Translation of Pre-Clinical Studies into Successful Clinical Trials for Alzheimer’s Disease: What are the Roadblocks and How Can They Be Overcome?
Open accessAbstract
Preclinical studies are essential for translation to disease treatments and effective use in clinical practice. An undue emphasis on single approaches to Alzheimer’s disease (AD) appears to have retarded the pace of translation in the field, and there is much frustration in the public about the lack of an effective treatment. We critically reviewed past literature (1990–2014), analyzed numerous data, and discussed key issues at a consensus conference on Brain Ageing and Dementia to identify and overcome roadblocks in studies intended for translation. We highlight various factors that influence the translation of preclinical research and highlight specific preclinical strategies that have failed to demonstrate efficacy in clinical trials. The field has been hindered by the domination of the amyloid hypothesis in AD pathogenesis while the causative pathways in disease pathology are widely considered to be multifactorial. Understanding the causative events and mechanisms in the pathogenesis are equally important for translation. Greater efforts are necessary to fill in the gaps and overcome a variety of confounds in the generation, study design, testing, and evaluation of animal models and the application to future novel anti-dementia drug trials. A greater variety of potential disease mechanisms must be entertained to enhance progress.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Many AD clinical trials that failed were successful in preclinical testing using animal models.
“the very high failure rate of clinical trials of AD therapeutics (of ~99.6%), many of which were successful in preclinical testing using these animal models [6, 27, 139]”
From Alzheimer's disease: experimental models and reality (2017) · cites this paper as [6]
The lack of additional AD-associated pathology could at least partly account for the lack of translation between preclinical and clinical trials.
“This lack of additional AD associated pathology could at least partly account for the lack of translation between preclinical and clinical trials [6], although there have also been a few clinical trial failures for approaches not initially tested in transgenic models[69].”
From Alzheimer's disease: experimental models and reality (2017) · cites this paper as [6]
The failure rate of clinical trials of AD therapeutics is approximately 99.6%.
“the very high failure rate of clinical trials of AD therapeutics (of ~99.6%), many of which were successful in preclinical testing using these animal models [6, 27, 139]”
From Alzheimer's disease: experimental models and reality (2017) · cites this paper as [6]
The very poor success rate of ~99.6% with AD targeting clinical trials can in part be explained by the premature translation of successful pathology reduction in transgenic mice to humans.
“The very poor success rate of ~99.6% with AD targeting clinical trials can in part be explained by the premature translation of successful pathology reduction in transgenic mice to humans [6, 27, 139].”
From Alzheimer's disease: experimental models and reality (2017) · cites this paper as [6]
Cites
1 retracted
Retracted: ‘Clinical trials in Alzheimer’s disease’: immunotherapy approaches
Delrieu, J., Ousset, P., Caillaud, C., & Vellas, B. J. (2011) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07458.x · Cited by 140 · see citing works
RetractedMcKhann, G. M., Knopman, D. S., Chertkow, H., Hyman, B. T., Jack, C. R., Kawas, C. H., Klunk, W. E., Koroshetz, W. J., Manly, J. J., Mayeux, R., et al. (2011) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2011.03.005 · Cited by 18,657 · see citing works
Finding the missing heritability of complex diseases
Manolio, T. A., Collins, F. S., Cox, N. J., Goldstein, D. B., Hindorff, L. A., Hunter, D. J., McCarthy, M. I., Ramos, E. M., Cardon, L. R., Chakravarti, A., et al. (2009) · Nature · doi:10.1038/nature08494 · Cited by 8,336 · see citing works
Improving Bioscience Research Reporting: The ARRIVE Guidelines for Reporting Animal Research
Kilkenny, C., Browne, W. J., Cuthill, I. C., Emerson, M., & Altman, D. G. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000412 · Cited by 7,300 · see citing works
Dose translation from animal to human studies revisited.
Reagan‐Shaw, S., Nihal, M., & Ahmad, N. (2008) · The FASEB Journal · doi:10.1096/fj.07-9574lsf · Cited by 6,524 · see citing works
Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research
Kilkenny, C., Browne, W. J., Cuthill, I. C., Emerson, M., & Altman, D. G. (2010) · Journal of Pharmacology and Pharmacotherapeutics · doi:10.4103/0976-500x.72351 · Cited by 6,277 · see citing works
The global prevalence of dementia: a systematic review and metaanalysis.
Prince, M., Bryce, R., Albanese, E., Wimo, A., Ribeiro, W., & Ferri, C. P. (2013) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2012.11.007 · Cited by 4,941 · see citing works
Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound‐B
Klunk, W. E., Engler, H., Nordberg, A., Wang, Y., Blomqvist, G., Holt, D. P., Bergström, M., Savitcheva, I., Huang, G., Estrada, S., et al. (2004) · Annals of Neurology · doi:10.1002/ana.20009 · Cited by 4,496 · see citing works
The Alzheimer’s disease neuroimaging initiative (ADNI): MRI methods
Jack, C. R., Bernstein, M. A., Fox, N. C., Thompson, P., Alexander, G., Harvey, D., Borowski, B., Britson, P. J., L. Whitwell, J., Ward, C., et al. (2008) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.21049 · Cited by 4,347 · see citing works
Shankar, G. M., Li, S., Mehta, T. H., Garcia-Munoz, A., Shepardson, N. E., Smith, I., Brett, F. M., Farrell, M. A., Rowan, M. J., Lemere, C. A., et al. (2008) · Nature Medicine · doi:10.1038/nm1782 · Cited by 3,685 · see citing works
2013 Alzheimer's disease facts and figures
Thies, W. H., & Bleiler, L. (2013) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2013.02.003 · Cited by 3,331 · see citing works
The projected effect of risk factor reduction on Alzheimer's disease prevalence
Barnes, D. E., & Yaffe, K. S. (2011) · The Lancet Neurology · doi:10.1016/s1474-4422(11)70072-2 · Cited by 2,668 · see citing works
An active and socially integrated lifestyle in late life might protect against dementia
Fratiglioni, L., Paillard-Borg, S., & Winblad, B. (2004) · The Lancet Neurology · doi:10.1016/s1474-4422(04)00767-7 · Cited by 2,135 · see citing works
The Meaning of Translational Research and Why It Matters
Woolf, S. H. (2008) · JAMA · doi:10.1001/jama.2007.26 · Cited by 1,910 · see citing works
Revising the definition of Alzheimer's disease: a new lexicon
Dubois, B., Feldman, H. H., Jacova, C., Cummings, J. L., DeKosky, S. T., Barberger-Gateau, P., Delacourte, A., Frisoni, G., Fox, N. C., Galasko, D., et al. (2010) · The Lancet Neurology · doi:10.1016/s1474-4422(10)70223-4 · Cited by 1,869 · see citing works
Cerebrospinal fluid and plasma biomarkers in Alzheimer disease
Blennow, K., Hampel, H., Weiner, M., & Zetterberg, H. (2010) · Nature Reviews Neurology · doi:10.1038/nrneurol.2010.4 · Cited by 1,863 · see citing works
How were new medicines discovered?
