.
14. Hu T, Beattie WS, Mazer CD, et al. Treatment with a highly selective beta(1) antagonist causes dose-dependent impairment of cerebral perfusion after hemodilution in rats. Anesth Analg 2013; 116: 649-662.
15. Ragoonanan TE, Beattie WS, Mazer CD, et al. Metoprolol reduces cerebral tissue oxygen tension after acute hemodilution in rats. Anesthesiology 2009; 111: 988-1000.
16. Ashes C, Judelman S, Wijeysundera DN, et al. Selective beta1-Antagonism with bisoprolol is associated with fewer postoperative strokes than atenolol or metoprolol: A single-center cohort study of 44, 092 consecutive patients. Anesthesiology 2013; 119: 777-787.
17. Crawford MW, Shichor T, Engelhardt T, et al. The novel hemoglobin-based oxygen carrier HRC 101 improves survival in murine sickle cell disease. Anesthesiology 2007; 107: 281-287.
18. Kim YS, Nur E, van Beers EJ, et al. Dynamic cerebral autoregulation in homozygous Sickle cell disease. Stroke 2009; 40: 808-814.
19. Herold S, Brozovic M, Gibbs J, et al. Measurement of regional cerebral blood flow, blood volume and oxygen metabolism in patients with sickle cell disease using positron emission tomography. Stroke 1986; 17: 692-698.
20. Oguz KK, Golay X, Pizzini FB, et al. Sickle cell disease: continuous arterial spin-labelling perfusion MR imaging in children. Radiology 2003; 227: 567-574.
21. Strouse JJ, Cox CS, Melhem ER, et al. Inverse correlation between cerebral blood flow measured by continuous arterial spin-labeling (CASL) MRI and neurocognitive function in children with sickle cell anemia (SCA). Blood 2006; 108: 379-381.
22. Helton KJ, Paydar A, Glass J, et al. Arterial spin-labeled perfusion combined with segmentation techniques to evaluate cerebral blood flow in white and gray matter of children with sickle cell anemia. Pediatr Blood Cancer 2009; 52: 85-91.
23. Gevers S, Nederveen AJ, Fijnvandraat K, et al. Arterial spin labeling measurement of cerebral perfusion in children with sickle cell disease. J Magn Reson Imaging 2012; 35: 779-787.
24. Kim JA, Leung J, Lerch JP, et al. Reduced cerebrovascular reserve is regionally associated with cortical thickness reductions in children with sickle cell disease. Brain Res 2016; 1642: 263-269.
25. Wu LC, Sun CW, Ryan TM, et al. Correction of sickle cell disease by homologous recombination in embryonic stem cells. Blood 2006; 108: 1183-1188.
26. Hanna J, Wernig M, Markoulaki S, et al. Treatment of sickle cell anemia mouse model with iPS cells generated from autologous skin. Science 2007; 318: 1920-1923.
27. Luo W, Su EJ, Wang J, et al. Increased stroke size following MCA occlusion in a mouse model of sickle cell disease. Blood 2014; 123: 1965-1967.
28. Chugh BP, Bishop J, Zhou YQ, et al. Robust method for 3D arterial spin labeling in mice. Magn Reson Med 2012; 68: 98-106.
29. Foster FS, Mehi J, Lukacs M, et al. A new 15-50MHz array-based micro-ultrasound scanner for preclinical imaging. Ultrasound Med Biol 2009; 35: 1700-1708.
30. Collins KA, Korcarz CE and Lang RM. Use of echocardiography for the phenotypic assessment of genetically altered mice. Physiol Genomics 2003; 13: 227-239.
31. Zhou YQ, Zhu SN, Foster FS, et al. Aortic regurgitation dramatically alters the distribution of atherosclerotic lesions and enhances atherogenesis in mice. Arterioscler Thromb Vasc Biol 2010; 30: 1181-1188.
32. Vinogradov SA, Lo LW and Wilson DF. Dendritic polyglutamic porphoryns: Probing porphyrin protection by oxygen-dependent quenching of phosphorescence. Chemistry 1999; 5: 1338-1347.
33. Yu J, Ramadeen A, Tsui AK, et al. Quantitative assessment of brain microvascular and tissue oxygenation during cardiac arrest and resuscitation in pigs. Anaesthesia 2013; 68: 723-735.
34. Spring S, Lerch JP and Henkelman RM. Sexual dimorphism revealed in the structure of the mouse brain using three-dimensional magnetic resonance imaging. Neuroimage 2007; 35: 1424-1433.
35. Cahill LS, Laliberte CL, Ellegood J, et al. Preparation of fixed mouse brains for MRI. Neuroimage 2012; 60: 933-939.
36. Dazai J, Spring S, Cahill LS, et al. Multiple-mouse neuroanatomical magnetic resonance imaging. J Vis Exp 2011; 48: e2497.
37. Thomas DL, De Vita E, Roberts S, et al. High-resolution fast spin echo imaging of the human brain at 4.7 T: implementation and sequence characteristics. Magn Reson Med 2004; 51: 1254-1264.
