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Brain White Matter Hyperintensity Changes Associated with Vascular Cognitive Impairment and Dementia, Alzheimer's Dementia and Normal Aging

Year 2021, Volume: 23 Issue: 3, 305 - 312, 30.12.2021
https://doi.org/10.18678/dtfd.1012133

Abstract

Aim: The aim of this study was to analyze the relationship between the distribution and grading of white matter hyperintensity (WMH) obtained by brain magnetic resonance imaging and cognitive impairment associated with vascular cognitive impairment and dementia (VCID), Alzheimer's dementia (AD) and normal aging in individuals aged 65 years and older.
Material and Methods: Retrospective analysis was performed on a total of 372 patients, who met the criteria for AD, VCID and normal aging. The basic clinical criteria of DSM-V and NIA-AA were considered for AD. The DSM-V and NINDS-AIREN diagnostic criteria were used for VCID and probable vascular dementia (VaD). WMHs were graded according to the Fazekas criteria.
Results: Normal aging was detected in 58.3% (n=217) of the patients, AD in 24.7% (n=92) and VCID in 16.9% (n=63). The relationship between WMH and dementia was significant. (p<0.001). Periventricular hyperintensity was detected as 76.2% (n=70) in AD, 95.2% (n=60) in VCID, 40.6% (n=88) in normal aging, and deep white matter hyperintensity was detected as 63.0% (n=58) in AD, 74.5% (n=47) in VCID, 44.2% (n=96) in normal aging. In the VCID group, 52.4% (n=33) had basal ganglia lesions and 60.3% (n=38) had classical infarct areas. No relationship was found between the presence of cortical lesion and cognition.
Conclusion: This study is important in terms of showing that it would be better to focus on markers of brain damage and dementia, such as WMH rather than focusing on clinical diagnoses with mixed-type pathologies such as Alzheimer's disease or vascular cognitive impairment.

