Arterial hypertension and brain damage - Evidence from animal models

Clinical and Experimental Hypertension

Volumn 25, Issue 6, 2003, Pages 359-380

  Amenta, Francesco ^a   Di Tullio, Maria Antonietta ^a   Tomassoni, Daniele ^a  

^a UNIVERSITY OF CAMERINO   (Italy)

Author keywords

Animal models; Anti hypertensive treatment; Brain damage; Hypertension

Indexed keywords

CALCIUM ANTAGONIST; DIHYDROPYRIDINE DERIVATIVE;

ANIMAL MODEL; BRAIN ATROPHY; BRAIN INJURY; BRAIN PROTECTION; CEREBROVASCULAR DISEASE; COGNITIVE DEFECT; GLIA; HYPERTENSION; NERVE CELL NECROSIS; NONHUMAN; RAT; REVIEW; SPONTANEOUSLY HYPERTENSIVE RAT; STROKE;

ANIMALS; ANTIHYPERTENSIVE AGENTS; BRAIN DAMAGE, CHRONIC; DOGS; HYPERTENSION; MICE; MODELS, ANIMAL; RABBITS; RATS;

EID: 0043026941     PISSN: 10641963     EISSN: None     Source Type: Journal    
DOI: 10.1081/CEH-120023545     Document Type: Review

References (150)

1. Babikian VL, Hyde C, Pochay V, Winter MR. Clinical correlates of high-intensity transient signals detected on transcranial Doppler sonography in patients with cerebrovascular disease. Stroke 1994; 25:1570-1573.
2. Leys D, Deplanque D, Mounier-Vehier C, Mackowiak-Cordoliani MA, Lucas C, Bordet R. Stroke prevention: management of modifiable vascular risk factors. J Neurol 2002; 249:507-517.
3. Gorelick PB. Stroke prevention: windows of opportunity and failed expectations? A discussion of modifiable cardiovascular risk factors and a prevention proposal. Neuroepidemiology 1997; 16:163-173.
4. Gorelick PB, Sacco RL, Smith DB, Alberts M, Mustone-Alexander L, Rader D, Ross JL, Raps E, Ozer MN, Brass LM, Malone ME, Goldberg S, Booss J, Hanley DF, Toole JF, Greengold NL, Rhew DC. Prevention of a first stroke: a review of guidelines and a multidisciplinary consensus statement from the National Stroke Association. JAMA 1999; 281:1112-1120.
5. Goldstein LB, Adams R, Becker K, Furberg CD, Gorelick PB, Hademenos G, Hill M, Howard G, Howard VJ, Jacobs B, Levine SR, Mosca L, Sacco RL, Sherman DG, Wolf PA, del Zoppo GJ. Primary prevention of ischemic stroke: a statement for healthcare professionals from the Stroke Council of the American Heart Association. StrokeJan 2001; 32:280-299.
6. Franklin SS. Cardiovascular risks related to increased diastolic, systolic and pulse pressure. An epidemiologist's point of view. Pathol Biol (Paris) 1999; 47:594-603.
7. Staessen JA, O'Brien ET, Thijs L, Fagard RH. Modern approaches to blood pressure measurement. Occup Environ Med 2000; 57:510-520.
8. Millar JA, Lever AF. Implications of pulse pressure as a predictor of cardiac risk in patients with hypertension. Hypertension 2000; 36:907-911.
9. Safar ME. Pulse pressure, arterial stiffness, and cardiovascular risk. Curr Opin Cardiol 2000; 15:258-263.
10. Sacco RL. Newer risk factors for stroke. Neurology 2001; 57:S31-S34.
11. Gautier JC. Cerebral ischemia in hypertension. In: Ross-Russel RW, ed. Vascular Disease of the Central Nervous System. Churchill: Livingstone, Edinburgh, London, 1983:224-244.
12. Johansson BB. Cerebral vascular bed in hypertension and consequences for the brain. Hypertension 1984; 6:81-86.
13. Amenta F, Ferrante F, Sabbatini M, Ricci A. Quantitative image analysis study of the cerebral vasodilatory activity of nicardipine in spontaneously hypertensive rats. Clin Exper Hypertens 1994; 16:359-371.
14. Fujishima M, Omae T. Lower limit of cerebral autoregulation in normotensive and spontaneously hypertensive rats. Experientia 1976; 32:1019-1021.
