Prion-specific and surrogate CSF biomarkers in Creutzfeldt-Jakob disease: diagnostic accuracy in relation to molecular subtypes and analysis of neuropathological correlates of p-tau and Aβ42 levels

Acta Neuropathologica

Volumn 133, Issue 4, 2017, Pages 559-578

  Lattanzio, Francesca ^a   Abu Rumeileh, Samir ^a   Franceschini, Alessia ^a   Kai, Hideaki ^a,e   Amore, Giulia ^a   Poggiolini, Ilaria ^a   Rossi, Marcello ^b   Baiardi, Simone ^a   McGuire, Lynne ^c   Ladogana, Anna ^d   Pocchiari, Maurizio ^d   Green, Alison ^c   Capellari, Sabina ^a,b   Parchi, Piero ^a,b  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b IRCCS   (Italy)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^e TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Alzheimer s disease; Amyloid beta; Biomarkers; Human prions; Protease sensitive prionopathy; RT QuIC; Tauopathy

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; BIOLOGICAL MARKER; PRION PROTEIN; PROTEIN 14 3 3; TAU PROTEIN; AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (1-42); MAPT PROTEIN, HUMAN; PEPTIDE FRAGMENT;

ADULT; ARTICLE; CEREBROSPINAL FLUID; CREUTZFELDT JAKOB DISEASE; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST ACCURACY STUDY; DIAGNOSTIC VALUE; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MIDDLE AGED; NEUROPATHOLOGY; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN CEREBROSPINAL FLUID LEVEL; PROTEIN DETERMINATION; REAL TIME QUAKING INDUCED PRION CONVERSION ASSAY; RECEIVER OPERATING CHARACTERISTIC; SENSITIVITY AND SPECIFICITY; AGED; BRAIN; DIFFERENTIAL DIAGNOSIS; FEMALE; FOLLOW UP; IMMUNOHISTOCHEMISTRY; LUMBAR PUNCTURE; MALE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SPECIMEN HANDLING; TIME FACTOR;

14-3-3 PROTEINS; AGED; AMYLOID BETA-PEPTIDES; BIOMARKERS; BRAIN; CREUTZFELDT-JAKOB SYNDROME; DIAGNOSIS, DIFFERENTIAL; FEMALE; FOLLOW-UP STUDIES; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PRION PROTEINS; SENSITIVITY AND SPECIFICITY; SPECIMEN HANDLING; SPINAL PUNCTURE; TAU PROTEINS; TIME FACTORS;

EID: 85012864946     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-017-1683-0     Document Type: Article

References (81)

1. Abu Rumeileh S, Lattanzio F, Stanzani Maserati M, Rizzi R, Capellari S, Parchi P (2017) Diagnostic Accuracy of a Combined Analysis of Cerebrospinal Fluid t-PrP, t-tau, p-tau, and Aβ42 in the Differential Diagnosis of Creutzfeldt-Jakob Disease from Alzheimer’s Disease with Emphasis on Atypical Disease Variants. J Alzheimers Dis 55(4):1471–1480. doi:10.3233/JAD-160740
2. Alafuzoff I, Arzberger T, Al-Sarraj S, Bodi I, Bogdanovic N, Braak H, Bugiani O, Del-Tredici K, Ferrer I, Gelpi E, Giaccone G, Graeber MB, Ince P, Kamphorst W, King A, Korkolopoulou P, Kovács GG, Larionov S, Meyronet D, Monoranu C, Parchi P, Patsouris E, Roggendorf W, Seilhean D, Tagliavini F, Stadelmann C, Streichenberger N, Thal DR, Wharton SB, Kretzschmar H (2008) Staging of neurofibrillary pathology in Alzheimer’s disease: a study of the BrainNet Europe Consortium. Brain Pathol 18(4):484–496. doi:10.1111/j.1750-3639.2008.00147.x
