Iatrogenic Alzheimer's disease in recipients of cadaveric pituitary-derived growth hormone.
Journal
Nature medicine
ISSN: 1546-170X
Titre abrégé: Nat Med
Pays: United States
ID NLM: 9502015
Informations de publication
Date de publication:
Feb 2024
Feb 2024
Historique:
received:
03
10
2023
accepted:
17
11
2023
medline:
22
2
2024
pubmed:
30
1
2024
entrez:
29
1
2024
Statut:
ppublish
Résumé
Alzheimer's disease (AD) is characterized pathologically by amyloid-beta (Aβ) deposition in brain parenchyma and blood vessels (as cerebral amyloid angiopathy (CAA)) and by neurofibrillary tangles of hyperphosphorylated tau. Compelling genetic and biomarker evidence supports Aβ as the root cause of AD. We previously reported human transmission of Aβ pathology and CAA in relatively young adults who had died of iatrogenic Creutzfeldt-Jakob disease (iCJD) after childhood treatment with cadaver-derived pituitary growth hormone (c-hGH) contaminated with both CJD prions and Aβ seeds. This raised the possibility that c-hGH recipients who did not die from iCJD may eventually develop AD. Here we describe recipients who developed dementia and biomarker changes within the phenotypic spectrum of AD, suggesting that AD, like CJD, has environmentally acquired (iatrogenic) forms as well as late-onset sporadic and early-onset inherited forms. Although iatrogenic AD may be rare, and there is no suggestion that Aβ can be transmitted between individuals in activities of daily life, its recognition emphasizes the need to review measures to prevent accidental transmissions via other medical and surgical procedures. As propagating Aβ assemblies may exhibit structural diversity akin to conventional prions, it is possible that therapeutic strategies targeting disease-related assemblies may lead to selection of minor components and development of resistance.
Identifiants
pubmed: 38287166
doi: 10.1038/s41591-023-02729-2
pii: 10.1038/s41591-023-02729-2
pmc: PMC10878974
doi:
Substances chimiques
Growth Hormone
9002-72-6
Amyloid beta-Peptides
0
Prions
0
Biomarkers
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
394-402Subventions
Organisme : Medical Research Council
ID : MC_UU_00024/9
Pays : United Kingdom
Informations de copyright
© 2024. The Author(s).
Références
Collinge, J. Mammalian prions and their wider relevance in neurodegenerative diseases. Nature 539, 217–226 (2016).
pubmed: 27830781
Manka, S. W. et al. A structural basis for prion strain diversity. Nat. Chem. Biol. 19, 607–613 (2023).
pubmed: 36646960
pmcid: 10154210
Collinge, J. et al. Kuru in the 21st century—an acquired human prion disease with very long incubation periods. Lancet 367, 2068–2074 (2006).
pubmed: 16798390
Mead, S. et al. Balancing selection at the prion protein gene consistent with prehistoric kurulike epidemics. Science 300, 640–643 (2003).
pubmed: 12690204
Collinge, J., Sidle, K. C., Meads, J., Ironside, J. & Hill, A. F. Molecular analysis of prion strain variation and the aetiology of ‘new variant’ CJD. Nature 383, 685–690 (1996).
pubmed: 8878476
Will, R. G. et al. A new variant of Creutzfeldt–Jakob disease in the UK. Lancet 347, 921–925 (1996).
pubmed: 8598754
Wickner, R. B. [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 264, 566–569 (1994).
pubmed: 7909170
Jucker, M. & Walker, L. C. Self-propagation of pathogenic protein aggregates in neurodegenerative diseases. Nature 501, 45–51 (2013).
pubmed: 24005412
pmcid: 3963807
Baker, H. F., Ridley, R. M., Duchen, L. W., Crow, T. J. & Bruton, C. J. Induction of β(A4)-amyloid in primates by injection of Alzheimer’s disease brain homogenate. Comparison with transmission of spongiform encephalopathy. Mol. Neurobiol. 8, 25–39 (1994).
pubmed: 8086126
Jucker, M. & Walker, L. C. Propagation and spread of pathogenic protein assemblies in neurodegenerative diseases. Nat. Neurosci. 21, 1341–1349 (2018).
pubmed: 30258241
pmcid: 6375686
Jaunmuktane, Z. et al. Evidence for human transmission of amyloid-β pathology and cerebral amyloid angiopathy. Nature 525, 247–250 (2015).