15. Nobili F, Arvigo F, De Carli F, Franconieri N, Marenco S, Rodriguez G, Rosadini G. Changes of regional cerebral blood flow in chronic hypertensive patients. IRCS Med Sci 1986; 14:869-870.
16. Fujishima M, Ibayashi S, Fuji H, Ooboshi H, Mori S, Nakane H. Cerebral blood flow and hypertensive treatment in hypertension. Hypertens Res 1994; 17:12-16.
17. Schmidt R. Vascular dementia. Wien Med Wochenschr 2002; 152:85-91.
18. de Leeuw FE, de Groot JC, Oudkerk M, Witteman JC, Hofman A, van Gijn J, Breteler MM. Hypertension and cerebral white matter lesions in a prospective cohort study. Brain 2002; 125:765-772.
19. Kalra M, al-Khaffaf H, Farrell A, Wallbank WA, Charlesworth D. Comparison of measurement of stump pressure and transcranial measurement of flow velocity in the middle cerebral artery in carotid surgery. Ann Vasc Surg 1994; 8:225-231.
20. Salerno JA, Murphy DG, Horwitz B, De Carli C, Haxby JV, Rapoport SI, Schapiro MB. Brain atrophy in hypertension. A volumetric magnetic resonance imaging study. Hypertension 1992; 20:340-348.
21. Fujii T, Okuno T, Ito M, Motoh K, Hamazaki S, Okada S, Kusaka H, Mikawa H. CT, MRI, and autopsy findings in brain of a patient with MELAS. Pediatr Neurol 1990; 6:253-256.
22. Tatemichi TK, Paik M, Bagiella E, Desmond DW, Pirro M, Hanzawa LK. Dementia after stroke is a predictor of long-term survival. Stroke 1994; 25:1915-1919.
23. Goldblatt H, Lynch J, Hanzal RF, Summerville WW. The production of persistent elevation of systolic blood pressure by means of renal ischemia. J Exp Med 1934; 59:347-379.
24. Goldblatt PJ, Laragh J, Brenner B, eds. Hypertension, Phatophysiology, Diagnosis and Management. 2nd ed. Raven Press: NY, 1995:27-36.
25. Zhu HB, Geng MY, Guan HS, Zhang JT. Antihypertensive effects of D-polyman-nuronic sulphate and its related mechanisms in renovascular hypertensive rats. Acta Pharmacol Sin 2000; 21:727-732.
26. Bianciotti LG, de Bold AJ. Modulation of cardiac natriuretic peptide ge expression following endothelin type A receptor blockage in renovascular hypertension. Cardiovasc Res 2001; 49:808-816.
27. Ocaranza MP, Piddo AM, Faundez P, Lavandero S, Jalil JE. Angiotensin I-converting enzyme gene polimorphism influences chronic hypertensive responce in the rat Goldglatt model. J Hypertens 2002; 20:413-420.
28. Yamaguchi T, Nagano H, Yamaguchi M, Suzuki T, Saito Y, Tano Y. The effects of kallidinogenase on choroidal flow in a hypertensive rabbit model. Curr Eye Res 1999; 18:417-422.
29. Head GA, Burke SL. Renal and cardiac sympathetic baroreflexes in hypertensive rabbits. Clin Exper Pharm Physiol 2001; 28:972-975.
30. Gomez-Sanchez EP, Zhou M, Gomez-Sanchez CE. Mineralocorticoids, salt and high blood pressure. Steroids 1996; 61:184-188.
31. Hazama F, Haebara H, Amano S, Ozaki T. Proceedings: autoradiographic investigation of cell proliferation in the brain of spontaneously hypertensive rats. Jpn Heart J 1976; 17:370.
32. Johansson BB, Fredriksson K. Cerebral arteries in hypertension: structural and hemodynamic aspects. J Cardiovasc Pharmacol 1985; 7:S90-S93.
33. Smith TL, Hutchins PM. Central hemodynamics in the developmental stage of spontaneous hypertension in the unanesthetized rat. Hypertension 1979; 1:508-517.
34. Watanabe K, Nishio T, Mori C, Kihara M, Yamori Y. Changes in hemodynamics with advancing age in conscious spontaneously hypertensive rats. Jpn Circ J 1985; 49:446-450.