Swinney, D. C., & Anthony, J. (2011) · Nature Reviews Drug Discovery · doi:10.1038/nrd3480 · Cited by 1,812 · see citing works
Sex bias in neuroscience and biomedical research
Beery, A. K., & Zucker, I. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.07.002 · Cited by 1,763 · see citing works
Advances in the Study of Behavior
(1998) · Advances in the study of behavior · doi:10.1016/s0065-3454(13)60001-7 · Cited by 1,749 · see citing works
A mutation in APP protects against Alzheimer’s disease and age-related cognitive decline
Jonsson, T., Atwal, J. K., Steinberg, S., Snaedal, J., Jonsson, P. V., Bjornsson, S., Stefansson, H., Sulem, P., Gudbjartsson, D., Maloney, J., et al. (2012) · Nature · doi:10.1038/nature11283 · Cited by 1,738 · see citing works
Natural oligomers of the amyloid-β protein specifically disrupt cognitive function
Cleary, J. P., Walsh, D. M., Hofmeister, J. J., Shankar, G. M., Kuskowski, M. A., Selkoe, D. J., & Ashe, K. H. (2004) · Nature Neuroscience · doi:10.1038/nn1372 · Cited by 1,677 · see citing works
Epidemiology of Alzheimer disease
Reitz, C., Brayne, C., & Mayeux, R. (2011) · Nature Reviews Neurology · doi:10.1038/nrneurol.2011.2 · Cited by 1,675 · see citing works
Cellular prion protein mediates impairment of synaptic plasticity by amyloid-β oligomers
Laurén, J., Gimbel, D. A., Nygaard, H. B., Gilbert, J. W., & Strittmatter, S. M. (2009) · Nature · doi:10.1038/nature07761 · Cited by 1,560 · see citing works
Alzheimer’s Disease Neuroimaging Initiative
Mueller, S. G., Weiner, M. W., Thal, L. J., Petersen, R. C., Jack, C. R., Jagust, W. J., Trojanowski, J. Q., Toga, A. W., & Beckett, L. A. (2007) · Springer eBooks · doi:10.1007/978-0-387-72076-0_18 · Cited by 1,493 · see citing works
Can Animal Models of Disease Reliably Inform Human Studies?
van der Worp, H. B., Howells, D. W., Sena, E. S., Porritt, M. J., Rewell, S., O'Collins, V., & Macleod, M. R. (2010) · PLoS Medicine · doi:10.1371/journal.pmed.1000245 · Cited by 1,354 · see citing works
Lindsay, J. (2002) · American Journal of Epidemiology · doi:10.1093/aje/kwf074 · Cited by 1,261 · see citing works
Central challenges facing the national clinical research enterprise
Sung, N. S., Crowley, W. F., Genel, M., Salber, P., Sandy, L., Sherwood, L. M., Johnson, S. B., Catanese, V., Tilson, H., Getz, K., et al. (2003) · JAMA · doi:10.1001/jama.289.10.1278 · Cited by 1,235 · see citing works
Kalaria, R. N., Maestre, G. E., Arizaga, R., Friedland, R. P., Galasko, D., Hall, K., Luchsinger, J. A., Ogunniyi, A., Perry, E. K., Potocnik, F., et al. (2008) · The Lancet Neurology · doi:10.1016/s1474-4422(08)70169-8 · Cited by 1,233 · see citing works
Self-citationA call for transparent reporting to optimize the predictive value of preclinical research
Landis, S. C., Amara, S. G., Asadullah, K., Austin, C. P., Blumenstein, R., Bradley, E. W., Crystal, R. G., Darnell, R. B., Ferrante, R. J., Fillit, H., et al. (2012) · Nature · doi:10.1038/nature11556 · Cited by 1,196 · see citing works
CSF Biomarkers and Incipient Alzheimer Disease in Patients With Mild Cognitive Impairment
Mattsson, N. (2009) · JAMA · doi:10.1001/jama.2009.1064 · Cited by 1,176 · see citing works
The National Alzheimer's Coordinating Center (NACC) Database: The Uniform Data Set
Beekly, D. L., Ramos, E. M., Lee, W. W., Deitrich, W. D., Jacka, M. E., Wu, J., Hubbard, J. L., Koepsell, T. D., Morris, J. C., & Kukull, W. A. (2007) · Alzheimer Disease & Associated Disorders · doi:10.1097/wad.0b013e318142774e · Cited by 907 · see citing works
Kilkenny, C., Parsons, N., Kadyszewski, E., Festing, M. F. W., Cuthill, I. C., Fry, D., Hutton, J., & Altman, D. G. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007824 · Cited by 860 · see citing works
Immunization reverses memory deficits without reducing brain Aβ burden in Alzheimer's disease model
Dodart, J.-C., Bales, K. R., Gannon, K. S., Greene, S. J., DeMattos, R. B., Mathis, C., DeLong, C. A., Wu, S., Wu, X., Holtzman, D. M., et al. (2002) · Nature Neuroscience · doi:10.1038/nn842 · Cited by 858 · see citing works
Neuropathology of Alzheimer's Disease
Perl, D. P. (2010) · Mount Sinai Journal of Medicine: A Journal of Translational and Personalized Medicine · doi:10.1002/msj.20157 · Cited by 825 · see citing works
The question of familial meningiomas and schwannomas:
King, A. A., & Gutmann, D. H. (2000) · Neurology · doi:10.1212/wnl.54.1.4 · Cited by 814 · see citing works
Maruyama, M., Shimada, H., Suhara, T., Shinotoh, H., Ji, B., Maeda, J., Zhang, M.-R., Trojanowski, J. Q., Lee, V. M.-Y., Ono, M., et al. (2013) · Neuron · doi:10.1016/j.neuron.2013.07.037 · Cited by 760 · see citing works
Lannfelt, L., Blennow, K., Zetterberg, H., Batsman, S., Ames, D., Harrison, J., Masters, C. L., Targum, S., Bush, A. I., Murdoch, R., et al. (2008) · The Lancet Neurology · doi:10.1016/s1474-4422(08)70167-4 · Cited by 725 · see citing works
Self-citationSex Differences in the Brain: The Not So Inconvenient Truth
McCarthy, M. M., Arnold, A. P., Ball, G. F., Blaustein, J. D., & De Vries, G. J. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.5372-11.2012 · Cited by 724 · see citing works
Adlard, P. A., Cherny, R. A., Finkelstein, D. I., Gautier, E., Robb, E., Cortes, M., Volitakis, I., Liu, X., Smith, J. P., Perez, K., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.06.018 · Cited by 672 · see citing works
Self-citationBent, S. (2008) · Journal of General Internal Medicine · doi:10.1007/s11606-008-0632-y · Cited by 611 · see citing works
Better reporting of randomised controlled trials: the CONSORT statement
Altman, D. G. (1996) · BMJ · doi:10.1136/bmj.313.7057.570 · Cited by 605 · see citing works
Oxidative stress in the progression of Alzheimer disease in the frontal cortex
Ansari, M. A., & Scheff, S. W. (2010) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e3181cb5af4 · Cited by 605 · see citing works
Publication bias in reports of animal stroke studies leads to major overstatement of efficacy
Sena, E. S., van der Worp, H. B., Bath, P. M. W., Howells, D. W., & Macleod, M. R. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000344 · Cited by 600 · cited 2× · see citing works
“Thus, the validity of the outcomes may be questionable, widening the chasm between preclinical and clinical investigations [218].”