References

  • Debette S, Markus HS. The clinical importance of white matter hyperintensities on brain magnetic resonance imaging: systematic review and meta-analysis. BMJ. 2010;341:c3666.
  • Sachdev PS, Thalamuthu A, Mather KA, Ames D, Wright MJ, Wen W, et al. White matter hyperintensities are under strong genetic influence. Stroke. 2016;47(6):1422-8.
  • Gouw AA, Seewann A, van der Flier WM, Barkhof F, Rozemuller AM, Scheltens P, et al. Heterogeneity of small vessel disease: a systematic review of MRI and histopathology correlations. J Neurol Neurosurg Psychiatry. 2011;82(2):126-35.
  • Schmidt R, Schmidt H, Haybaeck J, Loitfelder M, Weis S, Cavalieri M, et al. Heterogeneity in age-related white matter changes. Acta Neuropathol. 2011;122(2):171-85.
  • Kim SH, Park JS, Ahn HJ, Seo SW, Lee JM, Kim ST, et al. Voxel-based analysis of diffusion tensor imaging in patients with subcortical vascular cognitive impairment: correlates with cognitive and motor deficits. J Neuroimaging. 2011;21(4):317-24.
  • Béjot Y, Aboa-Eboulé C, Durier J, Rouaud O, Jacquin A, Ponavoy E, et al. Prevalence of early dementia after first-ever stroke: a 24-year population-based study. Stroke. 2011;42(3):607-12.
  • Gorelick PB, Scuteri A, Black SE, Decarli C, Greenberg SM, Iadecola C, et al. Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2011;42(9):2672-713.
  • Regier DA, Kuhl EA, Kupfer DJ. The DSM-5: Classification and criteria changes. World Psychiatry. 2013;12(2):92-8.
  • McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR Jr, Kawas CH, et al. The diagnosis of dementia due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement. 2011;7(3):263-9.
  • Pohjasvaara T, Mäntylä R, Ylikoski R, Kaste M, Erkinjuntti T. Comparison of different clinical criteria (DSM-III, ADDTC, ICD-10, NINDS-AIREN, DSM-IV) for the diagnosis of vascular dementia. National Institute of Neurological Disorders and Stroke-Association Internationale pour la Recherche et l'Enseignement en Neurosciences. Stroke. 2000;31(12):2952-7.
  • Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA. MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol. 1987;149(2):351-6.
  • Senda J, Ito K, Kotake T, Kanamori M, Kishimoto H, Kadono I, et al. Association of leukoaraiosis with convalescent rehabilitation outcome in patients with ischemic stroke. Stroke. 2016;47(1):160-6.
  • Kapasi A, DeCarli C, Schneider JA. Impact of multiple pathologies on the threshold for clinically overt dementia. Acta Neuropathol. 2017;134(2):171-86.
  • Bartzokis G. Alzheimer’s disease as homeostatic responses to agerelated myelin breakdown. Neurobiol Aging. 2011;32(8):1341-71.
  • Matute C. Calcium dyshomeostasis in white matter pathology. Cell Calcium. 2010;47(2):150-7.
  • Marnane M, Al-Jawadi OO, Mortazavi S, Pogorzelec KJ, Wang BW, Feldman HH, et al. Periventricular hyperintensities are associated with elevated cerebral amyloid. Neurology. 2016;86(6):535-43.
  • Lee S, Viqar F, Zimmerman ME, Narkhede A, Tosto G, Benzinger TL, et al. White matter hyperintensities are a core feature of Alzheimer’s disease: evidence from the dominantly inherited Alzheimer network. Ann Neurol. 2016;79(6):929-39.
  • Smith EE. Cerebral amyloid angiopathy as a cause of neurodegeneration. J Neurochem. 2018;144(5):651-8.
  • Roseborough A, Ramirez J, Black SE, Edwards JD. Associations between amyloid beta and white matter hyperintensities: a systematic review. Alzheimers Dement. 2017;13(10):1154-67.
  • Dallaire-Théroux C, Callahan BL, Potvin O, Saikali S, Duchesne S. Radiological- pathological correlation in Alzheimer’s disease: systematic review antemortem magnetic resonance imaging findings. J Alzheimers Dis. 2017;57(2):575-601.
  • McAleese KE, Walker L, Graham S, Moya ELJ, Johnson M, Erskine D, et al. Parietal white matter lesions in Alzheimer’s disease are associated with cortical neurodegenerative pathology, but not with small vessel disease. Acta Neuropathol. 2017;134(3):459-73.
  • Kalaria RN, Akinyemi R, Ihara M. Does vascular pathology contribute to Alzheimer changes? J Neurol Sci. 2012;322(1-2):141-7.
  • Pendlebury ST, Rothwell PM, Oxford Vascular Study. Incidence and prevalence of dementia associated with transient ischaemic attack and stroke: analysis of the population-based Oxford Vascular Study. Lancet Neurol. 2019;18(3):248-58.
  • Moulin S, Labreuche J, Bombois S, Rossi C, Boulouis G, Hénon H, et al. Dementia risk after spontaneous intracerebral haemorrhage: a prospective cohort study. Lancet Neurol. 2016;15(8):820-9.
  • Iadecola C, Yaffe K, Biller J, Bratzke LC, Faraci FM, Gorelick PB, et al. Impact of hypertension on cognitive function: a scientific statement from the American Heart Association. Hypertension. 2016;68(6):e67-94.
  • Umegaki H. Impaired glycemia and Alzheimer’s disease. Neurobiol Aging. 2014;35(10):e21.
  • Abner EL, Nelson PT, Kryscio RJ, Schmitta FA, Fardo DW, Woltjer RL, et al. Diabetes is associated with cerebrovascular but not Alzheimer neuropathology. Alzheimers Dement. 2016;12(8):882-9.
  • Moon JH, Lim S, Han JW, Kim KM, Choi SH, Park KS, et al. Carotid intima-media thickness is associated with the progression of cognitive impairment in older adults. Stroke. 2015;46(4):1024-30.
  • Kandiah N, Goh O, Mak E, Marmin M, Ng A. Carotid stenosis: a risk factor for cerebral white-matter disease. J Stroke Cerebrovasc Dis. 2014;23(1):136-9.
  • Baradaran H, Mtui EE, Richardson JE, Delgado D, Dunning A, Marshall RS, et al. White matter diffusion abnormalities in carotid artery disease: a systematic review and meta-analysis. J Neuroimaging. 2016;26(5):481-8.
  • Ryberg C, Rostrup E, Paulson OB, Barkhof F, Scheltens P, van Straaten EC, et al. Corpus callosum atrophy as a predictor of age-related cognitive and motor impairment: a 3-year follow-up of the LADIS study cohort. J Neurol Sci. 2011;307(1-2):100-5.
  • Marshall RS. Effects of altered cerebral hemodynamics on cognitive function. J Alzheimers Dis. 2012;32(3):633-42.
  • Shih AY, Blinder P, Tsai PS, Friedman B, Stanley G, Lyden PD, et al. The smallest stroke: occlusion of one penetrating vessel leads to infarction and a cognitive deficit. Nat Neurosci. 2013;16(1):55-63.
  • Iadecola C. The neurovascular unit coming of age: a journey through neurovascular coupling in health and disease. Neuron.2017;96(1):17-42.
  • Joutel A, Chabriat H. Pathogenesis of white matter changes in cerebral small vessel diseases: beyond vessel-intrinsic mechanisms. Clin Sci. 2017;131(8):635-51.
  • Hase Y, Horsburgh K, Ihara M, Kalaria RN. White matter degeneration in vascular and other ageing-related dementias. J Neurochem. 2018;144(5):617-33.
  • Kalaria RN, Akinyemi R, Ihara M. Stroke injury, cognitive impairment and vascular dementia. Biochim Biophys Acta. 2016;1862(5):915-25.
  • Arvanitakis Z, Capuano AW, Leurgans SE, Bennett DA, Schneider JA. Relation of cerebral vessel disease to Alzheimer’s disease dementia and cognitive function in elderly people: a cross-sectional study. Lancet Neurol. 2016;15(9):934-43.
  • Thal DR, Grinberg LT, Attems J. Vascular dementia: different forms of vessel disorders contribute to the development of dementia in the elderly brain. Exp Gerontol. 2012;47(11):816-24.
  • Iadecola C. The pathobiology of vascular dementia. Neuron. 2013;80(4):844-66.
  • Schneider JA, Arvanitakis Z, Bang W, Bennett DA. Mixed brain pathologies account for most dementia cases in community-dwelling older persons. Neurology. 2007;69(24):2197-204.
  • Kalaria RN, Kenny RA, Ballard CG, Perry R, Ince P, Polvikoski T. Towards defining the neuropathological substrates of vascular dementia. J Neurol Sci. 2004;226(1-2):75-80.
  • Fernando MS, Simpson JE, Matthews F, Brayne C, Lewis CE, Barber R, et al. White matter lesions in an unselected cohort of the elderly: molecular pathology suggests origin from chronic hypoperfusion injury. Stroke. 2006;37(6):1391-8.
  • Valdés Hernández MC, Piper RJ, Bastin ME, Royle NA, Maniega SM, Aribisala BS, et al. Morphologic, distributional, volumetric, and intensity characterization of periventricular hyperintensities. AJNR Am J Neuroradiol. 2014;35(1):55-62.
  • Fazekas F. Incidental periventricular white matter hyperintensities revisited: what detailed morphologic image analyses can tell us. AJNR Am J Neuroradiol. 2014;35(1):63-4.
  • Ryu WS, Woo SH, Schellingerhout D, Chung MK, Kim CK, Jang MU, et al. Grading and interpretation of white matter hyperintensities using statistical maps. Stroke. 2014;45(12):3567-75.