35. Okamoto K, Aoki K. Development of a strain of spontaneoulsy hypertensive rats. Jpn Circ J 1963; 27:282-293.
36. Okamoto K, Yamori Y, Nagoaka A. Establishment of the stroke-prone SHR. Circ Res 1974; 34/35:143-153.
37. Yamori Y. Development of the spontaneously hypertensive rat (SHR), the stroke-prone SHR (SHRSP) and their various substrain models for hypertension-related cardiovascular disease. In: Ganten D, de Jong W, eds. Handbook of hypertension. Experimental and genetic models of hypertension. Vol 16. Elsevier Science, 1994.
38. Dahl LK, Heine M, Tassinari L. Effects of chronic excess salt ingestion. Evidence that genetic factors play an important role in susceptibility to experimental hypertension. J Exp Med 1962; 115:1173-1190.
39. Ben-Ishay D, Saliternick R, Welner A. Separation of two strains of rats inbred for dissimilar sensitivity to DOCA_salt hypertension. Experientia 1972; 28:1321-1322.
40. Hilbert P, Lindpaintner K, Beckmann JS, Serikawa T, Soubrier F, Dubay C, Cartwright P, De Gouyon B, Julier C, Takahasi, S, Vincent M, Ganten D, Georges M, Lathrop GM. Chromosomal mapping of two genetic loci associated with blood pressure regulation in hereditary hypertensive rat. Nature 1991; 353:521-529.
41. Jacob HJ, Lindpaintner K, Lincoln SE, Kusumi K, Bunker RK, Mao YP, Ganten D, Dzau VJ, Lander ES. Genetic mapping of a gene causing hypertension in the stroke-prone spontaneoulsy hypertensive rat. Cell 1991; 67:213-224.
42. Nara Y, Nabika T, Ikeda K, Sawamura M, Endo J, Yamori Y. Blood pressure cosegregates with a microsatellite of angiotensin I converting enzyme (ACE) in F2 generation from a cross between original normotensive Wistar-Kyoto rat (WKY) and stroke-prone spontaneously hypertensive rat (SHRSP). Biochem Biophys Res Commun 1991; 181:941-946.
43. Nara Y, Nabika T, Ikeda K, Sawamura M, Mano M, Endo J, Yamori Y. Basal high blood pressure cosegregates with the loci on chromosome 1 in the F2 generation from crosses between normotensive Wistar Kyoto rats and stroke-prone spontaneously hypertensive rats. Biochem Biophis Res Commun 1993; 194:1344-1351.
44. Nabika T, Nara Y, Ikeda K, Endo J, Yamori Y. A new genetic locus cosegregating with blood pressure in F2 progeny obtained from stroke-prone spontaneously hypertensive rats and Wistar-Kyoto rats. J Hypertens 1993; 11:13-18.
45. Iwai N, Inagami T. Isolation of preferentially expressed genes in the kidneys of hypertensive rats. Hypertension 1991; 17:242-246.
46. Okuda T, Sumiya T, Iwai N, Miyata T. Difference of gene expression profiles in spontaneous hypertensive rats and Wistar-Kyoto rats from two sources. Biochem Biophys Res Commun 2002; 296:537-543.
47. Meneely GR, Ball COT. Experimental epidemiology of chronic sodium chloride toxicity and the protective effect of potassium chloride. Am J Med 1958; 25:713.
48. Pfeffer MA, Pfeffer J, Mirsky I, Iwai J. Cardiac hypertrophy and performance of Dahl hypertensive rats on graded salt diets. Hypertension 1984; 6:475-481.
49. Inoko M, Kihara Y, Sasayama S. Neurohumoral factors during transition from left ventricular hypertrophy to failure in Dahl salt sensitive rats. Biochem Biophys Res Commun 1995; 206:814-820.
50. Sterzel RB, Luft FC, Gao Y, Schnermann J, Briggs JP, Ganten D, Waldherr R, Schnabel E, Kriz W. Renal disease and the development of hypertension in salt sensitive Dahl rats. Kidney Int 1988; 3:1119-1129.
51. Rapp JP. Dahl salt-susceptible and salt-resistant rats. A review. Hypertension 1982; 4:753-763.
52. Terry AV Jr, Hernandez CM, Buccafusco JJ. Dahl salt-sensitive and salt-resistant rats: examination of learning and memory performance, blood pressure, and the expression of central nicotinic acetylcholine receptors. Neuroscience 2001; 103:351-363.
53. Langheinrich M, Lee MA, Bohm M, Pinto YM, Ganten D, Paul M. The hypertensive Ren-2 transgenic rat TGR (mREN2)27 in hypertension research. Characteristics and functional aspects. Am J Hypertens 1996; 9:506-512.