pubmed: 26354483
Purro, S. A. et al. Transmission of amyloid-β protein pathology from cadaveric pituitary growth hormone. Nature 564, 415–419 (2018).
pubmed: 30546139
pmcid: 6708408
Swerdlow, A. J., Higgins, C. D., Adlard, P., Jones, M. E. & Preece, M. A. Creutzfeldt–Jakob disease in United Kingdom patients treated with human pituitary growth hormone. Neurology 61, 783–791 (2003).
pubmed: 14504321
Brown, P. et al. Iatrogenic Creutzfeldt–Jakob disease, final assessment. Emerg. Infect. Dis. 18, 901–907 (2012).
pubmed: 22607808
pmcid: 3358170
National CJD Surveillance Unit. NCJDSU Annual Report 2022. https://www.cjd.ed.ac.uk/sites/default/files/report31.pdf (Univ. of Edinburgh, 2022).
Cali, I. et al. Iatrogenic Creutzfeldt–Jakob disease with amyloid-β pathology: an international study. Acta Neuropathol. Commun. 6, 5 (2018).
pubmed: 29310723
pmcid: 5759292
Ritchie, D. L. et al. Amyloid-β accumulation in the CNS in human growth hormone recipients in the UK. Acta Neuropathol. 134, 221–240 (2017).
pubmed: 28349199
pmcid: 5508038
Duyckaerts, C. et al. Neuropathology of iatrogenic Creutzfeldt–Jakob disease and immunoassay of French cadaver-sourced growth hormone batches suggest possible transmission of tauopathy and long incubation periods for the transmission of Aβ pathology. Acta Neuropathol. 135, 201–212 (2018).
pubmed: 29209767
Kovacs, G. G. et al. Dura mater is a potential source of Aβ seeds. Acta Neuropathol. 131, 911–923 (2016).
pubmed: 27016065
pmcid: 4865536
Hamaguchi, T. et al. Significant association of cadaveric dura mater grafting with subpial Aβ deposition and meningeal amyloid angiopathy. Acta Neuropathol. 132, 313–315 (2016).
pubmed: 27314593
Iwasaki, Y. et al. Autopsied case of non-plaque-type dura mater graft-associated Creutzfeldt–Jakob disease presenting with extensive amyloid-β deposition. Neuropathology 38, 549–556 (2018).
pubmed: 30084170
Frontzek, K., Lutz, M. I., Aguzzi, A., Kovacs, G. G. & Budka, H. Amyloid-beta pathology and cerebral amyloid angiopathy are frequent in iatrogenic Creutzfeldt–Jakob disease after dural grafting. Swiss Med. Wkly 146, w14287 (2016).
pubmed: 26812492
Herve, D. et al. Fatal Aβ cerebral amyloid angiopathy 4 decades after a dural graft at the age of 2 years. Acta Neuropathol. 135, 801–803 (2018).
pubmed: 29508058
Jaunmuktane, Z. et al. Evidence of amyloid-β cerebral amyloid angiopathy transmission through neurosurgery. Acta Neuropathol. 135, 671–679 (2018).
pubmed: 29450646
pmcid: 5904220
Banerjee, G. et al. The increasing impact of cerebral amyloid angiopathy: essential new insights for clinical practice. J. Neurol. Neurosurg. Psychiatry 88, 982–994 (2017).
pubmed: 28844070
Banerjee, G. et al. Iatrogenic cerebral amyloid angiopathy: an emerging clinical phenomenon. J. Neurol. Neurosurg. Psychiatry 93, 693–700 (2022).
Brown, P. et al. Iatrogenic Creutzfeldt–Jakob disease at the millennium. Neurology 55, 1075–1081 (2000).
pubmed: 11071481
Thompson, A. G. et al. The Medical Research Council prion disease rating scale: a new outcome measure for prion disease therapeutic trials developed and validated using systematic observational studies. Brain 136, 1116–1127 (2013).
pubmed: 23550114
Rudge, P. et al. Iatrogenic CJD due to pituitary-derived growth hormone with genetically determined incubation times of up to 40 years. Brain 138, 3386–3399 (2015).
pubmed: 26268531
pmcid: 4620512
McKhann, G. M. 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. 7, 263–269 (2011).
pubmed: 21514250
pmcid: 3312024
American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders: DSM-V-TR (American Psychiatric Association, 2013).