Vasküler Kognitif Bozukluk ve Demans, Alzheimer Demans ve Normal Yaşlanma ile İlişkili Beyin Beyaz Cevher Hiperintensite Değişiklikleri

Year 2021, Volume: 23 Issue: 3, 305 - 312, 30.12.2021
https://doi.org/10.18678/dtfd.1012133

Abstract

Amaç: Bu çalışmanın amacı, 65 yaş ve üstü bireylerde, beyin manyetik rezonans görüntüleme (MRG) ile elde edilen beyaz madde hiperintensitesinin (white matter hyperintensity, WMH) dağılımı ve derecelendirmesi ile vasküler kognitif bozukluk ve demans (VCID), Alzheimer demans (AD) ve normal yaşlanma ile ilişkili kognitif etkilenme arasındaki ilişkiyi analiz etmektir.
Gereç ve Yöntemler: AD, VCID ve normal yaşlanma kriterlerine uygun toplam 372 hasta ile geriye dönük analiz yapıldı. AD için DSM-V ve 2011 NIA-AA temel klinik kriterleri dikkate alındı. VCID ve olası vasküler demans (VaD) için DSM-V ve NINDS-AIREN tanı kriterleri kullanıldı. WMH'ler Fazekas kriterlerine göre derecelendirildi.
Bulgular: Katılımcıların %58,3’ünde (n=217) normal yaşlanma, %24,7’sinde (n=92) AD ve %16,9’unda (n=63) VCID tespit edildi. WMH ile demans arasındaki ilişki anlamlı idi (p<0.001). Periventriküler hiperintensite AD’de %76,2 (n=70), VCID’de %95,2 (n=60), normal yaşlanmada %40,6 (n=88) olarak tespit edildi ve derin beyaz madde hiperintensitesi ise AD’de %63,0 (n=58), VCID’de %74,5 (n=47), normal yaşlanmada %44,2 (n=96) olarak saptandı. VCID grubunda %52,4 (n=33) ile bazal ganglion lezyonları ve %60,3 (n=38) ile klasik enfarkt alanları mevcuttu. Kortikal lezyon varlığı ile kognisyon arasındaki ilişki tespit edilmedi.
Sonuç: Bu çalışma Alzheimer hastalığı veya vasküler bilişsel bozukluk gibi mix tip patolojileri olan klinik tanılara odaklanmak yerine, belki de WMH gibi beyin hasarı ve demans belirteçlerine odaklanmanın daha iyi olacağını göstermesi açısından önemlidir.

