PET imaging for the evaluation of cerebral amyloid angiopathy: a systematic review

Francesco Dondi1, Mattia Bertoli2, Silvia Lucchini2, Elisabetta Cerudelli2, Domenico Albano1, Francesco Bertagna1
1Nuclear Medicine, University of Brescia and ASST Spedali Civili Brescia, Brescia, Italy
2Nuclear Medicine, ASST Spedali Civili Brescia, Brescia, Italy

Tóm tắt

In the last years, the role of PET imaging in the assessment of cerebral amyloid angiopathy (CAA) is emerging. In this setting, some tracers have proven their utility for the evaluation of the disease (mainly 11C-Pittsburgh compound B [11C-PIB]), however, the value of other radiotracers has to be clarified. The aim of this systematic review is, therefore, to assess the role of PET imaging in the evaluation of CAA. A wide literature search of the PubMed/MEDLINE, Scopus, Embase, Web of Science and Cochrane library databases was made to find relevant published articles about the diagnostic performance of PET imaging for the evaluation of CAA. Quality assessment including the risk of bias and applicability concerns was carried out using QUADAS-2 evaluation. The comprehensive computer literature search revealed 651 articles. On reviewing the titles and abstracts, 622 articles were excluded because the reported data were not within the field of interest. Twenty-nine studies were included in the review. In general, PET imaging with amyloid tracers revealed its value for the assessment of CAA, for its differential diagnosis and a correlation with some clinico-pathological features. With less evidence, a role for 18F-fluorodeoxiglucose (18F-FDG) and tau tracers is starting to emerge. PET imaging demonstrated its utility for the assessment of CAA. In particular, amiloid tracers revealed higher retention in CAA patients, correlation with cerebral bleed, the ability to differentiate between CAA and other related conditions (such as Alzheimer's disease) and a correlation with some cerebrospinal fluid biomarkers.

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Chen SJ, Tsai HH, Tsai LK, Tang SC, Lee BC, Liu HM, Yen RF, Jeng JS (2019) Advances in cerebral amyloid angiopathy imaging. Ther Adv Neurol Disord 3(12):1756286419844113 Charidimou A, Boulouis G, Gurol ME et al (2017) Emerging concepts in sporadic cerebral amyloid angiopathy. Brain 140:1829–1850 Yamada M, Tsukagoshi H, Otomo E et al (1987) Cerebral amyloid angiopathy in the aged. J Neurol 234:371–376 Yamada M (2015) Cerebral amyloid angiopathy: emerging concepts. J Stroke 17:17–30 Charidimou A, Farid K, Tsai HH, Tsai LK, Yen RF, Baron JC (2018) Amyloid-PET burden and regional distribution in cerebral amyloid angiopathy: a systematic review and meta-analysis of biomarker performance. J Neurol Neurosurg Psychiatry 89(4):410–417 Viswanathan A, Greenberg SM (2011) Cerebral amyloid angiopathy in the elderly. Ann Neurol 70:871–880 Charidimou A, Gang Q, Werring DJ (2012) Sporadic cerebral amyloid angiopathy revisited: recent insights into pathophysiology and clinical spectrum. J Neurol Neurosurg Psychiatry 83:124–137 Linn J, Halpin A, Demaerel P et al (2010) Prevalence of superficial siderosis in patients with cerebral amyloid angiopathy. Neurology 74:1346–1350 Rosand J, Muzikansky A, Kumar A, Wisco JJ, Smith EE, Betensky RA et al (2005) Spatial clustering of hemorrhages in probable cerebral amyloid angiopathy. Ann Neurol 58:459–462 Knudsen KA, Rosand J, Karluk D et al (2001) Clinical diagnosis of cerebral amyloid angiopathy: validation of the Boston criteria. Neurology 56:537–539 Martinez-Ramirez S, Romero JR, Shoamanesh A et al (2015) Diagnostic value of lobar microbleeds in individuals without intracerebral hemorrhage. Alzheimers Dement 11:1480–1488 Farid K, Charidimou A, Baron JC (2017) Amyloid positron emission tomography in sporadic cerebral amyloid angiopathy: a systematic critical update. Neuroimage Clin 5(15):247–263 Knudsen KA, Rosand J, Karluk D, Greenberg SM (2001) Clinical diagnosis of cerebral amyloid angiopathy: validation of the Boston criteria. Neurology 56:537–539 Linn J, Halpin A, Demaerel P, Ruhland J, Giese AD, Dichgans M, van Buchem MA, Bruckmann H, Greenberg