3. Alafuzoff I, Thal DR, Arzberger T, Bogdanovic N, Al-Sarraj S, Bodi I, Boluda S, Bugiani O, Duyckaerts C, Gelpi E, Gentleman S, Giaccone G, Graeber M, Hortobagyi T, Höftberger R, Ince P, Ironside JW, Kavantzas N, King A, Korkolopoulou P, Kovács GG, Meyronet D, Monoranu C, Nilsson T, Parchi P, Patsouris E, Pikkarainen M, Revesz T, Rozemuller A, Seilhean D, Schulz-Schaeffer W, Streichenberger N, Wharton SB, Kretzschmar H (2009) Assessment of beta-amyloid deposits in human brain: a study of the BrainNet Europe Consortium. Acta Neuropathol 117(3):309–320. doi:10.1007/s00401-009-0485-4
4. Assar H, Topakian R, Weis S, Rahimi J, Trenkler J, Höftberger R, Aboulenein-Djamshidian F, Ströbel T, Budka H, Yull H, Head MW, Ironside JW, Kovacs GG (2015) A case of variably protease-sensitive prionopathy treated with doxycyclin. J Neurol Neurosurg Psychiatry 86(7):816–818. doi:10.1136/jnnp-2014-309871
5. Atarashi R, Satoh K, Sano K, Fuse T, Yamaguchi N, Ishibashi D, Matsubara T, Nakagaki T, Yamanaka H, Shirabe S, Yamada M, Mizusawa H, Kitamoto T, Klug G, McGlade A, Collins SJ, Nishida N (2011) Ultrasensitive human prion detection in cerebrospinal fluid by real-time quaking-induced conversion. Nat Med 17(2):175–178. doi:10.1038/nm.2294
6. Baldeiras IE, Ribeiro MH, Pacheco P, Machado A, Santana I, Cunha L, Oliveira CR (2009) Diagnostic value of CSF protein profile in a Portuguese population of sCJD patients. J Neurol 256(9):1540–1550. doi:10.1007/s00415-009-5160-0
7. Beck J, Pittman A, Adamson G, Campbell T, Kenny J, Houlden H, Rohrer JD, de Silva R, Shoai M, Uphill J, Poulter M, Hardy J, Mummery CJ, Warren JD, Schott JM, Fox NC, Rossor MN, Collinge J, Mead S (2014) Validation of next-generation sequencing technologies in genetic diagnosis of dementia. Neurobiol Aging 35(1):261–265. doi:10.1016/j.neurobiolaging.2013.07.017
8. Bertrand A, Brandel JP, Grignon Y, Sazdovitch V, Seilhean D, Faucheux B, Privat N, Brault JL, Vital A, Uro-Coste E, Pluot M, Chapon F, Maurage CA, Letournel F, Vespignani H, Place G, Degos CF, Peoc’h K, Haïk S, Hauw JJ (2009) Wernicke encephalopathy and Creutzfeldt-Jakob disease. J Neurol 256(6):904–909. doi:10.1007/s00415-009-5038-1
9. Blennow K, Johansson A, Zetterberg H (2005) Diagnostic value of 14-3-3beta immunoblot and T-tau/P-tau ratio in clinically suspected Creutzfeldt-Jakob disease. Int J Mol Med 16(6):1147–1149
10. Braak H, Alafuzoff I, Arzberger T, Kretzschmar H, Del Tredici K (2006) Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol 112(4):389–404
11. Buerger K, Ewers M, Pirttilä T, Zinkowski R, Alafuzoff I, Teipel SJ, DeBernardis J, Kerkman D, McCulloch C, Soininen H, Hampel H (2006) CSF phosphorylated tau protein correlates with neocortical neurofibrillary pathology in Alzheimer’s disease. Brain 129(Pt 11):3035–3041
12. Buerger K, Otto M, Teipel SJ, Zinkowski R, Blennow K, DeBernardis J, Kerkman D, Schröder J, Schönknecht P, Cepek L, McCulloch C, Möller HJ, Wiltfang J, Kretzschmar H, Hampel H (2006) Dissociation between CSF total tau and tau protein phosphorylated at threonine 231 in Creutzfeldt-Jakob disease. Neurobiol Aging 27(1):10–15
13. Caobelli F, Cobelli M, Pizzocaro C, Pavia M, Magnaldi S, Guerra UP (2015) The role of neuroimaging in evaluating patients affected by Creutzfeldt-Jakob disease: a systematic review of the literature. J Neuroimaging 25(1):2–13. doi:10.1111/jon.12098
14. Capellari S, Strammiello R, Saverioni D, Kretzschmar H, Parchi P (2011) Genetic Creutzfeldt Jakob disease and fatal familial insomnia: insights into phenotypic variability and disease pathogenesis. Acta Neuropathol 121(1):21–37. doi:10.1007/s00401-010-0760-4