References

  • Debette S, Markus HS. The clinical importance of white matter hyperintensities on brain magnetic resonance imaging: systematic review and meta-analysis. BMJ. 2010;341:c3666.
  • Sachdev PS, Thalamuthu A, Mather KA, Ames D, Wright MJ, Wen W, et al. White matter hyperintensities are under strong genetic influence. Stroke. 2016;47(6):1422-8.
  • Gouw AA, Seewann A, van der Flier WM, Barkhof F, Rozemuller AM, Scheltens P, et al. Heterogeneity of small vessel disease: a systematic review of MRI and histopathology correlations. J Neurol Neurosurg Psychiatry. 2011;82(2):126-35.
  • Schmidt R, Schmidt H, Haybaeck J, Loitfelder M, Weis S, Cavalieri M, et al. Heterogeneity in age-related white matter changes. Acta Neuropathol. 2011;122(2):171-85.
  • Kim SH, Park JS, Ahn HJ, Seo SW, Lee JM, Kim ST, et al. Voxel-based analysis of diffusion tensor imaging in patients with subcortical vascular cognitive impairment: correlates with cognitive and motor deficits. J Neuroimaging. 2011;21(4):317-24.
  • Béjot Y, Aboa-Eboulé C, Durier J, Rouaud O, Jacquin A, Ponavoy E, et al. Prevalence of early dementia after first-ever stroke: a 24-year population-based study. Stroke. 2011;42(3):607-12.
  • Gorelick PB, Scuteri A, Black SE, Decarli C, Greenberg SM, Iadecola C, et al. Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2011;42(9):2672-713.
  • Regier DA, Kuhl EA, Kupfer DJ. The DSM-5: Classification and criteria changes. World Psychiatry. 2013;12(2):92-8.
  • McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR Jr, Kawas CH, et al. The diagnosis of dementia due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement. 2011;7(3):263-9.
  • Pohjasvaara T, Mäntylä R, Ylikoski R, Kaste M, Erkinjuntti T. Comparison of different clinical criteria (DSM-III, ADDTC, ICD-10, NINDS-AIREN, DSM-IV) for the diagnosis of vascular dementia. National Institute of Neurological Disorders and Stroke-Association Internationale pour la Recherche et l'Enseignement en Neurosciences. Stroke. 2000;31(12):2952-7.
  • Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA. MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol. 1987;149(2):351-6.
  • Senda J, Ito K, Kotake T, Kanamori M, Kishimoto H, Kadono I, et al. Association of leukoaraiosis with convalescent rehabilitation outcome in patients with ischemic stroke. Stroke. 2016;47(1):160-6.
  • Kapasi A, DeCarli C, Schneider JA. Impact of multiple pathologies on the threshold for clinically overt dementia. Acta Neuropathol. 2017;134(2):171-86.
  • Bartzokis G. Alzheimer’s disease as homeostatic responses to agerelated myelin breakdown. Neurobiol Aging. 2011;32(8):1341-71.
  • Matute C. Calcium dyshomeostasis in white matter pathology. Cell Calcium. 2010;47(2):150-7.
  • Marnane M, Al-Jawadi OO, Mortazavi S, Pogorzelec KJ, Wang BW, Feldman HH, et al. Periventricular hyperintensities are associated with elevated cerebral amyloid. Neurology. 2016;86(6):535-43.
  • Lee S, Viqar F, Zimmerman ME, Narkhede A, Tosto G, Benzinger TL, et al. White matter hyperintensities are a core feature of Alzheimer’s disease: evidence from the dominantly inherited Alzheimer network. Ann Neurol. 2016;79(6):929-39.
  • Smith EE. Cerebral amyloid angiopathy as a cause of neurodegeneration. J Neurochem. 2018;144(5):651-8.
  • Roseborough A, Ramirez J, Black SE, Edwards JD. Associations between amyloid beta and white matter hyperintensities: a systematic review. Alzheimers Dement. 2017;13(10):1154-67.
  • Dallaire-Théroux C, Callahan BL, Potvin O, Saikali S, Duchesne S. Radiological- pathological correlation in Alzheimer’s disease: systematic review antemortem magnetic resonance imaging findings. J Alzheimers Dis. 2017;57(2):575-601.
  • McAleese KE, Walker L, Graham S, Moya ELJ, Johnson M, Erskine D, et al. Parietal white matter lesions in Alzheimer’s disease are associated with cortical neurodegenerative pathology, but not with small vessel disease. Acta Neuropathol. 2017;134(3):459-73.
  • Kalaria RN, Akinyemi R, Ihara M. Does vascular pathology contribute to Alzheimer changes? J Neurol Sci. 2012;322(1-2):141-7.
  • Pendlebury ST, Rothwell PM, Oxford Vascular Study. Incidence and prevalence of dementia associated with transient ischaemic attack and stroke: analysis of the population-based Oxford Vascular Study. Lancet Neurol. 2019;18(3):248-58.
