Using radiomics-based modelling to predict individual progression from mild cognitive impairment to Alzheimer's disease.


Journal

European journal of nuclear medicine and molecular imaging
ISSN: 1619-7089
Titre abrégé: Eur J Nucl Med Mol Imaging
Pays: Germany
ID NLM: 101140988

Informations de publication

Date de publication:
06 2022
Historique:
received: 02 08 2021
accepted: 11 01 2022
pubmed: 16 1 2022
medline: 26 5 2022
entrez: 15 1 2022
Statut: ppublish

Résumé

Predicting the risk of disease progression from mild cognitive impairment (MCI) to Alzheimer's disease (AD) has important clinical significance. This study aimed to provide a personalized MCI-to-AD conversion prediction via radiomics-based predictive modelling (RPM) with multicenter 18F-fluorodeoxyglucose positron emission tomography (FDG PET) data. FDG PET and neuropsychological data of 884 subjects were collected from Huashan Hospital, Xuanwu Hospital, and from the Alzheimer's Disease Neuroimaging Initiative (ADNI) database. First, 34,400 radiomic features were extracted from the 80 regions of interest (ROIs) for all PET images. These features were then concatenated for feature selection, and an RPM model was constructed and validated on the ADNI dataset. In addition, we used clinical data and the routine semiquantification index (standard uptake value ratio, SUVR) to establish clinical and SUVR Cox models for further comparison. FDG images from local hospitals were used to explore RPM performance in a separate cohort of individuals with healthy controls and different cognitive levels (a complete AD continuum). Finally, correlation analysis was conducted between the radiomic biomarkers and neuropsychological assessments. The experimental results showed that the predictive performance of the RPM Cox model was better than that of other Cox models. In the validation dataset, Harrell's consistency coefficient of the RPM model was 0.703 ± 0.002, while those of the clinical and SUVR models were 0.632 ± 0.006 and 0.683 ± 0.009, respectively. Moreover, most crucial imaging biomarkers were significantly different at different cognitive stages and significantly correlated with cognitive disease severity. The preliminary results demonstrated that the developed RPM approach has the potential to monitor progression in high-risk populations with AD.

Sections du résumé

BACKGROUND
Predicting the risk of disease progression from mild cognitive impairment (MCI) to Alzheimer's disease (AD) has important clinical significance. This study aimed to provide a personalized MCI-to-AD conversion prediction via radiomics-based predictive modelling (RPM) with multicenter 18F-fluorodeoxyglucose positron emission tomography (FDG PET) data.
METHOD
FDG PET and neuropsychological data of 884 subjects were collected from Huashan Hospital, Xuanwu Hospital, and from the Alzheimer's Disease Neuroimaging Initiative (ADNI) database. First, 34,400 radiomic features were extracted from the 80 regions of interest (ROIs) for all PET images. These features were then concatenated for feature selection, and an RPM model was constructed and validated on the ADNI dataset. In addition, we used clinical data and the routine semiquantification index (standard uptake value ratio, SUVR) to establish clinical and SUVR Cox models for further comparison. FDG images from local hospitals were used to explore RPM performance in a separate cohort of individuals with healthy controls and different cognitive levels (a complete AD continuum). Finally, correlation analysis was conducted between the radiomic biomarkers and neuropsychological assessments.
RESULTS
The experimental results showed that the predictive performance of the RPM Cox model was better than that of other Cox models. In the validation dataset, Harrell's consistency coefficient of the RPM model was 0.703 ± 0.002, while those of the clinical and SUVR models were 0.632 ± 0.006 and 0.683 ± 0.009, respectively. Moreover, most crucial imaging biomarkers were significantly different at different cognitive stages and significantly correlated with cognitive disease severity.
CONCLUSION
The preliminary results demonstrated that the developed RPM approach has the potential to monitor progression in high-risk populations with AD.