SM (2010) Prevalence of superficial siderosis in patients with cerebral amyloid angiopathy. Neurology 74:1346–1350 Farid K, Charidimou A, Baron JC (2017) Amyloid positron emission tomography in sporadic cerebral amyloid angiopathy: a systematic critical update. Neuroimage Clin 15:247–263 Whiting PF, Rutjes AWS, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, Leeflang MMG, Sterne JAC, Bossuyt PMM, QUADAS-2 Group (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155:529–536 Dierksen GA, Skehan ME, Khan MA, Jeng J, Nandigam RN, Becker JA, Kumar A, Neal KL, Betensky RA, Frosch MP, Rosand J, Johnson KA, Viswanathan A, Salat DH, Greenberg SM (2010) Spatial relation between microbleeds and amyloid deposits in amyloid angiopathy. Ann Neurol 68(4):545–548 Ly JV, Donnan GA, Villemagne VL, Zavala JA, Ma H, O’Keefe G, Gong SJ, Gunawan RM, Saunder T, Ackerman U, Tochon-Danguy H, Churilov L, Phan TG, Rowe CC (2010) 11C-PIB binding is increased in patients with cerebral amyloid angiopathy-related hemorrhage. Neurology 74(6):487–493 Gurol ME, Dierksen G, Betensky R, Gidicsin C, Halpin A, Becker A, Carmasin J, Ayres A, Schwab K, Viswanathan A, Salat D, Rosand J, Johnson KA, Greenberg SM (2012) Predicting sites of new hemorrhage with amyloid imaging in cerebral amyloid angiopathy. Neurology 79(4):320–326 Gurol ME, Viswanathan A, Gidicsin C, Hedden T, Martinez-Ramirez S, Dumas A, Vashkevich A, Ayres AM, Auriel E, van Etten E, Becker A, Carmasin J, Schwab K, Rosand J, Johnson KA, Greenberg SM (2013) Cerebral amyloid angiopathy burden associated with leukoaraiosis: a positron emission tomography/magnetic resonance imaging study. Ann Neurol 73(4):529–536 Baron JC, Farid K, Dolan E, Turc G, Marrapu ST, O’Brien E, Aigbirhio FI, Fryer TD, Menon DK, Warburton EA, Hong YT (2014) Diagnostic utility of amyloid PET in cerebral amyloid angiopathy-related symptomatic intracerebral hemorrhage. J Cereb Blood Flow Metab 34(5):753–758 Farid K, Hong YT, Aigbirhio FI, Fryer TD, Menon DK, Warburton EA, Baron JC (2015) Early-phase 11C-PiB PET in amyloid angiopathy-related symptomatic cerebral hemorrhage: potential diagnostic value? PLoS ONE 10(10):e0139926 Samuraki M, Matsunari I, Yoshita M, Shima K, Noguchi-Shinohara M, Hamaguchi T, Ono K, Yamada M (2015) Cerebral amyloid angiopathy-related microbleeds correlate with glucose metabolism and brain volume in Alzheimer’s disease. J Alzheimers Dis 48(2):517–528 Gurol ME, Becker JA, Fotiadis P, Riley G, Schwab K, Johnson KA, Greenberg SM (2016) Florbetapir-PET to diagnose cerebral amyloid angiopathy: a prospective study. Neurology 87(19):2043–2049 Raposo N, Planton M, Péran P, Payoux P, Bonneville F, Lyoubi A, Albucher JF, Acket B, Salabert AS, Olivot JM, Hitzel A, Chollet F, Pariente J (2017) Florbetapir imaging in cerebral amyloid angiopathy-related hemorrhages. Neurology 89(7):697–704 Renard D, Tatu L, Collombier L, Wacongne A, Ayrignac X, Charif M, Boukriche Y, Chiper L, Fourcade G, Azakri S, Gaillard N, Mercier E, Lehmann S, Thouvenot E (2018) Cerebral amyloid angiopathy and cerebral amyloid angiopathy-related inflammation: comparison of hemorrhagic and DWI MRI features. J Alzheimers Dis 64(4):1113–1121 Renard D, Collombier L, Demattei C, Wacongne A, Charif M, Ayrignac X, Azakri S, Gaillard N, Boudousq V, Lehmann S, Menjot de Champfleur N, Thouvenot E (2018) Cerebrospinal fluid, MRI, and florbetaben-PET in cerebral amyloid angiopathy-related inflammation. J Alzheimers Dis 61(3):1107–1117 Tsai HH, Pasi M, Tsai LK, Chen YF, Lee BC, Tang SC, Fotiadis P, Huang CY, Yen RF, Gurol ME, Jeng JS (2018) Distribution of lacunar infarcts in asians with intracerebral hemorrhage: a magnetic resonance imaging and amyloid positron emission tomography study. Stroke 49(6):1515–1517 Jang H, Jang YK, Kim HJ, Werring DJ, Lee JS, Choe YS, Park S, Lee J, Kim KW, Kim Y, Cho SH, Kim SE, Kim SJ, Charidimou A, Na DL, Seo SW (2019) Clinical significance of amyloid β positivity in patients with probable cerebral amyloid angiopathy markers. Eur J Nucl Med Mol Imaging 46(6):1287–1298 Raposo N, Planton M, Payoux P, Péran P, Albucher JF, Calviere L, Viguier A, Rousseau V, Hitzel A, Chollet