  • Moulin S, Labreuche J, Bombois S, Rossi C, Boulouis G, Hénon H, et al. Dementia risk after spontaneous intracerebral haemorrhage: a prospective cohort study. Lancet Neurol. 2016;15(8):820-9.
  • Iadecola C, Yaffe K, Biller J, Bratzke LC, Faraci FM, Gorelick PB, et al. Impact of hypertension on cognitive function: a scientific statement from the American Heart Association. Hypertension. 2016;68(6):e67-94.
  • Umegaki H. Impaired glycemia and Alzheimer’s disease. Neurobiol Aging. 2014;35(10):e21.
  • Abner EL, Nelson PT, Kryscio RJ, Schmitta FA, Fardo DW, Woltjer RL, et al. Diabetes is associated with cerebrovascular but not Alzheimer neuropathology. Alzheimers Dement. 2016;12(8):882-9.
  • Moon JH, Lim S, Han JW, Kim KM, Choi SH, Park KS, et al. Carotid intima-media thickness is associated with the progression of cognitive impairment in older adults. Stroke. 2015;46(4):1024-30.
  • Kandiah N, Goh O, Mak E, Marmin M, Ng A. Carotid stenosis: a risk factor for cerebral white-matter disease. J Stroke Cerebrovasc Dis. 2014;23(1):136-9.
  • Baradaran H, Mtui EE, Richardson JE, Delgado D, Dunning A, Marshall RS, et al. White matter diffusion abnormalities in carotid artery disease: a systematic review and meta-analysis. J Neuroimaging. 2016;26(5):481-8.
  • Ryberg C, Rostrup E, Paulson OB, Barkhof F, Scheltens P, van Straaten EC, et al. Corpus callosum atrophy as a predictor of age-related cognitive and motor impairment: a 3-year follow-up of the LADIS study cohort. J Neurol Sci. 2011;307(1-2):100-5.
  • Marshall RS. Effects of altered cerebral hemodynamics on cognitive function. J Alzheimers Dis. 2012;32(3):633-42.
  • Shih AY, Blinder P, Tsai PS, Friedman B, Stanley G, Lyden PD, et al. The smallest stroke: occlusion of one penetrating vessel leads to infarction and a cognitive deficit. Nat Neurosci. 2013;16(1):55-63.
  • Iadecola C. The neurovascular unit coming of age: a journey through neurovascular coupling in health and disease. Neuron.2017;96(1):17-42.
  • Joutel A, Chabriat H. Pathogenesis of white matter changes in cerebral small vessel diseases: beyond vessel-intrinsic mechanisms. Clin Sci. 2017;131(8):635-51.
  • Hase Y, Horsburgh K, Ihara M, Kalaria RN. White matter degeneration in vascular and other ageing-related dementias. J Neurochem. 2018;144(5):617-33.
  • Kalaria RN, Akinyemi R, Ihara M. Stroke injury, cognitive impairment and vascular dementia. Biochim Biophys Acta. 2016;1862(5):915-25.
  • Arvanitakis Z, Capuano AW, Leurgans SE, Bennett DA, Schneider JA. Relation of cerebral vessel disease to Alzheimer’s disease dementia and cognitive function in elderly people: a cross-sectional study. Lancet Neurol. 2016;15(9):934-43.
  • Thal DR, Grinberg LT, Attems J. Vascular dementia: different forms of vessel disorders contribute to the development of dementia in the elderly brain. Exp Gerontol. 2012;47(11):816-24.
  • Iadecola C. The pathobiology of vascular dementia. Neuron. 2013;80(4):844-66.
  • Schneider JA, Arvanitakis Z, Bang W, Bennett DA. Mixed brain pathologies account for most dementia cases in community-dwelling older persons. Neurology. 2007;69(24):2197-204.
  • Kalaria RN, Kenny RA, Ballard CG, Perry R, Ince P, Polvikoski T. Towards defining the neuropathological substrates of vascular dementia. J Neurol Sci. 2004;226(1-2):75-80.
  • Fernando MS, Simpson JE, Matthews F, Brayne C, Lewis CE, Barber R, et al. White matter lesions in an unselected cohort of the elderly: molecular pathology suggests origin from chronic hypoperfusion injury. Stroke. 2006;37(6):1391-8.
  • Valdés Hernández MC, Piper RJ, Bastin ME, Royle NA, Maniega SM, Aribisala BS, et al. Morphologic, distributional, volumetric, and intensity characterization of periventricular hyperintensities. AJNR Am J Neuroradiol. 2014;35(1):55-62.
  • Fazekas F. Incidental periventricular white matter hyperintensities revisited: what detailed morphologic image analyses can tell us. AJNR Am J Neuroradiol. 2014;35(1):63-4.
  • Ryu WS, Woo SH, Schellingerhout D, Chung MK, Kim CK, Jang MU, et al. Grading and interpretation of white matter hyperintensities using statistical maps. Stroke. 2014;45(12):3567-75.
There are 46 citations in total.