Identifiants

pubmed: 35032179
doi: 10.1007/s00259-022-05687-y
pii: 10.1007/s00259-022-05687-y
doi:

Substances chimiques

Biomarkers 0
Fluorodeoxyglucose F18 0Z5B2CJX4D

Types de publication

Journal Article Multicenter Study

Langues

eng

Sous-ensembles de citation

IM

Pagination

2163-2173

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

2020 Alzheimer’s disease facts and figures. Alzheimers Dement. 2020. https://doi.org/10.1002/alz.12068 .
Scheltens P, Blennow K, Breteler MM, de Strooper B, Frisoni GB, Salloway S, et al. Alzheimer’s disease. Lancet. 2016;388(10043):505–17. https://doi.org/10.1016/S0140-6736(15)01124-1 .
doi: 10.1016/S0140-6736(15)01124-1 pubmed: 26921134
Jack CR Jr, Wiste HJ, Weigand SD, Therneau TM, Lowe VJ, Knopman DS, et al. Defining imaging biomarker cut points for brain aging and Alzheimer’s disease. Alzheimers Dement. 2017;13(3):205–16. https://doi.org/10.1016/j.jalz.2016.08.005 .
doi: 10.1016/j.jalz.2016.08.005 pubmed: 27697430
Long JM, Holtzman DM. Alzheimer disease: an update on pathobiology and treatment strategies. Cell. 2019;179(2):312–39. https://doi.org/10.1016/j.cell.2019.09.001 .
doi: 10.1016/j.cell.2019.09.001 pubmed: 31564456 pmcid: 6778042
Jack CR Jr, Bennett DA, Blennow K, Carrillo MC, Dunn B, Haeberlein SB, et al. NIA-AA Research framework: toward a biological definition of Alzheimer’s disease. Alzheimers Dement. 2018;14(4):535–62. https://doi.org/10.1016/j.jalz.2018.02.018 .
doi: 10.1016/j.jalz.2018.02.018 pubmed: 29653606 pmcid: 5958625
Mitchell AJ, Shiri-Feshki M. Rate of progression of mild cognitive impairment to dementia—meta-analysis of 41 robust inception cohort studies. Acta Psychiatr Scand. 2009;119(4):252–65. https://doi.org/10.1111/j.1600-0447.2008.01326.x .
doi: 10.1111/j.1600-0447.2008.01326.x pubmed: 19236314
Farias ST, Mungas D, Reed BR, Harvey D, DeCarli C. Progression of mild cognitive impairment to dementia in clinic- vs community-based cohorts. Arch Neurol. 2009;66(9):1151–7. https://doi.org/10.1001/archneurol.2009.106 .
doi: 10.1001/archneurol.2009.106 pubmed: 19752306 pmcid: 2863139
Schneider JA, Arvanitakis Z, Leurgans SE, Bennett DA. The neuropathology of probable Alzheimer disease and mild cognitive impairment. Ann Neurol. 2009;66(2):200–8.
doi: 10.1002/ana.21706
Petersen RC, Roberts RO, Knopman DS, Boeve BF, Geda YE, Ivnik RJ, et al. Mild cognitive impairment ten years later. Arch Neurol-Chicago. 2009;66(12):1447–55.
doi: 10.1001/archneurol.2009.266
Dubois B, Hampel H, Feldman HH, Scheltens P, Aisen P, Andrieu S, et al. Preclinical Alzheimer’s disease: definition, natural history, and diagnostic criteria. Alzheimers Dement. 2016;12(3):292–323. https://doi.org/10.1016/j.jalz.2016.02.002 .
doi: 10.1016/j.jalz.2016.02.002 pubmed: 27012484 pmcid: 6417794
Farrell ME, Jiang S, Schultz AP, Properzi MJ, Price JC, Becker JA, et al. Defining the lowest threshold for amyloid-PET to predict future cognitive decline and amyloid accumulation. Neurology. 2021;96(4):e619–31. https://doi.org/10.1212/wnl.0000000000011214 .
doi: 10.1212/wnl.0000000000011214 pubmed: 33199430 pmcid: 7905788
Salvadó G, Molinuevo JL, Brugulat-Serrat A, Falcon C, Grau-Rivera O, Suárez-Calvet M, et al. Centiloid cut-off values for optimal agreement between PET and CSF core AD biomarkers. Alzheimer's Res Ther. 2019;11(1):27. https://doi.org/10.1186/s13195-019-0478-z .
doi: 10.1186/s13195-019-0478-z
Fakhry-Darian D, Patel NH, Khan S, Barwick T, Svensson W, Khan S, et al. Optimisation and usefulness of quantitative analysis of (18)F-florbetapir PET. Br J Radiol. 2019;92(1101):20181020. https://doi.org/10.1259/bjr.20181020 .
doi: 10.1259/bjr.20181020 pubmed: 31017465 pmcid: 6732916