54. Lee MA, Bohm M, Paul M, Bader M, Ganten U, Ganten D. Phisiological characterization of the hypertensive transgenic rat TGR (mREN2)27. Am J Physiol 1996; 270:E919-E929.
55. Pinto YM, Buikema H, van Gilst WH, Scholtens E, van Geel PP, de Graeff PA, Wagner J, Paul M. Cardiac and vascular dysfunction is more severe in hypertensive transgenic mREN2 gene than in spontaneoulsy hypertensive rats. J Mol Med 1997; 75:371-377.
56. Bohlender J, Hildenbrand U, Wagner KD, Gunther J, Hempel P, Schlegel WP, Luft FC, Krause EG, Bartel S. Myocardial adrenergic dysfunction in rats with transgenic, human renin-dependent hypertension. J Hypertens 2001; 19:1453-1463.
57. Heur J, Dechend R, Muller DN, Park JK, Fiebeler A, Barta P, Ganten D, Haller H, Dietz R, Luft FC. Angiotensin II induced inflammation in the kidney and in the heart of double transgenic rats. BMC Cardiovasc Disord 2002; 2:3.
58. Cvetkovic B, Sidmund CD. Understanding hypertension through genetic manipulation in mice. Kidney Int 2000; 57:863-874.
59. Fukamizu A, Seo MS, Hatae T, Yokoyama M, Nomura T, Katsuki, M, Marukami K. Tissue specific expression of the human renin gene in transgenic mice. Biochem Biophys Res Commun 1989; 165:826-832.
60. Yang G, Sigmund CD. Development expression of human angiotensinogen in transgenic mice. Am J Physiol 1998; 274:F932-F939.
61. Fukamizu A, Sugimura K, Takimoto E, Sugiyama F, Seo MS, Takahashi S, Hatae T, Kajiwara N, Yagami K, Murakami K. Chimeric renin-angiotensin system demonstrates sustained increase in blood pressure of transgenic mice carrying both human renin and human renin and human angiotensinogen genes. J Clin Invest 1993; 268:11617-11621.
62. Merril DC, Thompson MW, Carney C, Schlager G, Robillard JE, Sigmund CD. Chronic hypertension and altered baroflex responses in transgenic mice containing the human renin and human angiotensinogen genes. J Clin Invest 1996; 97:1047-1055.
63. Shimokama T, Haraoka S, Horoguchi H, Sugiyama F, Murakami K, Watanabe T. The Tsukuba hypertensive mouse (transgenic mouse carrying human genes for both renin and angiotensinogen) as a model of human malignant hypertension: development of lesions and morphometric analysis. Virchows Arch 1998; 432:169-175.
64. Kim HS, Krege JH, Kluckman KD, Hagaman JR, Hodgin JB, Best CF, Jennette JC, Coffman TM, Maeda N, Smithies O. Genetic control of blood pressure and the angiotensinogen locus. Proc Natl Acad Sci USA 1995; 92:2735-2739.
65. Tanimoto K, Sugiyama F, Goto Y, Ishida J, Takimoto E, Yagami K, Fukamizu A, Murakami K. Angiotensinogen-deficient mice with hypotension. J Biol Chem 1994; 269:31334-31337.
66. Shesely EG, Maeda N, Kim HS, Desai KM, Krege JH, Laubach VE, Sherman PA, Sessa WC, Smithies O. Elevated blood pressures in mice lacking endothelial nitric oxide synthase. Proc Natl Acad Sci USA 1996; 93:13176-13181.
67. Rudic RD, Shesely EG, Maeda N, Smithies O, Segal SS, Sessa WC. Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodelling. J Clin Invest 1998; 101:731-736.
68. Alfie ME, Sigmon DH, Pomposiello SI, Carretero OA. Effect of high salt intake in mutant mice lacking branykinin-B2 receptor. Hypertension 1997; 29:483-487.
69. Albrecht FE, Drago J, Felder RA, Printz MP, Eisner GM, Robillard JE, Sibley DR, Westphal HJ, Jose PA. Role of the D1A dopamine receptor in the pathogenesis of genetic hypertension. J Clin Invest 1996; 97:2283-2288.
70. John SW, Krege JH, Oliver PM, Hagaman JR, Hodgin JB, Pang SC, Flynn TG, Smithies O. Genetic decreases in atrial natriuretic peptide and salt-sensitive hypertension. Science 1995; 267:679-681.