Um, J. W., Kaufman, A. C., Kostylev, M., Heiss, J. K., Stagi, M., Takahashi, H., Kerrisk, M. E., Vortmeyer, A., Wisniewski, T., Koleske, A. J., et al. (2013) · Neuron · doi:10.1016/j.neuron.2013.06.036 · Cited by 572 · see citing works
Castellani, R. J., Rolston, R. K., & Smith, M. A. (2010) · Disease-a-Month · doi:10.1016/j.disamonth.2010.06.001 · Cited by 561 · see citing works
Takeda, S., Sato, N., Uchio‐Yamada, K., Sawada, K., Kunieda, T., Takeuchi, D., Kurinami, H., Shinohara, M., Rakugi, H., & Morishita, R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000645107 · Cited by 506 · see citing works
Asuni, A. A., Boutajangout, A., Quartermain, D., & Sigurdsson, E. M. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2361-07.2007 · Cited by 506 · see citing works
A Unifying Role for Prions in Neurodegenerative Diseases
Prusiner, S. B. (2012) · Science · doi:10.1126/science.1222951 · Cited by 495 · see citing works
Divergence of human and mouse brain transcriptome highlights Alzheimer disease pathways
Miller, J. A., Horvath, S., & Geschwind, D. H. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914257107 · Cited by 480 · see citing works
Wu, J., Basha, R. M., Brock, B., Cox, D. P., Cardozo‐Pelaez, F., McPherson, C. A., Harry, J., Rice, D. C., Maloney, B., Chen, D., et al. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4405-07.2008 · Cited by 473 · see citing works
Self-citationFreiherr, J., Hallschmid, M., Frey, W. H., Brünner, Y. F., Chapman, C. D., Hölscher, C., Craft, S., Felice, F. G. D., & Benedict, C. (2013) · CNS Drugs · doi:10.1007/s40263-013-0076-8 · Cited by 470 · see citing works
Metal Binding Modes of Alzheimer's Amyloid β-Peptide in Insoluble Aggregates and Soluble Complexes
Miura, T., Suzuki, K., Kohata, N., & Takeuchi, H. (2000) · Biochemistry · doi:10.1021/bi0002479 · Cited by 452 · see citing works
Alzheimer disease models and human neuropathology: similarities and differences
Duyckaerts, C. J., Potier, M., & Delatour, B. (2007) · Acta Neuropathologica · doi:10.1007/s00401-007-0312-8 · Cited by 441 · see citing works
Animal Models of Alzheimer Disease
LaFerla, F. M., & Green, K. N. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a006320 · Cited by 419 · see citing works
Phenotypic vs. Target-Based Drug Discovery for First-in-Class Medicines
Swinney, D. C. (2013) · Clinical Pharmacology & Therapeutics · doi:10.1038/clpt.2012.236 · Cited by 417 · see citing works
A new amyloid β variant favoring oligomerization in Alzheimer's‐type dementia
Tomiyama, T., Nagata, T., Shimada, H., Teraoka, R., Fukushima, A., Kanemitsu, H., Takuma, H., Kuwano, R., Imagawa, M., Ataka, S., et al. (2008) · Annals of Neurology · doi:10.1002/ana.21321 · Cited by 414 · see citing works
Kim, T., Vidal, G. S., Djurisic, M., William, C. M., Birnbaum, M. E., Garcia, K. C., Hyman, B. T., & Shatz, C. J. (2013) · Science · doi:10.1126/science.1242077 · Cited by 410 · see citing works
The Alzheimer's Association external quality control program for cerebrospinal fluid biomarkers
Mattsson, N., Andréasson, U., Persson, S., Arai, H., Batish, S. D., Bernardini, S., Bocchio‐Chiavetto, L., Blankenstein, M. A., Carrillo, M. C., Chalbot, S., et al. (2011) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2011.05.2243 · Cited by 409 · see citing works
Self-citationPBT2 Rapidly Improves Cognition in Alzheimer's Disease: Additional Phase II Analyses
Faux, N. G., Ritchie, C. W., Gunn, A. P., Rembach, A., Tsatsanis, A., Bedő, J., Harrison, J., Lannfelt, L., Blennow, K., Zetterberg, H., et al. (2010) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-1390 · Cited by 406 · see citing works
Self-citationTomiyama, T., Matsuyama, S., Iso, H., Umeda, T., Takuma, H., Ohnishi, K., Ishibashi, K., Teraoka, R., Sakama, N., Yamashita, T., et al. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5825-09.2010 · Cited by 396 · see citing works
Minamide, L. S., Striegl, A. M., Boyle, J. A., Meberg, P. J., & Bamburg, J. R. (2000) · Nature Cell Biology · doi:10.1038/35023579 · Cited by 394 · see citing works
Self-citationLobo, A., Launer, L. J., Fratiglioni, L., Andersen, K., Di Carlo, A., Breteler, M. M. B., Copeland, J., Dartigues, J. F., Jagger, C., Martinez-Lage, J., et al. (2000) · University of Southern Denmark Research Portal (University of Southern Denmark) · Cited by 388 · see citing works
Computational Drug Repositioning: From Data to Therapeutics
Hurle, M. R., Yang, L., Xie, Q. S., Rajpal, D. K., Sanséau, P., & Agarwal, P. (2013) · Clinical Pharmacology & Therapeutics · doi:10.1038/clpt.2013.1 · Cited by 375 · see citing works
Basha, R. M., Wei, W., Bakheet, S. A., Benitez, N. B., Siddiqi, H. K., Ge, Y., Lahiri, D. K., & Zawia, N. H. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4335-04.2005 · Cited by 353 · see citing works
Self-citationArendash, G. W., King, D. L., Gordon, M. N., Morgan, D., Hatcher, J. M., Hope, C. E., & Diamond, D. M. (2001) · Brain Research · doi:10.1016/s0006-8993(00)03186-3 · Cited by 349 · see citing works
Similarities and Differences in Genome-Wide Expression Data of Six Organisms
Bergmann, S., Ihmels, J., & Barkai, N. (2003) · PLoS Biology · doi:10.1371/journal.pbio.0020009 · Cited by 348 · see citing works
Blood–Brain Barrier Pathology in Alzheimer's and Parkinson's Disease: Implications for Drug Therapy
Desai, B. S., Monahan, A. J., Carvey, P. M., & Hendey, B. (2007) · Cell Transplantation · doi:10.3727/000000007783464731 · Cited by 339 · see citing works
Removing Obstacles in Neuroscience Drug Discovery: The Future Path for Animal Models
Markou, A., Chiamulera, C., Geyer, M. A., Tricklebank, M., & Steckler, T. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.173 · Cited by 328 · see citing works
Traumatic brain injury: A risk factor for Alzheimer's disease
Sivanandam, T. M., & Thakur, M. K. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.02.013 · Cited by 326 · see citing works
ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity
Gu, J., Lee, C. W., Fan, Y., Komlos, D., Tang, X., Sun, C., Yu, K., Hartzell, H. C., Chen, G., Bamburg, J. R., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2634 · Cited by 325 · see citing works
Self-citationJacob, C. P., Koutsilieri, E., Bartl, J., Neuen-Jacob, E., Arzberger, T., Zander, N., Ravid, R., Roggendorf, W., Riederer, P., & Grünblatt, E. (2007) · Journal of Alzheimer's Disease · doi:10.3233/jad-2007-11113 · Cited by 317 · see citing works
Role of p21-activated kinase pathway defects in the cognitive deficits of Alzheimer disease
Zhao, L., Ma, Q.-L., Calon, F., Harris-White, M. E., Yang, F., Lim, G. P., Morihara, T., Ubeda, O. J., Ambegaokar, S., Hansen, J. E., et al. (2006) · Nature Neuroscience · doi:10.1038/nn1630 · Cited by 317 · see citing works
Mouse models of Alzheimer's disease
Hall, A. M., & Roberson, E. D. (2012) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2011.11.017 · Cited by 317 · see citing works
The future of blood‐based biomarkers for Alzheimer's disease
Henriksen, K., O’Bryant, S. E., Hampel, H. J., Trojanowski, J. Q., Montine, T. J., Jeromin, A., Blennow, K., Lönneborg, A., Wyss‐Coray, T., Soares, H. D., et al. (2013) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2013.01.013 · Cited by 312 · see citing works
Bond, M., Rogers, G., Peters, J., Anderson, R., Hoyle, M., Miners, A. H., Moxham, T., Davis, S., Thokala, P., Wailoo, A., et al. (2012) · Health Technology Assessment · doi:10.3310/hta16210 · Cited by 308 · see citing works
Cerebrospinal fluid markers for differential dementia diagnosis in a large memory clinic cohort
Schoonenboom, N. S. M., Reesink, F. E., Verwey, N. A., Kester, M. I., Teunissen, C. E., van de Ven, P. M., Pijnenburg, Y. A. L., Blankenstein, M. A., Rozemuller, A. J., Scheltens, P., et al. (2012) · Neurology · doi:10.1212/wnl.0b013e31823ed0f0 · Cited by 302 · see citing works
Young, J. W., Powell, S. B., Risbrough, V. B., Marston, H. M., & Geyer, M. A. (2009) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2009.02.004 · Cited by 299 · see citing works
Calabrese, C., Gregory, W. L., Leo, M., Kraemer, D., Bone, K., & Oken, B. (2008) · The Journal of Alternative and Complementary Medicine · doi:10.1089/acm.2008.0018 · Cited by 281 · cited 1× · see citing works
“successful human trials [15–17].”