Kreisl WC, Kim M-J, Coughlin JM, Henter ID, Owen DR, Innis RB. PET imaging of neuroinflammation in neurological disorders. The Lancet Neurology. 2020;19(11):940–50. https://doi.org/10.1016/s1474-4422(20)30346-x .
doi: 10.1016/s1474-4422(20)30346-x pubmed: 33098803 pmcid: 7912433
Blazhenets G, Ma Y, Sörensen A, Rücker G, Schiller F, Eidelberg D, et al. Principal components analysis of brain metabolism predicts development of Alzheimer dementia. J Nucl Med. 2019;60(6):837–43. https://doi.org/10.2967/jnumed.118.219097 .
doi: 10.2967/jnumed.118.219097 pubmed: 30389825
Shen T, Jiang J, Lu J, Wang M, Zuo C, Yu Z, et al. Predicting Alzheimer disease from mild cognitive impairment with a deep belief network based on 18F-FDG-PET images. Mol Imaging. 2019;18:1536012119877285. https://doi.org/10.1177/1536012119877285 .
doi: 10.1177/1536012119877285 pubmed: 31552787 pmcid: 6764042
Wang M, Jiang J, Yan Z, Alberts I, Ge J, Zhang H, et al. Individual brain metabolic connectome indicator based on Kullback-Leibler Divergence Similarity Estimation predicts progression from mild cognitive impairment to Alzheimer’s dementia. Eur J Nucl Med Mol Imaging. 2020;47(12):2753–64. https://doi.org/10.1007/s00259-020-04814-x .
doi: 10.1007/s00259-020-04814-x pubmed: 32318784 pmcid: 7567735
Landau SM, Harvey D, Madison CM, Koeppe RA, Reiman EM, Foster NL, et al. Associations between cognitive, functional, and FDG-PET measures of decline in AD and MCI. Neurobiol Aging. 2011;32(7):1207–18. https://doi.org/10.1016/j.neurobiolaging.2009.07.002 .
doi: 10.1016/j.neurobiolaging.2009.07.002 pubmed: 19660834
Cabral C, Morgado PM, Costa DC, Silveira M, Initi AsDN. Predicting conversion from MCI to AD with FDG-PET brain images at different prodromal stages. Comput Biol Med. 2015;58:101-9. https://doi.org/10.1016/j.compbiomed.2015.01.003
Pagani M, Giuliani A, Öberg J, De Carli F, Morbelli S, Girtler N, et al. Progressive disintegration of brain networking from normal aging to Alzheimer disease: analysis of independent components of (18)F-FDG PET data. J Nucl Med. 2017;58(7):1132–9. https://doi.org/10.2967/jnumed.116.184309 .
doi: 10.2967/jnumed.116.184309 pubmed: 28280223
Rizzo S, Botta F, Raimondi S, Origgi D, Fanciullo C, Morganti AG, et al. Radiomics: the facts and the challenges of image analysis. Eur Radiol Exp. 2018;2(1):1–8.
doi: 10.1186/s41747-018-0068-z
Lambin P, Leijenaar RT, Deist TM, Peerlings J, De Jong EE, Van Timmeren J, et al. Radiomics: the bridge between medical imaging and personalized medicine. Nat Rev Clin Oncol. 2017;14(12):749.
doi: 10.1038/nrclinonc.2017.141
Hu X, Sun X, Hu F, Liu F, Ruan W, Wu T, et al. Multivariate radiomics models based on (18)F-FDG hybrid PET/MRI for distinguishing between Parkinson’s disease and multiple system atrophy. Eur J Nucl Med Mol Imaging. 2021;48(11):3469–81. https://doi.org/10.1007/s00259-021-05325-z .
doi: 10.1007/s00259-021-05325-z pubmed: 33829415
Wu Y, Jiang JH, Chen L, Lu JY, Ge JJ, Liu FT, et al. Use of radiomic features and support vector machine to distinguish Parkinson’s disease cases from normal controls. Ann Transl Med. 2019;7(23):773. https://doi.org/10.21037/atm.2019.11.26 .
doi: 10.21037/atm.2019.11.26 pubmed: 32042789 pmcid: 6990013
Zhou H, Jiang J, Lu J, Wang M, Zhang H, Zuo C. Dual-model radiomic biomarkers predict development of mild cognitive impairment progression to Alzheimer’s disease. Front Neurosci. 2018;12:1045. https://doi.org/10.3389/fnins.2018.01045 .
doi: 10.3389/fnins.2018.01045 pubmed: 30686995
Li TR, Wu Y, Jiang JJ, Lin H, Han CL, Jiang JH, et al. Radiomics analysis of magnetic resonance imaging facilitates the identification of preclinical Alzheimer’s disease: an exploratory study. Front Cell Dev Biol. 2020;8: 605734. https://doi.org/10.3389/fcell.2020.605734 .
doi: 10.3389/fcell.2020.605734 pubmed: 33344457 pmcid: 7744815