Jack, C. R. Jr et al. NIA-AA research framework: toward a biological definition of Alzheimer’s disease. Alzheimers Dement. 14, 535–562 (2018).
pubmed: 29653606
pmcid: 5958625
Thal, D. R., Rub, U., Orantes, M. & Braak, H. Phases of Aβ-deposition in the human brain and its relevance for the development of AD. Neurology 58, 1791–1800 (2002).
pubmed: 12084879
Mirra, S. S. et al. The Consortium to Establish a Registry for Alzheimer’s Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer’s disease. Neurology 41, 479–486 (1991).
pubmed: 2011243
Van Hout, C. V. et al. Exome sequencing and characterization of 49,960 individuals in the UK Biobank. Nature 586, 749–756 (2020).
pubmed: 33087929
pmcid: 7759458
Collins, R. L. et al. A structural variation reference for medical and population genetics. Nature 581, 444–451 (2020).
pubmed: 32461652
pmcid: 7334194
Braak, H. & Braak, E. Frequency of stages of Alzheimer-related lesions in different age categories. Neurobiol. Aging 18, 351–357 (1997).
pubmed: 9330961
Braak, H., Thal, D. R., Ghebremedhin, E. & Del Tredici, K. Stages of the pathologic process in Alzheimer disease: age categories from 1 to 100 years. J. Neuropathol. Exp. Neurol. 70, 960–969 (2011).
pubmed: 22002422
Holland, A. J. Ageing and learning disability. Br. J. Psychiatry 176, 26–31 (2000).
pubmed: 10789322
Strydom, A., Livingston, G., King, M. & Hassiotis, A. Prevalence of dementia in intellectual disability using different diagnostic criteria. Br. J. Psychiatry 191, 150–157 (2007).
pubmed: 17666500
Strydom, A., Chan, T., King, M., Hassiotis, A. & Livingston, G. Incidence of dementia in older adults with intellectual disabilities. Res. Dev. Disabil. 34, 1881–1885 (2013).
pubmed: 23578903
Takenoshita, S. et al. Prevalence of dementia in people with intellectual disabilities: cross-sectional study. Int. J. Geriatr. Psychiatry 35, 414–422 (2020).
pubmed: 31894597
Dementia and People with Intellectual Disabilities (British Psychological Society, 2015).
Webb, E. A. et al. Effect of growth hormone deficiency on brain structure, motor function and cognition. Brain 135, 216–227 (2012).
pubmed: 22120144
Nyberg, F. & Hallberg, M. Growth hormone and cognitive function. Nat. Rev. Endocrinol. 9, 357–365 (2013).
pubmed: 23629538
Falleti, M. G., Maruff, P., Burman, P. & Harris, A. The effects of growth hormone (GH) deficiency and GH replacement on cognitive performance in adults: a meta-analysis of the current literature. Psychoneuroendocrinology 31, 681–691 (2006).
pubmed: 16621325
Cramer, C. K. et al. Mild cognitive impairment in long-term brain tumor survivors following brain irradiation. J. Neurooncol. 141, 235–244 (2019).
pubmed: 30406339
Kokmen, E., Beard, C. M., Bergstralh, E., Anderson, J. A. & Earle, J. D. Alzheimer’s disease and prior therapeutic radiation exposure: a case–control study. Neurology 40, 1376–1379 (1990).
pubmed: 2392221
Duffner, P. K. Risk factors for cognitive decline in children treated for brain tumors. Eur. J. Paediatr. Neurol. 14, 106–115 (2010).
pubmed: 19931477
Sugihara, S., Ogawa, A., Nakazato, Y. & Yamaguchi, H. Cerebral beta amyloid deposition in patients with malignant neoplasms: its prevalence with aging and effects of radiation therapy on vascular amyloid. Acta Neuropathol. 90, 135–141 (1995).
pubmed: 7484088
Kalm, M. et al. Neurochemical evidence of potential neurotoxicity after prophylactic cranial irradiation. Int. J. Radiat. Oncol. Biol. Phys. 89, 607–614 (2014).
pubmed: 24803034
Huang, A. J., Kornguth, D. & Kornguth, S. Cognitive decline secondary to therapeutic brain radiation—similarities and differences to traumatic brain injury. Brain Sci. 9, 97 (2019).