Neuroprotection for Ischaemic Stroke: Translation from the Bench to the Bedside
Sutherland, B. A., Minnerup, J., Balami, J. S., Arba, F., Buchan, A. M., & Kleinschnitz, C. (2012) · International Journal of Stroke · doi:10.1111/j.1747-4949.2012.00770.x · Cited by 259 · see citing works
Genome-wide association studies in Alzheimer’s disease
Bertram, L., & Tanzi, R. E. (2009) · Human Molecular Genetics · doi:10.1093/hmg/ddp406 · Cited by 257 · see citing works
Genetics of familial and sporadic Alzheimer s disease
Piaceri, I. (2013) · Frontiers in Bioscience · doi:10.2741/e605 · Cited by 256 · see citing works
Bakulski, K. M., Dolinoy, D. C., Sartor, M. A., Paulson, H. L., Konen, J. R., Lieberman, A. P., Albin, R. L., Hu, H., & Rozek, L. S. (2012) · Journal of Alzheimer's Disease · doi:10.3233/jad-2012-111223 · Cited by 255 · see citing works
Shaffer, J. L., Petrella, J. R., Sheldon, F. C., Choudhury, K. R., Calhoun, V. D., Coleman, R. E., Doraiswamy, P. M., & Initiative, A. D. N. (2012) · Radiology · doi:10.1148/radiol.12120010 · Cited by 255 · see citing works
Donald, J. M. M., Savva, G. M., Brayne, C., Welzel, A. T., Forster, G., Shankar, G. M., Selkoe, D. J., Ince, P. G., & Walsh, D. M. (2010) · Brain · doi:10.1093/brain/awq065 · Cited by 251 · see citing works
Palanza, P., Gioiosa, L., & Parmigiani, S. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00494-2 · Cited by 244 · see citing works
Emergency medicine animal research: does use of randomization and blinding affect the results?
Bebarta, V., Luyten, D., & Heard, K. (2003) · Academic Emergency Medicine · doi:10.1111/j.1553-2712.2003.tb00056.x · Cited by 244 · see citing works
Animal models in the drug discovery pipeline for Alzheimer's disease
Dam, D. V., & Deyn, P. P. D. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01299.x · Cited by 228 · see citing works
Amyloid-β assessed by florbetapir F 18 PET and 18-month cognitive decline
Doraiswamy, P. M., Sperling, R. A., Coleman, R. E., Johnson, K. A., Reiman, E. M., Davis, M. D., Grundman, M., Sabbagh, M. N., Sadowsky, C., Fleisher, A., et al. (2012) · Neurology · doi:10.1212/wnl.0b013e3182661f74 · Cited by 228 · see citing works
Evidence for Ordering of Alzheimer Disease Biomarkers
Jack, C. R. (2011) · Archives of Neurology · doi:10.1001/archneurol.2011.183 · Cited by 221 · see citing works
Behrendt, G., Baer, K., Buffo, A., Curtis, M. A., Faull, R. L., Rees, M. I., Götz, M., & Dimou, L. (2013) · Glia · doi:10.1002/glia.22432 · Cited by 219 · see citing works
A phenotypic and molecular characterization of the <i>fmr1‐tm1Cgr</i> Fragile X mouse
Yan, Q. J., Asafo‐Adjei, P. K., Arnold, H. M., Brown, R. E., & Bauchwitz, R. P. (2004) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2004.00087.x · Cited by 213 · see citing works
Self-citationThe LEARn model: an epigenetic explanation for idiopathic neurobiological diseases
Lahiri, D. K., Maloney, B., & Zawia, N. H. (2009) · Molecular Psychiatry · doi:10.1038/mp.2009.82 · Cited by 211 · see citing works
Self-citationAlzheimer's disease drug development and the problem of the blood‐brain barrier
Pardridge, W. M. (2009) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2009.06.003 · Cited by 203 · see citing works
Strain and Sex Differences in Anxiety-Like and Social Behaviors in C57BL/6J and BALB/cJ Mice
An, X., Jun-Xian, Z. O. U., Wu, R., Yang, Y., Tai, F., Zeng, S., Jia, R., Zhang, X., Liu, E., & Broders, H. G. (2011) · EXPERIMENTAL ANIMALS · doi:10.1538/expanim.60.111 · Cited by 203 · see citing works
A Mouse Model Characterizing Features of Vascular Dementia With Hippocampal Atrophy
Nishio, K., Ihara, M., Yamasaki, N., Kalaria, R. N., Maki, T., Fujita, Y., Ito, H., Oishi, N., Fukuyama, H., Miyakawa, T., et al. (2010) · Stroke · doi:10.1161/strokeaha.110.581686 · Cited by 202 · see citing works
Self-citationPallàs, M., Camins, A., Smith, M. A., Perry, G. L., Lee, H., & Casadesús, G. (2008) · Journal of Alzheimer s Disease · doi:10.3233/jad-2008-15408 · Cited by 199 · see citing works
Ballatore, C., Brunden, K. R., Huryn, D. M., Trojanowski, J. Q., Lee, V. M. ‐., & Smith, A. B. (2012) · Journal of Medicinal Chemistry · doi:10.1021/jm301079z · Cited by 197 · see citing works
Neuroinflammatory phenotype in early Alzheimer's disease
Sudduth, T. L., Schmitt, F. A., Nelson, P. T., & Wilcock, D. M. (2012) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2012.09.012 · Cited by 194 · see citing works
Bakulski, K., Rozek, L., Dolinoy, D., Paulson, H., & Hu, H. (2012) · Current Alzheimer Research · doi:10.2174/156720512800617991 · Cited by 193 · see citing works
Zommer, N., Sergeant, N., Schraen-Maschke, S., Blum, D., & Buee, L. (2012) · Current Alzheimer Research · doi:10.2174/156720512800492503 · Cited by 193 · see citing works
Regulatory Innovation and Drug Development for Early-Stage Alzheimer's Disease
Kozauer, N., & Katz, R. G. (2013) · New England Journal of Medicine · doi:10.1056/nejmp1302513 · Cited by 193 · see citing works
Targeted proteomics for quantification of histone acetylation in A lzheimer's disease
Zhang, K., Schrag, M., Crofton, A. R., Trivedi, R. K., Vinters, H. V., & Kirsch, W. M. (2012) · PROTEOMICS · doi:10.1002/pmic.201200010 · Cited by 191 · see citing works
Longitudinal Change of Biomarkers in Cognitive Decline
Lo, R. Y. (2011) · Archives of Neurology · doi:10.1001/archneurol.2011.123 · Cited by 190 · see citing works
Modern Phenotypic Drug Discovery Is a Viable, Neoclassic Pharma Strategy
Lee, J. A., Uhlik, M. T., Moxham, C. M., Tomandl, D., & Sall, D. J. (2012) · Journal of Medicinal Chemistry · doi:10.1021/jm201649s · Cited by 190 · see citing works
Visual detection, pattern discrimination and visual acuity in 14 strains of mice
Wong, A. A., & Brown, R. E. (2005) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2005.00173.x · Cited by 188 · see citing works
Self-citationSurveillance for ocular hypertension: an evidence synthesis and economic evaluation.