Li X, Wang X, Su L, Hu X, Han Y. Sino Longitudinal Study on Cognitive Decline (SILCODE): protocol for a Chinese longitudinal observational study to develop risk prediction models of conversion to mild cognitive impairment in individuals with subjective cognitive decline. BMJ Open. 2019;9(7): e028188. https://doi.org/10.1136/bmjopen-2018-028188 .
doi: 10.1136/bmjopen-2018-028188 pubmed: 31350244 pmcid: 6661672
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. https://doi.org/10.1016/j.jalz.2011.03.005 .
doi: 10.1016/j.jalz.2011.03.005 pubmed: 21514250 pmcid: 3312024
Jessen F, Amariglio RE, Van Boxtel M, Breteler M, Ceccaldi M, Chételat G, et al. A conceptual framework for research on subjective cognitive decline in preclinical Alzheimer’s disease. Alzheimers Dement. 2014;10(6):844–52.
doi: 10.1016/j.jalz.2014.01.001
Bondi MW, Edmonds EC, Jak AJ, Clark LR, Delano-Wood L, McDonald CR, et al. Neuropsychological criteria for mild cognitive impairment improves diagnostic precision, biomarker associations, and progression rates. J Alzheimer's Dis: JAD. 2014;42(1):275–89. https://doi.org/10.3233/jad-140276 .
doi: 10.3233/jad-140276
Landau SM, Mintun MA, Joshi AD, Koeppe RA, Petersen RC, Aisen PS, et al. Amyloid deposition, hypometabolism, and longitudinal cognitive decline. Ann Neurol. 2012;72(4):578–86. https://doi.org/10.1002/ana.23650 .
doi: 10.1002/ana.23650 pubmed: 23109153 pmcid: 3786871
Ge J, Wang M, Lin W, Wu P, Guan Y, Zhang H, et al. Metabolic network as an objective biomarker in monitoring deep brain stimulation for Parkinson’s disease: a longitudinal study. EJNMMI Res. 2020;10(1):131. https://doi.org/10.1186/s13550-020-00722-1 .
doi: 10.1186/s13550-020-00722-1 pubmed: 33119814 pmcid: 7596139
Woo CW, Chang LJ, Lindquist MA, Wager TD. Building better biomarkers: brain models in translational neuroimaging. Nat Neurosci. 2017;20(3):365–77. https://doi.org/10.1038/nn.4478 .
doi: 10.1038/nn.4478 pubmed: 28230847 pmcid: 5988350
Simon N, Friedman J, Hastie T, Tibshirani R. Regularization paths for Cox’s proportional hazards model via coordinate descent. J Stat Softw. 2011;39(5):1.
doi: 10.18637/jss.v039.i05
Friedman J, Hastie T, Tibshirani R. Regularization paths for generalized linear models via coordinate descent. J Stat Softw. 2010;33(1):1.
doi: 10.18637/jss.v033.i01
Therneau TM, Grambsch PM. Modeling survival data: extending the Cox model. Springer Science & Business Media; 2013.
Huang K, Lin Y, Yang L, Wang Y, Cai S, Pang L, et al. A multipredictor model to predict the conversion of mild cognitive impairment to Alzheimer’s disease by using a predictive nomogram. Neuropsychopharmacology. 2020;45(2):358–66. https://doi.org/10.1038/s41386-019-0551-0 .
doi: 10.1038/s41386-019-0551-0 pubmed: 31634898
Kato T, Inui Y, Nakamura A, Ito K. Brain fluorodeoxyglucose (FDG) PET in dementia. Ageing Res Rev. 2016;30:73–84. https://doi.org/10.1016/j.arr.2016.02.003 .
doi: 10.1016/j.arr.2016.02.003 pubmed: 26876244
Pini L, Pievani M, Bocchetta M, Altomare D, Bosco P, Cavedo E, et al. Brain atrophy in Alzheimer’s disease and aging. Ageing Res Rev. 2016;30:25–48. https://doi.org/10.1016/j.arr.2016.01.002 .
doi: 10.1016/j.arr.2016.01.002 pubmed: 26827786
Risacher SL, Saykin AJ. Neuroimaging in aging and neurologic diseases. Handb Clin Neurol. 2019;167:191–227. https://doi.org/10.1016/b978-0-12-804766-8.00012-1 .
doi: 10.1016/b978-0-12-804766-8.00012-1 pubmed: 31753134 pmcid: 9006168
Wang X, Song G, Jiang H, Zheng L, Pang P, Xu J. Can texture analysis based on single unenhanced CT accurately predict the WHO/ISUP grading of localized clear cell renal cell carcinoma? Abdom Radiol (NY). 2021;46(9):4289–300. https://doi.org/10.1007/s00261-021-03090-z .
doi: 10.1007/s00261-021-03090-z