38. Avants BB, Epstein CL, Grossman M, et al. Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal 2008; 12: 26-41.
39. Lerch JP, Sled JG and Henkelman RM. MRI phenotyping of genetically altered mice. Methods Mol Bio 2011; 711: 349-361.
40. Chung MK, Worsley KJ, Paus T, et al. A unified statistical approach to deformation-based morphometry. Neuroimage 2001; 14: 595-606.
41. Dorr AE, Lerch JP, Spring S, et al. High resolution threedimensional brain atlas using an average magnetic resonance image of 40 adult C57Bl/6J mice. Neuroimage 2008; 42: 60-69.
42. Chakravarty MM, Steadman P, van Eede MC, et al. Performing label-fusion-based segmentation using multiple automatically generated templates. Hum Brain Mapp 2013; 34: 2635-2654.
43. Tsui AK, Marsden PA, Mazer CD, et al. Differential HIF and NOS responses to acute anemia: defining organ-specific hemoglobin thresholds for tissue hypoxia. Am J Physiol Regul Integr Comp Physiol 2014; 307: R13-R25.
44. Genovese CR, Lazar NA and Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 2002; 15: 870-878.
45. Ahmed S, Siddiqui AK, Sadiq A, et al. Echocardiographic abnormalities in sickle cell disease. Am J Hematol 2004; 76: 195-198.
46. McLaren AT, Marsden PA, Mazer CD, et al. Increased expression of HIF-1alpha, nNOS, and VEGF in the cerebral cortex of anemic rats. Am J Physiol Regul Integr Comp Physiol 2007; 292: R403-R414.
47. Han JS, Mikulis DJ, Mardimae A, et al. Measurement of cerebrovascular reactivity in pediatric patients with cerebral vasculopathy using blood oxygen level-dependent MRI. Stroke 2011; 42: 1261-1269.
48. Mikulis DJ, Krolczyk G, Desal H, et al. Preoperative and postoperative mapping of cerebrovascular reactivity in moyamoya disease by using blood oxygen level-dependent magnetic resonance imaging. J Neurosurg 2005; 103: 347-355.
49. Ke Q and Costa M. Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol 2006; 70: 1469-1480.
50. Hare GM, Mazer CD, Mak W, et al. Hemodilutional anemia is associated with increased cerebral neuronal nitric oxide synthase gene expression. J Appl Physiol 2003; 94: 2058-2067.
51. Li M, Bertout JA, Ratcliffe SJ, et al. Acute anemia elicits cognitive dysfunction and evidence of cerebral cellular hypoxia in older rats with systemic hypertension. Anesthesiology 2010; 113: 845-858.
52. Weiskopf RB, Kramer JH, Viele M, et al. Acute severe isovolemic anemia impairs cognitive function and memory in humans. Anesthesiology 2000; 92: 1646-1652.
53. Weiskopf RB, Feiner J, Hopf HW, et al. Oxygen reverses deficits of cognitive function and memory and increased heart rate induced by acute severe isovolemic anemia. Anesthesiology 2002; 96: 871-877.
54. Clarke SE, Jukes MC, Njagi JK, et al. Effect of intermittent preventive treatment of malaria on health and education in schoolchildren: A cluster-randomised, double-blind, placebo-controlled trial. Lancet 2008; 372: 127-138.
55. Muller AM, Morales C, Briner J, et al. Loss of CO2 reactivity of cerebral blood flow is associated with severe brain damage in mechanically ventilated very low birth weight infants. Eur J Pediatr Neurol 1997; 1: 157-163.
56. Fierstra J, Poublanc J, Han JS, et al. Steal physiology is spatially associated with cortical thinning. J Neurol Neurosurg Psychiatry 2010; 81: 290-293.
57. Silvestrini M, Vernieri F, Pasqualetti P, et al. Impaired cerebral vasoreactivity and risk of stroke in patients with asymptomatic carotid artery stenosis. JAMA 2000; 283: 2122-2127.
58. Fierstra J, Maclean DB, Fisher JA, et al. Surgical revascularization reverses cerebral cortical thinning in patients with severe cerebrovascular steno-occlusive disease. Stroke 2011; 42: 1631-1637.
59. Maruyama M, Shimoji K, Ichikawa T, et al. The effects of extreme hemodilutions on the autoregulation of cerebral blood flow, electroencephalogram and cerebral metabolic rate of oxygen in the dog. Stroke 1985; 16: 675-679.
60. Scantlebury N, Mabbott D, Janzen L, et al. White matter integrity and core cognitive function in children diagnosed with sickle cell disease. J Pediatr Hematol Oncol 2011; 33: 163-171.
61. Pickett JL, Theberge DC, Brown WS, et al. Normalizing hematocrit in dialysis patients improves brain function. Am J Kidney Dis 1999; 33: 1122-1130.
62. Behpour AM, Shah PS, Mikulis DJ, et al. Cerebral blood flow abnormalities in children with sickle cell disease: A systematic review. Pediatr Neurol 2013; 48: 188-199.
63. Aviles-Reyes RX, Angelo MF, Villarreal A, et al. Intermittent hypoxia during sleep induces reactive gliosis and limited neuronal death in rats: implications for sleep apnea. J Neurochem 2010; 112: 854-869.
64. de Montalembert M, Aggoun Y, Niakate A, et al. Endothelial-dependent vasodilation is impaired in children with sickle cell disease. Haematologica 2007; 92: 1709-1710.