F, Olivot JM, Bonneville F, Pariente J (2019) Enlarged perivascular spaces and florbetapir uptake in patients with intracerebral hemorrhage. Eur J Nucl Med Mol Imaging 46(11):2339–2347 Schultz AP, Kloet RW, Sohrabi HR, van der Weerd L, van Rooden S, Wermer MJH, Moursel LG, Yaqub M, van Berckel BNM, Chatterjee P, Gardener SL, Taddei K, Fagan AM, Benzinger TL, Morris JC, Sperling R, Johnson K, Bateman RJ, Dominantly Inherited Alzheimer Network, Gurol ME, van Buchem MA, Martins R, Chhatwal JP, Greenberg SM (2019) Amyloid imaging of Dutch-type hereditary cerebral amyloid angiopathy carriers. Ann Neurol 86(4):616–625 Tsai HH, Pasi M, Tsai LK, Chen YF, Lee BC, Tang SC, Fotiadis P, Huang CY, Yen RF, Jeng JS, Gurol ME (2019) Microangiopathy underlying mixed-location intracerebral hemorrhages/microbleeds: a PiB-PET study. Neurology 92(8):e774–e781 Banerjee G, Ambler G, Keshavan A, Paterson RW, Foiani MS, Toombs J, Heslegrave A, Dickson JC, Fraioli F, Groves AM, Lunn MP, Fox NC, Zetterberg H, Schott JM, Werring DJ (2020) Cerebrospinal fluid biomarkers in cerebral amyloid angiopathy. J Alzheimers Dis 74(4):1189–1201 Jung YH, Jang H, Park SB, Choe YS, Park Y, Kang SH, Lee JM, Kim JS, Kim J, Kim JP, Kim HJ, Na DL, Seo SW (2020) Strictly lobar microbleeds reflect amyloid angiopathy regardless of cerebral and cerebellar compartments. Stroke 51(12):3600–3607 Planton M, Saint-Aubert L, Raposo N, Payoux P, Salabert AS, Albucher JF, Olivot JM, Péran P, Pariente J (2020) Florbetapir regional distribution in cerebral amyloid angiopathy and Alzheimer’s disease: a PET study. J Alzheimers Dis 73(4):1607–1614 Planton M, Pariente J, Nemmi F, Albucher JF, Calviere L, Viguier A, Olivot JM, Salabert AS, Payoux P, Peran P, Raposo N (2020) Interhemispheric distribution of amyloid and small vessel disease burden in cerebral amyloid angiopathy-related intracerebral hemorrhage. Eur J Neurol 27(8):1664–1671 Tsai HH, Pasi M, Tsai LK, Chen YF, Chen YW, Tang SC, Gurol ME, Yen RF, Jeng JS (2020) Superficial cerebellar microbleeds and cerebral amyloid angiopathy: a magnetic resonance imaging/positron emission tomography study. Stroke 51(1):202–208 Papanastasiou G, Rodrigues MA, Wang C, Heurling K, Lucatelli C, Al-Shahi Salman R, Wardlaw JM, van Beek EJR, Thompson G (2021) Pharmacokinetic modelling for the simultaneous assessment of perfusion and 18F-flutemetamol uptake in cerebral amyloid angiopathy using a reduced PET-MR acquisition time: proof of concept. Neuroimage 15(225):117482 Bergeret S, Queneau M, Rodallec M, Curis E, Dumurgier J, Hugon J, Paquet C, Farid K, Baron JC (2021) [18 F]FDG PET may differentiate cerebral amyloid angiopathy from Alzheimer’s disease. Eur J Neurol 28(5):1511–1519 Bergeret S, Queneau M, Rodallec M, Landeau B, Chetelat G, Hong YT, Dumurgier J, Hugon J, Paquet C, Farid K, Baron JC (2021) Brain glucose metabolism in cerebral amyloid angiopathy: an FDG-PET study. Stroke 52(4):1478–1482 Chang Y, Liu J, Wang L, Li X, Wang Z, Lin M, Jin W, Zhu M, Xu B (2021) Diagnostic utility of integrated11C-pittsburgh compound B positron emission tomography/magnetic resonance for cerebral amyloid angiopathy: a pilot study. Front Aging Neurosci 25(13):721780 Tsai HH, Pasi M, Tsai LK, Huang CC, Chen YF, Lee BC, Yen RF, Gurol ME, Jeng JS (2021) Centrum semiovale perivascular space and amyloid deposition in spontaneous intracerebral hemorrhage. Stroke 52(7):2356–2362 Tsai HH, Chen YF, Yen RF, Lo YL, Yang KC, Jeng JS, Tsai LK, Chang CF (2021) Plasma soluble TREM2 is associated with white matter lesions independent of amyloid and tau. Brain 144(11):3371–3380 Schoemaker D, Charidimou A, ZanonZotin MC, Raposo N, Johnson KA, Sanchez JS, Greenberg SM, Viswanathan A (2021) Association of memory impairment with concomitant tau pathology in patients with cerebral amyloid angiopathy. Neurology 96(15):e1975–e1986 Gokcal E, Horn MJ, Becker JA, Das AS, Schwab K, Biffi A, Rost N, Rosand J, Viswanathan A, Polimeni JR, Johnson KA, Greenberg SM, Gurol ME (2022) Effect of vascular amyloid on white matter disease is mediated by vascular dysfunction in cerebral amyloid angiopathy. J Cereb Blood Flow Metab 28:271678X221076571