15. Castellani RJ, Colucci M, Xie Z, Zou W, Li C, Parchi P, Capellari S, Pastore M, Rahbar MH, Chen SG, Gambetti P (2004) Sensitivity of 14-3-3 protein test varies in subtypes of sporadic Creutzfeldt-Jakob disease. Neurology 63(3):436–442
16. Chitravas N, Jung RS, Kofskey DM, Blevins JE, Gambetti P, Leigh RJ, Cohen ML (2011) Treatable neurological disorders misdiagnosed as Creutzfeldt-Jakob disease. Ann Neurol 70(3):437–444. doi:10.1002/ana.22454
17. Chohan G, Pennington C, Mackenzie JM, Andrews M, Everington D, Will RG, Knight RS, Green AJ (2010) The role of cerebrospinal fluid 14-3-3 and other proteins in the diagnosis of sporadic Creutzfeldt-Jakob disease in the UK: a 10-year review. J Neurol Neurosurg Psychiatry 81(11):1243–1248. doi:10.1136/jnnp.2009.197962
18. Coulthart MB, Jansen GH, Olsen E, Godal DL, Connolly T, Choi BC, Wang Z, Cashman NR (2011) Diagnostic accuracy of cerebrospinal fluid protein markers for sporadic Creutzfeldt-Jakob disease in Canada: a 6-year prospective study. BMC Neurol 11:133. doi:10.1186/1471-2377-11-133
19. Cramm M, Schmitz M, Karch A, Zafar S, Varges D, Mitrova E, Schroeder B, Raeber A, Kuhn F, Zerr I (2015) Characteristic CSF prion seeding efficiency in humans with prion diseases. Mol Neurobiol 51(1):396–405. doi:10.1007/s12035-014-8709-6
20. Crary JF, Trojanowski JQ, Schneider JA, Abisambra JF, Abner EL, Alafuzoff I, Arnold SE, Attems J, Beach TG, Bigio EH, Cairns NJ, Dickson DW, Gearing M, Grinberg LT, Hof PR, Hyman BT, Jellinger K, Jicha GA, Kovacs GG, Knopman DS, Kofler J, Kukull WA, Mackenzie IR, Masliah E, McKee A, Montine TJ, Murray ME, Neltner JH, Santa-Maria I, Seeley WW, Serrano-Pozo A, Shelanski ML, Stein T, Takao M, Thal DR, Toledo JB, Troncoso JC, Vonsattel JP, White CL 3rd, Wisniewski T, Woltjer RL, Yamada M, Nelson PT (2014) Primary age-related tauopathy (PART): a common pathology associated with human aging. Acta Neuropathol 128(6):755–766. doi:10.1007/s00401-014-1349-0
21. Dorey A, Tholance Y, Vighetto A, Perret-Liaudet A, Lachman I, Krolak-Salmon P, Wagner U, Struyfs H, De Deyn PP, El-Moualij B, Zorzi W, Meyronet D, Streichenberger N, Engelborghs S, Kovacs GG, Quadrio I (2015) Association of cerebrospinal fluid prion protein levels and the distinction between Alzheimer disease and Creutzfeldt-Jakob disease. JAMA Neurol 72(3):267–275
22. Geschwind MD, Martindale J, Miller D, DeArmond SJ, Uyehara-Lock J, Gaskin D, Kramer JH, Barbaro NM, Miller BL (2003) Challenging the clinical utility of the 14-3-3 protein for the diagnosis of sporadic Creutzfeldt-Jakob disease. Arch Neurol 60(6):813–816
23. Geschwind MD, Shu H, Haman A, Sejvar JJ, Miller BL (2008) Rapidly progressive dementia. Ann Neurol 64(1):97–108. doi:10.1002/ana.21430
24. Geschwind MD, Tan KM, Lennon VA, Barajas Jr RF, Haman A, Klein CJ, Josephson SA, Pittock SJ (2008) Voltage-gated potassium channel autoimmunity mimicking creutzfeldt-jakob disease. Arch Neurol 65(10):1341–1346. doi:10.1001/archneur.65.10.1341
25. Ghetti B, Tagliavini F, Kovacs GG, Piccardo P (2011) Gerstmann–Sträussler–Scheinker Disease. In: Dickson D, Weller RO (eds) Neurodegeneration: the molecular pathology of dementia and movement disorders, 2nd edn. Wiley-Blackwell, New York, pp 364–377