Burr, J., Botello-Pinzon, P., Takwoingi, Y., Hernández, R., Vazquez-Montes, M., Elders, A., Asaoka, R., Banister, K., van der Schoot, J., Fraser, C., et al. (2012) · Health Technology Assessment · doi:10.3310/hta16290 · Cited by 180 · see citing works
SNP association studies in Alzheimer's disease highlight problems for complex disease analysis
Emahazion, T. (2001) · Trends in Genetics · doi:10.1016/s0168-9525(01)02342-3 · Cited by 180 · see citing works
Ray, B., Bisht, S., Maitra, A., Maitra, A., & Lahiri, D. K. (2011) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-101374 · Cited by 177 · see citing works
Self-citationExposure to lead (Pb) and the developmental origin of oxidative DNA damage in the aging brain
Bolin, C. M., Basha, R. M., Cox, D., Zawia, N. H., Maloney, B., Lahiri, D. K., & Cardozo‐Pelaez, F. (2006) · The FASEB Journal · doi:10.1096/fj.05-5091fje · Cited by 173 · see citing works
Self-citationVerwey, N. A., van der Flier, W. M., Blennow, K., Clark, C. M., Sokolow, S., Deyn, P. P. D., Galasko, D. R., Hampel, H. J., Hartmann, T., Kapaki, E., et al. (2009) · Annals of Clinical Biochemistry International Journal of Laboratory Medicine · doi:10.1258/acb.2009.008232 · Cited by 169 · see citing works
Nonhuman Primate Models of Alzheimer-Like Cerebral Proteopathy
Heuer, E., F. Rosen, R., Cintron, A., & C. Walker, L. (2012) · Current Pharmaceutical Design · doi:10.2174/138161212799315885 · Cited by 169 · see citing works
Bellingham, S. A., Lahiri, D. K., Maloney, B., Fontaine, S. L., Multhaup, G., & Camakaris, J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m400805200 · Cited by 165 · see citing works
Self-citationUpdate on the Pharmacological Treatment of Alzheimers Disease
Massoud, F., & Gauthier, S. G. (2010) · Current Neuropharmacology · doi:10.2174/157015910790909520 · Cited by 161 · see citing works
Gao, J., Prough, D. S., McAdoo, D. J., Grady, J. J., Parsley, M. O., Ma, L., TARENSENKO, Y., & Wu, P. (2006) · Experimental Neurology · doi:10.1016/j.expneurol.2006.04.039 · Cited by 156 · see citing works
Devi, L., Alldred, M. J., Ginsberg, S. D., & Ohno, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032792 · Cited by 155 · see citing works
Akinyemi, R., Mukaetova-Ladinska, E., Attems, J., Ihara, M., & Kalaria, R. (2013) · Current Alzheimer Research · doi:10.2174/15672050113109990037 · Cited by 152 · see citing works
Self-citationVellas, B., Carrillo, M. C., Sampaio, C., Brashear, H. R., Siemers, E., Hampel, H., Schneider, L. S., Weiner, M., Doody, R., Khachaturian, Z., et al. (2013) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2013.03.007 · Cited by 147 · see citing works
The lonely mouse: Verification of a separation-induced model of depression in female mice
Martin, A. L., & Brown, R. E. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.10.006 · Cited by 147 · see citing works
Self-citationPlaques, Tangles, and Memory Loss in Mouse Models of Neurodegeneration
Eriksen, J. L., & Janus, C. G. (2007) · Behavior Genetics · doi:10.1007/s10519-006-9118-z · Cited by 146 · see citing works
Lewis, H. D., Beher, D., Cookson, N., Oakley, A. E., Piggott, M. A., Morris, C. M., Jaros, E., Perry, R., Ince, P. G., Kenny, R. A., et al. (2006) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2006.00696.x · Cited by 143 · see citing works
Self-citationMaesako, M., Uemura, K., Kubota, M., Kuzuya, A., Sasaki, K., Hayashida, N., Asada-Utsugi, M., Watanabe, K., Uemura, M., Kihara, T., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.367011 · Cited by 141 · see citing works
Intracerebroventricular Administration of Drugs
Cook, A. M., Mieure, K. D., Owen, R. D., Pesaturo, A. B., & Hatton, J. (2009) · Pharmacotherapy The Journal of Human Pharmacology and Drug Therapy · doi:10.1592/phco.29.7.832 · Cited by 139 · see citing works
Arisi, I., D’Onofrio, M., Brandi, R., Felsani, A., Capsoni, S., Drovandi, G., Felici, G., Weitschek, E., Bertolazzi, P., & Cattaneo, A. (2011) · Journal of Alzheimer s Disease · doi:10.3233/jad-2011-101881 · Cited by 139 · see citing works
Neuropathologic Studies of the Baltimore Longitudinal Study of Aging (BLSA)
O'Brien, R. J., Resnick, S. M., Zonderman, A. B., Ferrucci, L., Crain, B. J., Pletnikova, O., Rudow, G., Iacono, D., Riudavets, M. A., Driscoll, I., et al. (2009) · Journal of Alzheimer's Disease · doi:10.3233/jad-2009-1179 · Cited by 137 · see citing works
Epidemiological of and risk factors for Alzheimer's disease: A review
Povová, J., Ambrož, P., Bar, M., Pavuková, V., Šerý, O., Tomášková, H., & Janout, V. (2012) · Biomedical Papers · doi:10.5507/bp.2012.055 · Cited by 136 · see citing works
Accelerating drug discovery for Alzheimer's disease: best practices for preclinical animal studies
Shineman, D. W., Basi, G. S., Bizon, J. L., Colton, C. A., Greenberg, B., Hollister, B. A., Lincecum, J. M., Leblanc, G. G., Lee, L. H., Luo, F. R., et al. (2011) · Alzheimer s Research & Therapy · doi:10.1186/alzrt90 · Cited by 136 · see citing works
Brain imaging in the study of Alzheimer's disease
Reiman, E. M., & Jagust, W. J. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.11.075 · Cited by 134 · see citing works
Maloney, M. T., Minamide, L. S., Kinley, A. W., Boyle, J. A., & Bamburg, J. R. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3711-05.2005 · Cited by 131 · see citing works
Self-citationWhat are We Measuring When We Test Strain Differences in Anxiety in Mice?