Details

Primary Language English
Subjects Clinical Sciences
Journal Section Research Article
Authors

Ayfer Ertekin 0000-0002-4313-2826

Publication Date December 30, 2021
Submission Date October 19, 2021
Published in Issue Year 2021 Volume: 23 Issue: 3

Cite

APA Ertekin, A. (2021). Brain White Matter Hyperintensity Changes Associated with Vascular Cognitive Impairment and Dementia, Alzheimer’s Dementia and Normal Aging. Duzce Medical Journal, 23(3), 305-312. https://doi.org/10.18678/dtfd.1012133
AMA Ertekin A. Brain White Matter Hyperintensity Changes Associated with Vascular Cognitive Impairment and Dementia, Alzheimer’s Dementia and Normal Aging. Duzce Med J. December 2021;23(3):305-312. doi:10.18678/dtfd.1012133
Chicago Ertekin, Ayfer. “Brain White Matter Hyperintensity Changes Associated With Vascular Cognitive Impairment and Dementia, Alzheimer’s Dementia and Normal Aging”. Duzce Medical Journal 23, no. 3 (December 2021): 305-12. https://doi.org/10.18678/dtfd.1012133.
EndNote Ertekin A (December 1, 2021) Brain White Matter Hyperintensity Changes Associated with Vascular Cognitive Impairment and Dementia, Alzheimer’s Dementia and Normal Aging. Duzce Medical Journal 23 3 305–312.
IEEE A. Ertekin, “Brain White Matter Hyperintensity Changes Associated with Vascular Cognitive Impairment and Dementia, Alzheimer’s Dementia and Normal Aging”, Duzce Med J, vol. 23, no. 3, pp. 305–312, 2021, doi: 10.18678/dtfd.1012133.
ISNAD Ertekin, Ayfer. “Brain White Matter Hyperintensity Changes Associated With Vascular Cognitive Impairment and Dementia, Alzheimer’s Dementia and Normal Aging”. Duzce Medical Journal 23/3 (December 2021), 305-312. https://doi.org/10.18678/dtfd.1012133.
JAMA Ertekin A. Brain White Matter Hyperintensity Changes Associated with Vascular Cognitive Impairment and Dementia, Alzheimer’s Dementia and Normal Aging. Duzce Med J. 2021;23:305–312.
MLA Ertekin, Ayfer. “Brain White Matter Hyperintensity Changes Associated With Vascular Cognitive Impairment and Dementia, Alzheimer’s Dementia and Normal Aging”. Duzce Medical Journal, vol. 23, no. 3, 2021, pp. 305-12, doi:10.18678/dtfd.1012133.
Vancouver Ertekin A. Brain White Matter Hyperintensity Changes Associated with Vascular Cognitive Impairment and Dementia, Alzheimer’s Dementia and Normal Aging. Duzce Med J. 2021;23(3):305-12.