26. Giaccone G, Tagliavini F, Verga L, Frangione B, Farlow MR, Bugiani O, Ghetti B (1990) Neurofibrillary tangles of the Indiana kindred of Gerstmann-Sträussler-Scheinker disease share antigenic determinants with those of Alzheimer disease. Brain Res 530(2):325–329
27. Giaccone G, Mangieri M, Capobianco R, Limido L, Hauw JJ, Haïk S, Fociani P, Bugiani O, Tagliavini F (2008) Tauopathy in human and experimental variant Creutzfeldt-Jakob disease. Neurobiol Aging 29(12):1864–1873
28. Gmitterová K, Heinemann U, Krasnianski A, Gawinecka J, Zerr I (2016) Cerebrospinal fluid markers in the differentiation of molecular subtypes of sporadic Creutzfeldt-Jakob disease. Eur J Neurol 23(6):1126–1133. doi:10.1111/ene.12991
29. Goodall CA, Head MW, Everington D, Ironside JW, Knight RS, Green AJ (2006) Raised CSF phospho-tau concentrations in variant Creutzfeldt-Jakob disease: diagnostic and pathological implications. J Neurol Neurosurg Psychiatry 77(1):89–91
30. Hamlin C, Puoti G, Berri S, Sting E, Harris C, Cohen M, Spear C, Bizzi A, Debanne SM, Rowland DY (2012) A comparison of tau and 14-3-3 protein in the diagnosis of Creutzfeldt-Jakob disease. Neurology 79(6):547–552. doi:10.1212/WNL.0b013e318263565f
31. Head MW, Lowrie S, Chohan G, Knight R, Scoones DJ, Ironside JW (2010) Variably protease-sensitive prionopathy in a PRNP codon 129 heterozygous UK patient with co-existing tau, α synuclein and Aβ pathology. Acta Neuropathol 120(6):821–823. doi:10.1007/s00401-010-0766
32. Jansen C, Parchi P, Capellari S, Ibrahim-Verbaas CA, Schuur M, Strammiello R, Corrado P, Bishop MT, van Gool WA, Verbeek MM, Baas F, van Saane W, Spliet WG, Jansen GH, van Duijn CM, Rozemuller AJ (2012) Human prion diseases in the Netherlands (1998-2009): clinical, genetic and molecular aspects. PLoS One 7(4):e36333. doi:10.1371/journal.pone.0036333
33. Josephs KA, Ahlskog JE, Parisi JE, Boeve BF, Crum BA, Giannini C, Petersen RC (2009) Rapidly progressive neurodegenerative dementias. Arch Neurol 66(2):201–207. doi:10.1001/archneurol.2008.534
34. Kapaki E, Kilidireas K, Paraskevas GP, Michalopoulou M, Patsouris E (2001) Highly increased CSF tau protein and decreased beta-amyloid (1–42) in sporadic CJD: a discrimination from Alzheimer’s disease? J Neurol Neurosurg Psychiatry 71(3):401–403
35. Karch A, Hermann P, Ponto C, Schmitz M, Arora A, Zafar S, Llorens F, Müller-Heine A, Zerr I (2015) Cerebrospinal fluid tau levels are a marker for molecular subtype in sporadic Creutzfeldt-Jakob disease. Neurobiol Aging 36(5):1964–1968. doi:10.1016/j.neurobiolaging.2015.01.021
36. Kovacs GG, Rahimi J, Ströbel T, Lutz MI, Regelsberger G, Streichenberger N, Perret-Liaudet A, Höftberger R, Liberski PP, Budka H, Sikorska B (2016) Tau Pathology in Creutzfeldt-Jakob Disease Revisited. Brain Pathol. doi:10.1111/bpa.12411
37. Kovacs GG, Ferrer I, Grinberg LT, Alafuzoff I, Attems J, Budka H, Cairns NJ, Crary JF, Duyckaerts C, Ghetti B, Halliday GM, Ironside JW, Love S, Mackenzie IR, Munoz DG, Murray ME, Nelson PT, Takahashi H, Trojanowski JQ, Ansorge O, Arzberger T, Baborie A, Beach TG, Bieniek KF, Bigio EH, Bodi I, Dugger BN, Feany M, Gelpi E, Gentleman SM, Giaccone G, Hatanpaa KJ, Heale R, Hof PR, Hofer M, Hortobágyi T, Jellinger K, Jicha GA, Ince P, Kofler J, Kövari E, Kril JJ, Mann DM, Matej R, McKee AC, McLean C, Milenkovic I, Montine TJ, Murayama S, Lee EB, Rahimi J, Rodriguez RD, Rozemüller A, Schneider JA, Schultz C, Seeley W, Seilhean D, Smith C, Tagliavini F, Takao M, Thal DR, Toledo JB, Tolnay M, Troncoso JC, Vinters HV, Weis S, Wharton SB, White CL 3rd, Wisniewski T, Woulfe JM, Yamada M, Dickson DW (2016) Aging-related tau astrogliopathy (ARTAG): harmonized evaluation strategy. Acta Neuropathol 131(1):87–102. doi:10.1007/s00401-015-1509-x