O’Leary, T. P., Gunn, R. K., & Brown, R. E. (2013) · Behavior Genetics · doi:10.1007/s10519-012-9572-8 · Cited by 131 · see citing works
Self-citationter Riet, G., Korevaar, D. A., Leenaars, M., Sterk, P. J., Noorden, C. J. F. V., Bouter, L. M., Lutter, R., Elferink, R. P. J. O., & Hooft, L. (2012) · PLoS ONE · doi:10.1371/journal.pone.0043404 · Cited by 131 · see citing works
The blood-brain barrier and cerebral microcirculation in Alzheimer disease.
Kalaria, R. N. (1992) · PubMed · Cited by 130 · see citing works
Self-citationThe Genetics of the Human APOE Polymorphism
Seripa, D., D’Onofrio, G., Panza, F., Cascavilla, L., Masullo, C., & Pilotto, A. (2011) · Rejuvenation Research · doi:10.1089/rej.2011.1169 · Cited by 128 · see citing works
Tau‐targeted treatment strategies in Alzheimer's disease
Götz, J., Ittner, A., & Ittner, L. M. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01713.x · Cited by 127 · see citing works
Sex difference in pathology and memory decline in rTg4510 mouse model of tauopathy
Yue, M., Hanna, A., Wilson, J., Roder, H. M., & Janus, C. (2009) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2009.04.006 · Cited by 125 · see citing works
Innovative solutions to novel drug development in mental health
Insel, T. R., Voon, V., Nye, J. S., Brown, V. J., Altevogt, B. M., Bullmore, E. T., Goodwin, G. M., Howard, R. J., Kupfer, D. J., Malloch, G., et al. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.03.022 · Cited by 124 · see citing works
Mandel, R. J. (2010) · PubMed · Cited by 123 · see citing works
(2012) · doi:10.1038/nrneurol.2012.118 · Cited by 122 · see citing works
Adlard, P. A., Bica, L., White, A. R., Nurjono, M., Filiz, G., Crouch, P. J., Donnelly, P. S., Cappai, R., Finkelstein, D. I., & Bush, A. I. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017669 · Cited by 120 · see citing works
Recent rodent models for Alzheimer’s disease: clinical implications and basic research
Braidy, N., Muñoz, P., Palacios, A. G., Castellano‐González, G., Inestrosa, N. C., Chung, R. S., Sachdev, P. S., & Guillemin, G. J. (2011) · Journal of Neural Transmission · doi:10.1007/s00702-011-0731-5 · Cited by 119 · see citing works
Large scale comparison of global gene expression patterns in human and mouse
Zheng-Bradley, X., Rung, J., Parkinson, H., & Brāzma, A. (2010) · Genome biology · doi:10.1186/gb-2010-11-12-r124 · Cited by 119 · see citing works
Standards for the publication of mouse mutant studies
Crusio, W. E., Goldowitz, D., Holmes, A., & Wolfer, D. P. (2008) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2008.00438.x · Cited by 118 · see citing works
CNTRICS final animal model task selection: Control of attention
Lustig, C., Kozak, R., Sarter, M. F., Young, J. W., & Robbins, T. W. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.05.009 · Cited by 117 · see citing works
Overlapping profiles of Aβ peptides in the Alzheimer's disease and pathological aging brains
Moore, B. D., Chakrabarty, P., Levites, Y., Kukar, T. L., Baine, A.-M. T., Moroni, T., Ladd, T. B., Das, P., Dickson, D. W., & Golde, T. E. (2012) · Alzheimer s Research & Therapy · doi:10.1186/alzrt121 · Cited by 112 · see citing works
Cofilin-mediated neurodegeneration in alzheimer’s disease and other amyloidopathies
Maloney, M. T., & Bamburg, J. R. (2007) · Molecular Neurobiology · doi:10.1007/bf02700622 · Cited by 112 · see citing works
Self-citationToward the Treatment and Prevention of Alzheimer's Disease: Rational Strategies and Recent Progress
Gandy, S., & DeKosky, S. T. (2013) · Annual Review of Medicine · doi:10.1146/annurev-med-092611-084441 · Cited by 110 · see citing works
Pharmacogenomics in Alzheimer's Disease
Cacabelos, R. (2008) · Methods in molecular biology · doi:10.1007/978-1-59745-205-2_10 · Cited by 109 · see citing works
Traditional Chinese medicine: a promising candidate for the treatment of Alzheimer’s disease
Sun, Z., Yang, H., & Chen, S. (2013) · Translational Neurodegeneration · doi:10.1186/2047-9158-2-6 · Cited by 106 · see citing works
Drug delivery strategies for Alzheimer's disease treatment
Stefano, A. D., Iannitelli, A., Laserra, S., & Sozio, P. (2011) · Expert Opinion on Drug Delivery · doi:10.1517/17425247.2011.561311 · Cited by 105 · see citing works
Nathan, P. J., Clarke, J., Lloyd, J., Hutchison, C. W., Downey, L., & Stough, C. (2001) · Human Psychopharmacology Clinical and Experimental · doi:10.1002/hup.306 · Cited by 103 · see citing works
Pathogenesis and Disease-modifying Therapy in Alzheimer's Disease: The Flat Line of Progress
Castellani, R. J., & Perry, G. L. (2012) · Archives of Medical Research · doi:10.1016/j.arcmed.2012.09.009 · Cited by 103 · see citing works
Ray, B., Chauhan, N. B., & Lahiri, D. K. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.07145.x · Cited by 101 · see citing works
Self-citationAge-related changes in visual acuity, learning and memory in C57BL/6J and DBA/2J mice
Wong, A. A., & Brown, R. E. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.07.023 · Cited by 101 · see citing works
Self-citationEffectiveness of antidementia drugs in delaying Alzheimer's disease progression
Rountree, S. D., Atri, A., Lopez, O. L., & Doody, R. S. (2013) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2012.01.002 · Cited by 97 · see citing works
Davis, R. C., Marsden, I. T., Maloney, M. T., Minamide, L. S., Podlisny, M. B., Selkoe, D. J., & Bamburg, J. R. (2011) · Molecular Neurodegeneration · doi:10.1186/1750-1326-6-10 · Cited by 97 · see citing works
Self-citationCichon, J., Sun, C., Chen, B., Jiang, M., Chen, X. A., Sun, Y., Wang, Y., & Chen, G. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.301911 · Cited by 95 · see citing works
Amadoro, G., Corsetti, V., Atlante, A., Florenzano, F., Capsoni, S., Bussani, R., Mercanti, D., & Calissano, P. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2011.08.001 · Cited by 94 · see citing works
Selecting a Mouse Model of Alzheimer’s Disease
Chin, J. (2010) · Methods in molecular biology · doi:10.1007/978-1-60761-744-0_13 · Cited by 93 · see citing works
Do early-life insults contribute to the late-life development of Parkinson and Alzheimer diseases?