71. Wada T, Kanagawa R, Ishimura Y, Inada Y, Nishikawa K. Role of angiotensin II in cerebrovascular and renal damage in deoxycorticosterone acetate-salt hypertensive rats. J Hypertens 1995; 13:113-122.
72. Lehr RP Jr, Browning RA, Myers JH. Gross morphological brain differences between Wistar-Kyoto and spontaneously hypertensive rats. Clin Exp Hypertens 1980; 2:123-127.
73. Nelson DO, Boulant JA. Altered CNS neuroanatomical organization of spontaneously hypertensive (SHR) rats. Brain Res 1981; 226:119-130.
74. Tajima A, Hans FJ, Livingstone D, Wei L, Finnegan W, De Maro J, Fenstermacher J. Smaller local brain volumes and cerebral atrophy in spontaneously hypertensive rats. Hypertension 1993; 21:105-111.
75. Baumbach GL, Heistad DD. Drug-induced changes in mechanics and structure of cerebral arterioles. J Hypertens Suppl 1992; 10:S137-S140.
76. Baumbach GL, Dobrin PB, Hart MN, Heistad DD. Mechanics of cerebral arterioles in hypertensive rats. Circ Res 1988a; 62:56-64.
77. Heagerty AM, Aalkjaer C, Bund SJ, Korsgaard N, Mulvany MJ. Small artery structure in hypertension. Dual processes of remodeling and growth. Hypertension 1993; 21:391-397.
78. Sabbatini M, Strocchi P, Vitaioli L, Amenta F. Microanatomical changes of intracerebral arteries in spontaneously hypertensive rats: a model of cerebrovascular disease of the elderly. Mech Ageing Dev 2001a; 122:1257-1268.
79. Ritter S, Dinh TT. Progressive postnatal dilation of brain ventricles in spontaneously hypertensive rats. Brain Res 1986; 370:327-332.
80. Ritter S, Dinh TT, Stone S, Ross N. Cerebroventricular dilation in spontaneously hypertensive rats (SHRs) is not attenuated by reduction of blood pressure. Brain Res 1988; 450:354-359.
81. Bendel P, Eilam R. Quantitation of ventricular size in normal and spontaneously hypertensive rats by magnetic resonance imaging. Brain Res 1992; 574:224-228.
82. Sabbatini M, Baldoni E, Cadoni A, Vitaioli L, Zicca A, Amenta F. Forebrain white matter in spontaneously hypertensive rats: a quantitative image analysis study. Neurosci Lett 1999; 265:5-8.
83. Sabbatini M, Strocchi P, Vitaioli L, Amenta F. The hippocampus in spontaneously hypertensive rats: a quantitative microanatomical study. Neuroscience 2000; 100:251-258.
84. Sabbatini M, Tomassoni D, Amenta F. Hypertensive brain damage: comparative evaluation of protective effect of treatment with dihydropyridine derivatives in spontaneously hypertensive rats. Mech Ageing Dev 2001b; 122:2085-2105.
85. Sabbatini M, Catalani A, Consoli C, Marletta N, Tomassoni D, Avola R. The hippocampus in spontaneously hypertensive rats: an animal model of vascular dementia? Mech Ageing Dev 2002; 123:547-559.
86. Amenta F, Strocchi P, Sabbatini M. Vascular and neuronal hypertensive brain damage: protective effect of treatment with nicardipine. J Hypertens Suppl 1996; 14:S29-S35.
87. Breteler MM, van Swieten JC, Bots ML, Grobbee DE, Claus JJ, van den Hout JH, van Harskamp F, Tanghe HL, de Jong PT, van Gijn J. Cerebral white matter lesions, vascular risk factors, and cognitive function in a population-based study: the Rotterdam Study. Neurology 1994; 44:1246-1252.
88. Lindgren A, Roijer A, Rudling O, Norrving B, Larsson EM, Eskilsson J, Wallin L, Olsson B, Johansson BB. Cerebral lesions on magnetic resonance imaging, heart disease, and vascular risk factors in subjects without stroke. A population-based study. Stroke 1994; 25:929-934.
89. Baumbach GL, Walmsley JG, Hart MN. Composition and mechanics of cerebral arterioles in hypertensive rats. Am J Pathol 1988b; 133:464-471.
90. Hajdu MA, Heistad DD, Ghoneim S, Baumbach GL. Effects of antihypertensive treatment on composition of cerebral arterioles. Hypertension 1991; 18:II15-21.