38. Ladogana A, Sanchez-Juan P, Mitrová E, Green A, Cuadrado-Corrales N, Sánchez-Valle R, Koscova S, Aguzzi A, Sklaviadis T, Kulczycki J, Gawinecka J, Saiz A, Calero M, van Duijn CM, Pocchiari M, Knight R, Zerr I (2009) Cerebrospinal fluid biomarkers in human genetic transmissible spongiform encephalopathies. J Neurol 256(10):1620–1628. doi:10.1007/s00415-009-5163-x
39. Lewczuk P, Matzen A, Blennow K, Parnetti L, Molinuevo JL, Eusebi P, Kornhuber J, Morris JC, Fagan AM (2017) Cerebrospinal Fluid Aβ42/40 Corresponds Better than Aβ42 to Amyloid PET in Alzheimer’s Disease. J Alzheimers Dis 55(2):813–822
40. Mattsson N, Andreasson U, Persson S, Carrillo MC, Collins S, Chalbot S, Cutler N, Dufour-Rainfray D, Fagan AM, Heegaard NH, Hsiung GY, Hyman B, Iqbal K, Kaeser SA, Lachno DR, Lleó A, Lewczuk P, Molinuevo JL, Parchi P, Regeniter A, Rissman RA, Rosenmann H, Sancesario G, Schröder J, Shaw LM, Teunissen CE, Trojanowski JQ, Vanderstichele H, Vandijck M, Verbeek MM, Zetterberg H, Blennow K, Alzheimer’s Association QC Program Work Group (2013) CSF biomarker variability in the Alzheimer’s Association quality control program. Alzheimers Dement 9(3):251–261. doi:10.1016/j.jalz.2013.01.010
41. McGuire LI, Peden AH, Orrú CD, Wilham JM, Appleford NE, Mallinson G, Andrews M, Head MW, Caughey B, Will RG, Knight RS, Green AJ (2012) Real time quaking-induced conversion analysis of cerebrospinal fluid in sporadic Creutzfeldt–Jakob disease. Ann Neurol 72(2):278–285. doi:10.1002/ana.23589
42. McGuire LI, Poleggi A, Poggiolini I, Suardi S, Grznarova K, Shi S, de Vil B, Sarros S, Satoh K, Cheng K, Cramm M, Fairfoul G, Schmitz M, Zerr I, Cras P, Equestre M, Tagliavini F, Atarashi R, Knox D, Collins S, Haïk S, Parchi P, Pocchiari M, Green A (2016) Cerebrospinal fluid real-time quaking-induced conversion is a robust and reliable test for sporadic creutzfeldt–jakob disease: An international study. Ann Neurol 80(1):160–165. doi:10.1002/ana.24679
43. McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack Jr CR, Kawas CH, Klunk WE, Koroshetz WJ, Manly JJ, Mayeux R, Mohs RC, Morris JC, Rossor MN, Scheltens P, Carrillo MC, Thies B, Weintraub S, Phelps CH (2011) 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(3):263–269. doi:10.1016/j.jalz.2011.03.005
44. Muayqil T, Gronseth G, Camicioli R (2012) Evidence-based guideline: diagnostic accuracy of CSF 14-3-3 protein in sporadic Creutzfeldt-Jakob disease: report of the guideline development subcommittee of the American Academy of Neurology. Neurology 79(14):1499–1506. doi:10.1212/WNL.0b013e31826d5fc3
45. Orrú CD, Bongianni M, Tonoli G, Ferrari S, Hughson AG, Groveman BR, Fiorini M, Pocchiari M, Monaco S, Caughey B, Zanusso G (2014) A test for Creutzfeldt-Jakob disease using nasal brushings. N Engl J Med 371(6):519–529. doi:10.1056/NEJMoa1315200