Miller, D. B., & O'Callaghan, J. P. (2008) · Metabolism · doi:10.1016/j.metabol.2008.07.011 · Cited by 93 · see citing works
MicroRNA-Related Cofilin Abnormality in Alzheimer's Disease
Yao, J., Hennessey, T., Flynt, A. S., Lai, E. C., Beal, M. F., & Lin, M. T. S. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015546 · Cited by 92 · see citing works
Edrey, Y. H., Medina, D. X., Gaczynska, M. E., Osmulski, P. A., Oddo, S., Caccamo, A., & Buffenstein, R. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.03.032 · Cited by 91 · see citing works
Zhuo, J., & Praticò, D. (2009) · Experimental Gerontology · doi:10.1016/j.exger.2009.12.005 · Cited by 89 · see citing works
Luo, F. R., Rustay, N. R., Ebert, U., Hradil, V. P., Cole, T. B., Llano, D. A., Mudd, S. R., Zhang, Y., Fox, G. B., & Day, M. (2010) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2010.08.005 · Cited by 88 · see citing works
Calahorro, F., & Ruiz‐Rubio, M. (2011) · Invertebrate Neuroscience · doi:10.1007/s10158-011-0126-1 · Cited by 85 · see citing works
Bernstein, B. W., Shaw, A. E., Minamide, L. S., Pak, C. W., & Bamburg, J. R. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.6020-11.2012 · Cited by 84 · see citing works
Self-citationTang, J., Xu, H., Fan, X., Li, D., Rancourt, D. E., Zhou, G., Li, Z., & Li, Y. (2008) · Neuroscience Research · doi:10.1016/j.neures.2008.06.005 · Cited by 83 · see citing works
Normal cognition in transgenic BRI2-Aβ mice
Kim, J., Chakrabarty, P., Hanna, A., March, A., Dickson, D. W., Borchelt, D. R., Golde, T., & Janus, C. (2013) · Molecular Neurodegeneration · doi:10.1186/1750-1326-8-15 · Cited by 83 · see citing works
Hölscher, C. (2014) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2013.12.006 · Cited by 83 · see citing works
Developing novel immunogens for a safe and effective Alzheimer's disease vaccine
Lemere, C. A. (2009) · Progress in brain research · doi:10.1016/s0079-6123(09)17506-4 · Cited by 82 · see citing works
Zebrafish as a tool in Alzheimer's disease research
Newman, M., Verdile, G., Martins, R. N., & Lardelli, M. T. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2010.09.012 · Cited by 82 · see citing works
O’Leary, T. P., & Brown, R. E. (2011) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2011.09.027 · Cited by 82 · see citing works
Self-citationAn Active Lifestyle Postpones Dementia Onset by More than One Year in Very Old Adults
Paillard‐Borg, S., Fratiglioni, L., Xu, W., Winblad, B. G., & Wang, H. (2012) · Journal of Alzheimer s Disease · doi:10.3233/jad-2012-120724 · Cited by 81 · see citing works
O’Leary, T. P., & Brown, R. E. (2013) · Learning & Memory · doi:10.1101/lm.028076.112 · Cited by 81 · see citing works
Self-citationEpigenetic regulation of BACE1 in Alzheimer’s disease patients and in transgenic mice
Marques, S., Lemos, R., Ferreiro, E. B., Martins, M., de Mendonça, A., Santana, I. J., Outeiro, T. F., & Pereira, C. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.06.029 · Cited by 81 · see citing works
Linder, C. C. (2001) · PubMed · Cited by 80 · see citing works
The response of C57BL/6J and BALB/cJ mice to increased housing density.
(2009) · PubMed Central · Cited by 80 · see citing works
The relevance of individual genetic background and its role in animal models of epilepsy
Schauwecker, P. E. (2011) · Epilepsy Research · doi:10.1016/j.eplepsyres.2011.09.005 · Cited by 80 · see citing works
Isolation and Characterization of Cytoplasmic Cofilin-Actin Rods
Minamide, L. S., Maiti, S., Boyle, J. A., Davis, R. C., Coppinger, J. A., Bao, Y., Huang, T. Y., Yates, J. R., Bokoch, G., & Bamburg, J. R. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.063768 · Cited by 79 · see citing works
Self-citationGlobal similarity and local divergence in human and mouse gene co-expression networks
Tsaparas, P., Mariño‐Ramírez, L., Bodenreider, O., Koonin, E. V., & Jordan, I. K. (2006) · BMC Evolutionary Biology · doi:10.1186/1471-2148-6-70 · Cited by 79 · see citing works
Emergency Medicine Animal Research: Does Use of Randomization and Blinding Affect the Results?