91. Baumbach GL. ACE inhibitor-based therapy correte structural abnormalities of cerebral arterioles. Symposium Report - 9th Europ Meet Hypert 1999; 4-5.
92. Heckmann JG, Erbguth FJ, Hilz MJ, Lang CJ, Neundorfer B. Cerebrovascular circulation from a clinical view. Historical review, physiology, pathophysiology, diagnostic and therapeutic aspects. Med Klin 2001; 96:583-592.
93. Ogunniyi A, Talabi O. Cerebrovascular complications of hypertension. Niger J Med 2001; 10:158-161.
94. Wei L, Lin S, Tajima A, Nakata H, Acuff V, Patlak C, Pettigrew K, Fenstermacher J. Cerebral glucose utilization and blood flow in adult spontaneously hypertensive rats. Hypertension 1992; 20:501-510.
95. Katsuta T Decreased cerebral blood flow in young and aged spontaneously hypertensive rats. Fukuoka Igaku Zasshi 1997; 88:65-74.
96. Johansson BB. Pentoxifylline: cerebral blood flow and glucose utilization in conscious spontaneously hypertensive rats. Stroke 1986; 17:744-747.
97. Mori S, Kato M, Fujishima M. Impaired maze learning and cerebral glucose utilization in aged hypertensive rats. Hypertension 1995; 5:545-553.
98. Fujishima M, Ibayashi S, Fujii K, Mori S. Cerebral blood flow and brain function in hypertension. Hypertens Res 1995; 18:111-117.
99. Nordborg C, Fredriksson K, Johansson BB. The morphometry of consecutive segments in cerebral arteries of normotensive and spontaneously hypertensive rats. Stroke 1985; 16:313-320.
100. Baumbach GL, Heistand DD. Cerebral circulation in chronic arterial hypertension. Hypertension 1988; 12:89-95.
101. Mayan WG, Faraci FM. Cerebral vasoconstrictor responses to serotonin during chronic hypertension. Hypertension 1990; 15:872-876.
102. Fujishima M, Sadoshima S, Ogata J, Yoshida F, Shiokawa O, Ibayashi S, Omae T. Autoregulation of cerebral blood flow in young and aged spontaneously hypertensive rats (SHR). Gerontology 1984; 30:30-36.
103. Knox CA, Yates RD, Chen I, Klara PM. Effects of aging on the structural and permeability characteristics of cerebrovasculature in normotensive and hypertensive strains of rats. Acta Neuropathol 1980; 51:1-13.
104. Elias MF, Wolf PA, D'Agostino RB, Cobb J, White LR. Untreated blood pressure level is inversely related to cognitive functioning: the Framingham Study. Am J Epidemiol 1993; 138:353-364.
105. Elias MF, D'Agostino RB, Elias PK, Wolf PA. Neuropsychological test performance, cognitive functioning, blood pressure, and age: the Framingham Heart Study. Exp Aging Res 1995; 21:369-391.
106. Waldstein SR, Manuck SB, Ryan CM, Muldoon MF. Neuropsychological correlates of hypertension: review and methodologic considerations. Psychol Bull 1991a; 110:451-468.
107. Waldstein SR, Ryan CM, Manuck SB, Parkinson DK, Bromet EJ. Learning and memory function in men with untreated blood pressure elevation. J Consult Clin Psychol 1991b; 59:513-517.
108. Waldstein SR, Jennings JR, Ryan CM, Muldoon MF, Shapiro AP, Polefrone JM, Fazzari TV, Manuck SB. Hypertension and neuropsychological performance in men: interactive effects of age. Health Psychol 1996; 15:102-109.
109. Desmond DW, Tatemichi TK, Paik M, Stem Y. Risk factors for cerebrovascular disease as correlates of cognitive function in a stroke-free cohort. Arch Neurol 1993; 50:162-166.
110. Farmer ME, White LR, Abbott RD, Kittner SJ, Kaplan E, Wolz MM, Brody JA, Wolf PA. Blood pressure and cognitive performance. The Framingham Study. Am J Epidemiol 1987; 126:1103-1114.
111. Low WC, Whitehorn D, Hendley ED. Genetically related rats with differences in hippocampal uptake of norepinephrine and maze performance. Brain Res Bull 1984; 12:703-709.
112. Wyss JM, Fisk G, van Groen T. Impaired learning and memory in mature spontaneously hypertensive rats. Brain Res 1992; 592:135-140.