46. Orrú CD, Groveman BR, Hughson AG, Zanusso G, Coulthart MB, Caughey B (2015) Rapid and sensitive RT-QuIC detection of human Creutzfeldt-Jakob disease using cerebrospinal fluid. MBio 6(1):e02451–e02514. doi:10.1128/mBio.02451-14
47. Otto M, Esselmann H, Schulz-Shaeffer W, Neumann M, Schröter A, Ratzka P, Cepek L, Zerr I, Steinacker P, Windl O, Kornhuber J, Kretzschmar HA, Poser S, Wiltfang J (2000) Decreased beta-amyloid1-42 in cerebrospinal fluid of patients with Creutzfeldt-Jakob disease. Neurology 54(5):1099–1102
48. Otto M, Wiltfang J, Cepek L, Neumann M, Mollenhauer B, Steinacker P, Ciesielczyk B, Schulz-Schaeffer W, Kretzschmar HA, Poser S (2002) Tau protein and 14-3-3 protein in the differential diagnosis of Creutzfeldt-Jakob disease. Neurology 58(2):192–197
49. Parchi P, Castellani R, Capellari S, Ghetti B, Young K, Chen SG, Farlow M, Dickson DW, Sima AA, Trojanowski JQ, Petersen RB, Gambetti P (1996) Molecular basis of phenotypic variability in sporadic Creutzfeldt-Jakob disease. Ann Neurol 39(6):767–778
50. Parchi P, Giese A, Capellari S, Brown P, Schulz-Schaeffer W, Windl O, Zerr I, Budka H, Kopp N, Piccardo P, Poser S, Rojiani A, Streichemberger N, Julien J, Vital C, Ghetti B, Gambetti P, Kretzschmar H (1999) Classification of sporadic Creutzfeldt-Jakob disease based on molecular and phenotypic analysis of 300 subjects. Ann Neurol 46(2):224–233
51. Parchi P, Notari S, Weber P, Schimmel H, Budka H, Ferrer I, Haik S, Hauw JJ, Head MW, Ironside JW, Limido L, Rodriguez A, Ströbel T, Tagliavini F, Kretzschmar HA (2009) Inter-laboratory assessment of PrPSc typing in Creutzfeldt-Jakob disease: a Western blot study within the NeuroPrion Consortium. Brain Pathol 19(3):384–391. doi:10.1111/j.1750-3639.2008.00187.x
52. Parchi P, Strammiello R, Notari S, Giese A, Langeveld JP, Ladogana A, Zerr I, Roncaroli F, Cras P, Ghetti B, Pocchiari M, Kretzschmar H, Capellari S (2009) Incidence and spectrum of sporadic Creutzfeldt-Jakob disease variants with mixed phenotype and co-occurrence of PrPSc types: an updated classification. Acta Neuropathol 118(5):659–671. doi:10.1007/s00401-009-0585-1
53. Parchi P, Strammiello R, Giese A, Kretzschmar H (2011) Phenotypic variability of sporadic human prion disease and its molecular basis: past, present, and future. Acta Neuropathol 121(1):91–112. doi:10.1007/s00401-010-0779-6
54. Parchi P, de Boni L, Saverioni D, Cohen ML, Ferrer I, Gambetti P, Gelpi E, Giaccone G, Hauw JJ, Höftberger R, Ironside JW, Jansen C, Kovacs GG, Rozemuller A, Seilhean D, Tagliavini F, Giese A, Kretzschmar HA (2012) Consensus classification of human prion disease histotypes allows reliable identification of molecular subtypes: an inter-rater study among surveillance centres in Europe and USA. Acta Neuropathol 124(4):517–529. doi:10.1007/s00401-012-1002-8
55. Park JH, Choi YG, Lee YJ, Park SJ, Choi HS, Choi KC, Choi EK, Kim YS (2016) Real-time quaking-induced conversion analysis for the diagnosis of sporadic Creutzfeldt-Jakob disease in Korea. J Clin Neurol 12(1):101–106. doi:10.3988/jcn.2016.12.1.101
56. Plate A, Benninghoff J, Jansen GH, Wlasich E, Eigenbrod S, Drzezga A, Jansen NL, Kretzschmar HA, Bötzel K, Rujescu D, Danek A (2013) Atypical parkinsonism due to a D202N Gerstmann-Sträussler-Scheinker prion protein mutation: first in vivo diagnosed case. Mov Disord 28(2):241–244
57. Prusiner SB (1998) Prions. Proc Natl Acad Sci USA 95(23):13363–13383