Roberts, G. W., Gentleman, S. M., Lynch, A. & Graham, D. I. βA4 amyloid protein deposition in brain after head trauma. Lancet 338, 1422–1423 (1991).
pubmed: 1683421
Roberts, G. W. et al. Beta amyloid protein deposition in the brain after severe head injury: implications for the pathogenesis of Alzheimer’s disease. J. Neurol. Neurosurg. Psychiatry 57, 419–425 (1994).
pubmed: 8163989
pmcid: 1072869
Chen, X. H., Johnson, V. E., Uryu, K., Trojanowski, J. Q. & Smith, D. H. A lack of amyloid β plaques despite persistent accumulation of amyloid β in axons of long-term survivors of traumatic brain injury. Brain Pathol. 19, 214–223 (2009).
pubmed: 18492093
Hong, Y. T. et al. Amyloid imaging with carbon 11-labeled Pittsburgh compound B for traumatic brain injury. JAMA Neurol. 71, 23–31 (2014).
pubmed: 24217171
pmcid: 4084932
Liu, C. C., Liu, C. C., Kanekiyo, T., Xu, H. & Bu, G. Apolipoprotein E and Alzheimer disease: risk, mechanisms and therapy. Nat. Rev. Neurol. 9, 106–118 (2013).
pubmed: 23296339
pmcid: 3726719
Collinge, J. Molecular neurology of prion disease. J. Neurol. Neurosurg. Psychiatry 76, 906–919 (2005).
pubmed: 15965195
pmcid: 1739714
Eisele, Y. S. et al. Multiple factors contribute to the peripheral induction of cerebral β-amyloidosis. J. Neurosci. 34, 10264–10273 (2014).
pubmed: 25080588
pmcid: 6608275
Eisele, Y. S. et al. Peripherally applied Aβ-containing inoculates induce cerebral β-amyloidosis. Science 330, 980–982 (2010).
pubmed: 20966215
pmcid: 3233904
Ryan, N. S. & Rossor, M. N. Correlating familial Alzheimer’s disease gene mutations with clinical phenotype. Biomark. Med. 4, 99–112 (2010).
pubmed: 20387306
Ryan, N. S. et al. Clinical phenotype and genetic associations in autosomal dominant familial Alzheimer’s disease: a case series. Lancet Neurol. 15, 1326–1335 (2016).
pubmed: 27777022
Collinge, J. & Clarke, A. R. A general model of prion strains and their pathogenicity. Science 318, 930–936 (2007).
pubmed: 17991853
Bartz, J. C. Environmental and host factors that contribute to prion strain evolution. Acta Neuropathol. 142, 5–16 (2021).
pubmed: 33899132
pmcid: 8932343
Qiang, W., Yau, W. M., Lu, J. X., Collinge, J. & Tycko, R. Structural variation in amyloid-β fibrils from Alzheimer’s disease clinical subtypes. Nature 541, 217–221 (2017).
pubmed: 28052060
pmcid: 5233555
Yang, Y. et al. Cryo-EM structures of amyloid-β 42 filaments from human brains. Science 375, 167–172 (2022).
pubmed: 35025654
pmcid: 7612234
Jakel, L., De Kort, A. M., Klijn, C. J. M., Schreuder, F. & Verbeek, M. M. Prevalence of cerebral amyloid angiopathy: a systematic review and meta-analysis. Alzheimers Dement. 18, 10–28 (2022).
pubmed: 34057813
Sandberg, M. K., Al-Doujaily, H., Sharps, B., Clarke, A. R. & Collinge, J. Prion propagation and toxicity in vivo occur in two distinct mechanistic phases. Nature 470, 540–542 (2011).
pubmed: 21350487
Lauwers, E. et al. Potential human transmission of amyloid β pathology: surveillance and risks. Lancet Neurol. 19, 872–878 (2020).
pubmed: 32949547
Asher, D. M. et al. Risk of transmissibility from neurodegenerative disease-associated proteins: experimental knowns and unknowns. J. Neuropathol. Exp. Neurol. 79, 1141–1146 (2020).
pubmed: 33000167
pmcid: 7577514
Li, J., Browning, S., Mahal, S. P., Oelschlegel, A. M. & Weissmann, C. Darwinian evolution of prions in cell culture. Science 327, 869–872 (2010).
pubmed: 20044542
Sandberg, M. K. et al. Prion neuropathology follows the accumulation of alternate prion protein isoforms after infective titre has peaked. Nat. Commun. 5, 4347 (2014).
Oelschlegel, A. M. & Weissmann, C. Acquisition of drug resistance and dependence by prions. PLoS Pathog. 9, e1003158 (2013).
pubmed: 23408888
pmcid: 3567182