113. Gattu M, Pauly JR, Boss KL, Summers JB, Buccafusco JJ. Cognitive impairment in spontaneously hypertensive rats: role of central nicotinic receptors. I. Brain Res 1997; 771:89-103.
114. Gattu M, Pauly JR, Urbanawiz S, Buccafusco JJ. Autoradiographic comparison of muscarinic M1 and M2 binding sites in the CNS of spontaneously hypertensive and normotensive rats. Brain Res 1997; 771:173-183.
115. Kimura S, Saito H, Minami M, Togashi H, Nakamura N, Nemoto M, Parvez HS. Pathogenesis of vascular dementia in stroke-prone spontaneously hypertensive rats. Toxicology 2000; 153:167-178.
116. Saito H, Togashi H, Yoshioka M, Nakamura N, Minami M, Parvez SH. Animal models of vascular dementia with emphasis on stroke-prone spontaneously hypertensive rats. Clin Exp Pharmacol Physiol 1995; 22:S257-S259.
117. Togashi H, Matsumoto M, Yoshioka M, Hirokami M, Minami M, Saito H. Neurochemical profiles in cerebrospinal fluid of stroke-prone spontaneously hypertensive rats. Neurosci Lett 1994; 166:117-120.
118. Togashi H, Kimura S, Matsumoto M, Yoshioka M, Minami M, Saito H. Cholinergic changes in the hippocampus of stroke-prone spontaneously hypertensive rats. Stroke 1996; 27:520-525.
119. Ferrari R, Frasoldati A, Leo G, Torri C, Zini I, Agnati LF, Zoli M. Changes in nicotinic acetylcholine receptor subunit mRNAs and nicotinic binding in spontaneously hypertensive stroke prone rats. Neurosci Lett 1999; 277:169-172.
120. Knardahl S, Karlsen K. Passive-avoidance behavior of spontaneously hypertensive rats. Behav Neural Biol 1984; 42:9-22.
121. Sutturer JR, Devito W, Rykaszewski I. Developmental aspect of 2-way shuttlebox avoidance in the spontaneously hypertensive and normotensive rat. Devl Psychobiol 1981; 14:405-414.
122. Sutturer JR, Perry J, Devito W. Two-way shuttlebox and lever-press avoidance in the spontaneously hypertensive and normotensive rat. J Comp Physiol Psychol 1980; 94:155-163.
123. Meneses A, Castillo C, Ibarra M, Hong E. Effects of aging anf hypertension on learning, memory and activity in rats. Physiol Behav 1996; 60:341-345.
124. Nakamura-Palacios EM, Caldas CK, Fiorini A, Chagas KD, Chagas KN, Vasquez EC. Deficits and spatial learning and working memory in spontaneously hypertensive rats. Behav Brain Res 1996; 74:217-221.
125. Terry AV Jr, Hernandez CM, Buccafusco JJ, Gattu M. Deficits in spatial learning and nicotinic-acetylcholine receptors in older, spontaneously hypertensive rats. Neuroscience 2000; 101:357-368.
126. Gottfries CG, Blennow K, Karlsson I, Wallin A. The neurochemistry of vascular dementia. Dementia 1994; 5:163-167.
127. Wallin A, Alafuzoff I, Carlsson A, Eckemas SA, Gottfries CG, Karlsson I, Svennerholm L, Winblad B. Neurotransmitter deficits in a non-multi-infarct category of vascular dementia. Acta Neurol Scand 1989; 79:397-406.
128. Tohgi H, Abe T, Kimura M, Saheki M, Takahashi S. Cerebrospinal fluid acetylcholine and choline in vascular dementia of Binswanger and multiple small infarct types as compared with Alzheimer-type dementia. J Neural Transm 1996; 103:1211-1220.
129. Grabowski M, Nordborg C, Brundin P, Johansson BB. Middle cerebral artery occlusion in the hypertensive and normotensive rat: a study of histopathology and behaviour. J Hypertens 1988; 6:405-411.
130. Leys D, Deplanque D, Lucas C, Bordet R. Hypolipemic agents for stroke prevention. Clin Exp Hypertens 2002; 24:573-594.
131. Sauter A, Rudin M. Failure of isradipine in cerebral ischemia models. Stroke 1996; 27:775-776.
132. Hirata H, Asanuma M, Tanaka K, Kondo Y, Ogawa N. M1 receptors in blood pressure-controlled ischemic spontaneously hypertensive rats. Stroke 1995; 26:1268-1272.