58. Puoti G, Zou W, Kong Q, Tagliavini F, Parchi P, Gambetti P (2009) Tau protein in a novel prion disease with GSS features. J Neuropath Exp Neurol 68(5):553–554
59. Reiniger L, Lukic A, Linehan J, Rudge P, Collinge J, Mead S, Brandner S (2011) Tau, prions and Aβ: the triad of neurodegeneration. Acta Neuropathol 121(1):5–20. doi:10.1007/s00401-010-0691-0
60. Riemenschneider M, Wagenpfeil S, Vanderstichele H, Otto M, Wiltfang J, Kretzschmar H, Vanmechelen E, Förstl H, Kurz A (2003) Phospho-tau/total tau ratio in cerebrospinal fluid discriminates Creutzfeldt-Jakob disease from other dementias. Mol Psychiatry 8(3):343–347
61. Rosenbloom MH, Atri A (2011) The evaluation of rapidly progressive dementia. Neurologist 17(2):67–74. doi:10.1097/NRL.0b013e31820ba5e3
62. Sala I, Marquié M, Sánchez-Saudinós MB, Sánchez-Valle R, Alcolea D, Gómez-Ansón B, Gómez-Isla T, Blesa R, Lleó A (2012) Rapidly progressive dementia: experience in a tertiary care medical center. Alzheimer Dis Assoc Disord 26(3):267–271. doi:10.1097/WAD.0b013e3182368ed4
63. Sanchez-Juan P, Green A, Ladogana A, Cuadrado-Corrales N, Sáanchez-Valle R, Mitrováa E, Stoeck K, Sklaviadis T, Kulczycki J, Hess K, Bodemer M, Slivarichová D, Saiz A, Calero M, Ingrosso L, Knight R, Janssens AC, van Duijn CM, Zerr I (2006) CSF tests in the differential diagnosis of Creutzfeldt-Jakob disease. Neurology 67(4):637–643
64. Sano K, Satoh K, Atarashi R, Takashima H, Iwasaki Y, Yoshida M, Sanjo N, Murai H, Mizusawa H, Schmitz M, Zerr I, Kim YS, Nishida N (2013) Early detection of abnormal prion protein in genetic human prion diseases now possible using real-time QUIC assay. PLoS One 8(1):e54915. doi:10.1371/journal.pone.0054915
65. Seppälä TT, Nerg O, Koivisto AM, Rummukainen J, Puli L, Zetterberg H, Pyykkö OT, Helisalmi S, Alafuzoff I, Hiltunen M, Jääskeläinen JE, Rinne J, Soininen H, Leinonen V, Herukka SK (2012) CSF biomarkers for Alzheimer disease correlate with cortical brain biopsy findings. Neurology 78(20):1568–1575. doi:10.1212/WNL.0b013e3182563bd0
66. Sikorska B, Liberski PP, Sobów T, Budka H, Ironside JW (2009) Ultrastructural study of florid plaques in variant Creutzfeldt-Jakob disease: a comparison with amyloid plaques in kuru, sporadic Creutzfeldt-Jakob disease and Gerstmann-Sträussler-Scheinker disease. Neuropathol Appl Neurobiol 35(1):46–59. doi:10.1111/j.1365-2990.2008.00959.x
67. Skillbäck T, Rosén C, Asztely F, Mattsson N, Blennow K, Zetterberg H (2014) Diagnostic performance of cerebrospinal fluid total tau and phosphorylated tau in Creutzfeldt-Jakob disease: results from the Swedish Mortality Registry. JAMA Neurol 71(4):476–483
68. Stoeck K, Sanchez-Juan P, Gawinecka J, Green A, Ladogana A, Pocchiari M, Sanchez-Valle R, Mitrova E, Sklaviadis T, Kulczycki J, Slivarichova D, Saiz A, Calero M, Knight R, Aguzzi A, Laplanche JL, Peoc’h K, Schelzke G, Karch A, van Duijn CM, Zerr I (2012) Cerebrospinal fluid biomarker supported diagnosis of Creutzfeldt-Jakob disease and rapid dementias: a longitudinal multicentre study over 10 years. Brain 135(Pt 10):3051–3061
69. Strozyk D, Blennow K, White LR, Launer LJ (2003) CSF Abeta 42 levels correlate with amyloid-neuropathology in a population-based autopsy study. Neurology 60(4):652–656