Auteurs

Jiehui Jiang (J)

Institute of Biomedical Engineering, School of Life Science, Shanghai University, Shanghai, China. jiangjiehui@shu.edu.cn.

Min Wang (M)

Institute of Biomedical Engineering, School of Life Science, Shanghai University, Shanghai, China.

Ian Alberts (I)

Department of Nuclear Medicine, University Hospital Bern, Bern, Switzerland.

Xiaoming Sun (X)

Institute of Biomedical Engineering, School of Life Science, Shanghai University, Shanghai, China.

Taoran Li (T)

Department of Neurology, Xuanwu Hospital of Capital Medical University, Beijing, China.

Axel Rominger (A)

Department of Nuclear Medicine, University Hospital Bern, Bern, Switzerland.

Chuantao Zuo (C)

PET Center, Huashan Hospital, Fudan University, Shanghai, China. zuochuantao@fudan.edu.cn.
Human Phenome Institute, Fudan University, Shanghai, China. zuochuantao@fudan.edu.cn.

Ying Han (Y)

Department of Neurology, Xuanwu Hospital of Capital Medical University, Beijing, China. hanying@xwh.ccmu.edu.cn.
Center of Alzheimer's Disease, Beijing Institute for Brain Disorders, Beijing, China. hanying@xwh.ccmu.edu.cn.
School of Biomedical Engineering, Hainan University, Haikou, China. hanying@xwh.ccmu.edu.cn.
National Clinical Research Center for Geriatric Disorders, Beijing, China. hanying@xwh.ccmu.edu.cn.

Kuangyu Shi (K)

Department of Nuclear Medicine, University Hospital Bern, Bern, Switzerland.
Department of Informatics, Technische Universität München, Munich, Germany.

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