133. Amenta F, Mignini F, Rabbia F, Tomassoni D, Veglio F. Protective effect of anti-hypertensive treatment on cognitive function in essential hypertension. Analysis of published clinical data. J Neurol Sci 2002; 15:47-51.
134. Lazarewicz JW, Pluta R, Puka M, Salinska E. Diverse mechanisms of neuronal protection by nimodipine in experimental rabbit brain ischemia. Stroke 1990; 21:IV108-IV110.
135. Korenkov AI, Pahnke J, Frei K, Warzok R, Schroeder HW, Frick R, Muljana L, Piek J, Yonekawa Y, Gaab MR. Treatment with nimodipine or mannitol reduces programmed cell death and infarct size following focal cerebral ischemia. Neurosurg Rev 2000; 23:145-150.
136. Campbell CA, Mackay KB, Patel S, King PD, Stretton JL, Hadingham SJ, Hamilton TC. Effects of isradipine, an L-Type calcium channel blocker on permanent and transient focal cerebral ischemia in spontaneously hypertensive rats. Exp Neurol 1997; 148:45-50.
137. Shinyama H, Nagai H, Kawamura T, Narita Y, Nakamura N, Kagitani Y. Therapeutic effects of AE0047, a novel calcium antagonist, on progression of brain damage after stroke in stroke-prone spontaneously hypertensive rats. Gen Pharmacol 1998; 30:379-386.
138. Sabbatini M, Strocchi P, Amenta F. Nicardipine and treatment of cerebrovascular diseases with particular reference to hypertension-related disorders. Clin Exp Hypertens 1995; 17:719-750.
139. Sadoshima S, Ibayashi S, Nakane H, Okada Y, Ooboshi H, Fujishima M. Attenuation of ischemic and postischemic damage to brain metabolism and circulation by a novel Ca2+ channel antagonist, NC-1100, in spontaneously hypertensive rats. Eur J Pharmacol 1992; 224:109-115.
140. Blezer E, Nicolay K, Goldschmeding R, Koomans H, Joles J. Reduction of cerebral injury in stroke-prone spontaneously hypertensive rats by amlodipine. Eur J Pharmacol 2002; 444:75-81.
141. Zapater P, Moreno J, Horga JF. Neuroprotection by the novel calcium antagonist PCA50938, nimodipine and flunarizine, in gerbil global brain ischemia. Brain Res 1997; 772:57-62.
142. Takahashi M, Fritz-Zieroth B, Ohta Y, Chikugo T. Therapeutic effects of imidapril on cerebral lesions observed by magnetic resonance imaging in malignant stroke-prone spontaneously hypertensive rats. J Hypertens 1994; 12:761-768.
143. Blezer EL, Nicolay K, Koomans HA, Joles JA. Losartan versus enalapril on cerebral edema and proteinuria in stroke-prone hypertensive rats. Am J Hypertens 2001; 14:54-61.
144. Lysko PG, Lysko KA, Yue TL, Webb CL, Gu JL, Feuerstein G. Neuroprotective effects of carvedilol, a new antihypertensive agent, in cultured rat cerebellar neurons and in gerbil global brain ischemia. Stroke 1992; 23:1630-1635.
145. Ruchoux MM, Huguet F, Droy-Lefaix MT, Gelot A, Ruchoux P, Autret A. The effect of cicletanine on cerebrovascular injury in stroke-prone spontaneously hypertensive rats. Am J Hypertens 1989; 2:683-689.
146. Bataillard A, Schiavi P, Sassard J. Pharmacological properties of indapamide. Rationale for use in hypertension. Clin Pharmacokinet 1999; 37:7-12.
147. Delbarre B, Delbarre G. Effect of indapamide on an experimental model of cerebral ischemia in hypertensive rats. Am J Med 1988; 84:20-25.
148. Prince MJ. The treatment of hypertension in older people and its effect on cognitive function. Biomed Pharmacother 1997; 51:208-212.
149. Gorelick PB, Erkinjuntti T, Hofman A, Rocca WA, Skoog I, Winblad B. Prevention of vascular dementia. Alzheimer Dis Assoc Disord 1999; 13:S131-S139.
150. Brierly JB, Graham DI. Hypoxia and vascular disorders of the central nervous system. In: Adams JH, Corsellis JAN, Duchen LW, eds. Greenfield's Neuropathology. 4th ed. London: Arnold, 1984.