70. Tapiola T, Alafuzoff I, Herukka SK, Parkkinen L, Hartikainen P, Soininen H, Pirttilä T (2009) Cerebrospinal fluid β-amyloid 42 and tau proteins as biomarkers of Alzheimer-type pathologic changes in the brain. Arch Neurol 66(3):382–389. doi:10.1001/archneurol.2008.596
71. Van Everbroeck B, Green AJ, Pals P, Martin JJ, Cras P (1999) Decreased Levels of Amyloid-beta 1-42 in Cerebrospinal Fluid of Creutzfeldt-Jakob Disease Patients. J Alzheimers Dis 1(6):419–424
72. Van Everbroeck B, Quoilin S, Boons J, Martin JJ, Cras P (2003) A prospective study of CSF markers in 250 patients with possible Creutzfeldt–Jakob disease. J Neurol Neurosurg Psychiatry 74(9):1210–1214
73. Varges D, Jung K, Gawinecka J, Heinemann U, Schmitz M, von Ahsen N, Krasnianski A, Armstrong VW, Zerr I (2011) Amyloid-β 1-42 levels are modified by apolipoprotein E ε4 in Creutzfeldt-Jakob disease in a similar manner as in Alzheimer’s disease. J Alzheimers Dis 23(4):717–726. doi:10.3233/JAD-2010-101527
74. Will RG (2003) Acquired prion disease: iatrogenic CJD, variant CJD, kuru. Br Med Bull 66:255–265
75. Wiltfang J, Esselmann H, Smirnov A, Bibl M, Cepek L, Steinacker P, Mollenhauer B, Buerger K, Hampel H, Paul S, Neumann M, Maler M, Zerr I, Kornhuber J, Kretzschmar HA, Poser S, Otto M (2003) Beta-amyloid peptides in cerebrospinal fluid of patients with Creutzfeldt-Jakob disease. Ann Neurol 54(2):263–267
76. Wiltfang J, Esselmann H, Bibl M, Hüll M, Hampel H, Kessler H, Frölich L, Schröder J, Peters O, Jessen F, Luckhaus C, Perneczky R, Jahn H, Fiszer M, Maler JM, Zimmermann R, Bruckmoser R, Kornhuber J, Lewczuk P (2007) Amyloid beta peptide ratio 42/40 but not A beta 42 correlates with phospho-Tau in patients with low- and high-CSF A beta 40 load. J Neurochem 101(4):1053–1059
77. Zanusso G, Fiorini M, Ferrari S, Gajofatto A, Cagnin A, Galassi A, Richelli S, Monaco S (2011) Cerebrospinal fluid markers in sporadic Creutzfeldt-Jakob disease. Int J Mol Sci 12(9):6281–6292
78. Zanusso G, Monaco S, Pocchiari M, Caughey B (2016) Advanced tests for early and accurate diagnosis of Creutzfeldt-Jakob disease. Nat Rev Neurol 12(7):427. doi:10.1038/nrneurol.2016.92
79. Zerr I, Pocchiari M, Collins S, Brandel JP, de Cuesta Pedro J, Knight RS, Bernheimer H, Cardone F, Delasnerie-Lauprêtre N, Corrales NC, Ladogana A, Bodemer M, Fletcher A, Awan T, Ruiz Bremón A, Budka H, Laplanche JL, Will RG, Poser S (2000) Analysis of EEG and CSF 14-3-3 proteins as aids to the diagnosis of Creutzfeldt–Jakob disease. Neurology 55(6):811–815
80. Zerr I, Kallenberg K, Summers DM, Romero C, Taratuto A, Heinemann U, Breithaupt M, Varges D, Meissner B, Ladogana A, Schuur M, Haik S, Collins SJ, Jansen GH, Stokin GB, Pimentel J, Hewer E, Collie D, Smith P, Roberts H, Brandel JP, van Duijn C, Pocchiari M, Begue C, Cras P, Will RG, Sanchez-Juan P (2009) Updated clinical diagnostic criteria for sporadic Creutzfeldt-Jakob disease. Brain 132(Pt 10):2659–2668. doi:10.1093/brain/awp191
81. Zou WQ, Puoti G, Xiao X, Yuan J, Qing L, Cali I, Shimoji M, Langeveld JP, Castellani R, Notari S, Crain B, Schmidt RE, Geschwind M, Dearmond SJ, Cairns NJ, Dickson D, Honig L, Torres JM, Mastrianni J, Capellari S, Giaccone G, Belay ED, Schonberger LB, Cohen M, Perry G, Kong Q, Parchi P, Tagliavini F, Gambetti P (2010) Variably protease-sensitive prionopathy: a new sporadic disease of the prion protein. Ann Neurol 68(2):162–172. doi:10.1002/ana.22094