Bebarta, V. (2003) · Academic Emergency Medicine · doi:10.1197/aemj.10.6.684 · Cited by 79 · see citing works
Affinity of Cu+ for the Copper-Binding Domain of the Amyloid-β Peptide of Alzheimer’s Disease
Feaga, H. A., Maduka, R. C., Foster, M. N., & Szalai, V. A. (2011) · Inorganic Chemistry · doi:10.1021/ic100967s · Cited by 78 · see citing works
Schellinck, H. M., Cyr, D. P., & Brown, R. E. (2010) · Advances in the study of behavior · doi:10.1016/s0065-3454(10)41007-4 · Cited by 77 · see citing works
Self-citationA Review of the Major Vascular Risk Factors Related to Alzheimer's Disease
Polidori, M. C., Pientka, L., & Mecocci, P. (2012) · Journal of Alzheimer s Disease · doi:10.3233/jad-2012-120871 · Cited by 77 · see citing works
Norton, M. C., Dew, J. P., Smith, H., Fauth, E. B., Piercy, K. W., Breitner, J. C. S., Tschanz, J. T., Wengreen, H. J., Welsh-Bohmer, K. A., & for the Cache County Investigators (2012) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2011.03860.x · Cited by 77 · see citing works
Lessons from immunotherapy for Alzheimer disease
Wang, Y. (2014) · Nature Reviews Neurology · doi:10.1038/nrneurol.2014.44 · Cited by 77 · see citing works
Lista, S., Garaci, F., Ewers, M., Teipel, S. J., Zetterberg, H., Blennow, K., & Hampel, H. J. (2013) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2013.04.506 · Cited by 76 · see citing works
Hong, L., Carducci, T. M., Bush, W. D., Dudzik, C. G., Millhauser, G. L., & Simon, J. D. (2010) · The Journal of Physical Chemistry B · doi:10.1021/jp103272v · Cited by 73 · see citing works
The rat as an animal model of Alzheimer's disease
Benedikz, E., Kloskowska, E., & Winblad, B. G. (2009) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2009.00781.x · Cited by 73 · see citing works
Ferreira, F. A., de Souza, R. R., Moraes, B. D. S., Ferreira, A. M. D. A., Américo, M. A., Fracalanzza, S. E. L., Couceiro, J. N. D. S. S., & Figueiredo, A. M. S. (2013) · BMC Microbiology · doi:10.1186/1471-2180-13-93 · Cited by 72 · see citing works
Teunissen, C. E., Verwey, N. A., Kester, M. I., van Uffelen, K. W. J., & Blankenstein, M. A. (2010) · International Journal of Alzheimer s Disease · doi:10.4061/2010/635053 · Cited by 70 · see citing works
Downey, L. A., Kean, J., Nemeh, F., Lau, A., Poll, A., Gregory, R., Murray, M., Rourke, J., Patak, B., Pase, M. P., et al. (2013) · Phytotherapy Research · doi:10.1002/ptr.4864 · Cited by 70 · see citing works
The application of cerebrospinal fluid biomarkers in early diagnosis of Alzheimer disease
Blennow, K., & Zetterberg, H. (2013) · Medical Clinics of North America · doi:10.1016/j.mcna.2012.12.012 · Cited by 69 · see citing works
Promiscuous Alzheimer's Amyloid: Yet Another Partner
Benilova, I., & De Strooper, B. (2013) · Science · doi:10.1126/science.1244166 · Cited by 67 · see citing works
Quantifying the Pathophysiological Timeline of Alzheimer's Disease
Yang, E., Farnum, M. A., Lobanov, V. S., Schultz, T., Raghavan, N., Samtani, M. N., Novak, G., Narayan, V. A., DiBernardo, A., & Initiative1, A. T. A. D. N. (2011) · Journal of Alzheimer s Disease · doi:10.3233/jad-2011-110551 · Cited by 66 · see citing works
Walsh, K. P., Minamide, L. S., Kane, S. J., Shaw, A. E., Brown, D. R., Pulford, B. E., Zabel, M. D., Lambeth, J. D., Kuhn, T. B., & Bamburg, J. R. (2014) · PLoS ONE · doi:10.1371/journal.pone.0095995 · Cited by 65 · see citing works
Self-citationClinical and research diagnostic criteria for Alzheimer's disease
Sarazin, M., de Souza, L. C., Lehéricy, S., & Dubois, B. (2012) · Neuroimaging Clinics of North America · doi:10.1016/j.nic.2011.11.004 · Cited by 64 · see citing works
Criteria for the neuropathological diagnosis of dementing disorders: routes out of the swamp?
Jellinger, K. A. (2009) · Acta Neuropathologica · doi:10.1007/s00401-008-0466-z · Cited by 60 · see citing works
The levels of water-soluble and triton-soluble Aβ are increased in Alzheimer's disease brain
McDonald, J. M., Cairns, N. J., Taylor‐Reinwald, L., Holtzman, D. M., & Walsh, D. M. (2012) · Brain Research · doi:10.1016/j.brainres.2012.02.041 · Cited by 60 · see citing works
Do current therapeutic anti-Aβ antibodies for Alzheimer’s disease engage the target?
Watt, A. D., Crespi, G. A. N., Down, R. A., Ascher, D. B., Gunn, A. P., Perez, K. A., McLean, C., Villemagne, V. L., Parker, M. W., Barnham, K. J., et al. (2014) · Acta Neuropathologica · doi:10.1007/s00401-014-1290-2 · Cited by 60 · see citing works
Detecting spatial memory deficits beyond blindness in tg2576 Alzheimer mice
Yassine, N., Lazaris, A., Dorner‐Ciossek, C., Després, O., Meyer, L., Maître, M., Mensah‐Nyagan, A. G., Cassel, J., & Mathis, C. (2012) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2012.06.016 · Cited by 58 · see citing works
Supporting evidence for using biomarkers in the diagnosis of MCI due to AD
Galluzzi, S., Geroldi, C., Amicucci, G., Bocchio‐Chiavetto, L., Bonetti, M., Bonvicini, C., Cotelli, M., Ghidoni, R., Paghera, B., Zanetti, O. O., et al. (2012) · Journal of Neurology · doi:10.1007/s00415-012-6694-0 · Cited by 55 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Alzheimer's disease: experimental models and reality
Drummond, E., & Wisniewski, T. (2017) · Acta Neuropathologica · doi:10.1007/s00401-016-1662-x · Cited by 810 · see citing works
Advance of sporadic Alzheimer's disease animal models
Zhang, L., Chen, C., Mak, M. S., Lu, J., Wu, Z., Chen, Q., Han, Y., Li, Y., & Pi, R. (2020) · Medicinal Research Reviews · doi:10.1002/med.21624 · Cited by 116 · see citing works
Prati, F., Cavalli, A., & Bolognesi, M. (2016) · Molecules · doi:10.3390/molecules21040466 · Cited by 110 · see citing works
Vojtechova, I., Machacek, T., Kristofikova, Z., Stuchlik, A., & Petrasek, T. (2022) · PLOS Pathogens · doi:10.1371/journal.ppat.1010929 · Cited by 92 · see citing works
Hargis, K. E., & Blalock, E. M. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.05.007 · Cited by 90 · see citing works
- Authors
- Banik, A., Brown, R. E., Bamburg, J., Lahiri, D. K., Khurana, D., Friedland, R. P., Chen, W., Ding, Y., Mudher, A., Padjen, A. L., Mukaetova-Ladinska, E., Ihara, M., Srivastava, S., Padma Srivastava, M. V., Masters, C. L., Kalaria, R. N., & Anand, A.
- Affiliations
- Post Graduate Institute of Medical Education and Research (IN)
- Dalhousie University (CA)
- Colorado State University (US)
- Indiana University Indianapolis (US)
- University of Louisville (US)
- University of Pittsburgh (US)
- University of Southampton (GB)
- McGill University (CA)
- Institute of Neuroscience, Newcastle University, NIHR Biomedical Research Building, Campus for Ageing and Vitality, Newcastle upon Tyne, UK
- National Cerebral and Cardiovascular Center (JP)
- Central Drug Research Institute (IN)
- Department of Neurology, Neurosciences Centre, All India Institute of Medical Sciences, New Delhi, India
- Mental Health Research Institute (AU)
- Newcastle University (GB)
- Corresponding author
- Kalaria, Raj N.
- Anand, Akshay
- ORCID
- Venue
- Journal of Alzheimer’s Disease
- Publisher
- SAGE Publications
- Published
- 2015-08-11
- Volume
- 47
- Issue
- 4
- Pages
- 815-843
- ISSN
- 1387-2877 (ISSN-L)
- 1875-8908
- OpenAlex
- W2177793807
- Cited by
- 102
- References
- 267
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 9 · 2023: 9 · 2022: 14 · 2021: 20 · 2020: 11 · 2019: 10 · 2018: 6 · 2017: 3 · 2016: 6 · 2015: 1
- FWCI
- 0.65
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Locations
- Journal of Alzheimer s Disease (publishedVersion)
- PubMed (publishedVersion)
- Newcastle University ePrints (Newcastle Univesity)
- Funders
- Japan Society for the Promotion of Science (15H04271)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
- Keywords
- Alzheimer's disease, translational research
- MeSH terms
- Alzheimer Disease, Animals, Clinical Trials as Topic, Humans, Translational Research, Biomedical
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review