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Longitudinal Neuropsychological Study of Presymptomatic c.709-1G>A Progranulin Mutation Carriers

Published online by Cambridge University Press:  29 October 2018

Myriam Barandiaran ,
Fermín Moreno ,
María de Arriba ,
Begoña Indakoetxea ,
Irati Boda ,
Alazne Gabilondo ,
Mikel Tainta  and
Adolfo López de Munain
Myriam Barandiaran
Affiliation:
Cognitive Disorders Unit, Department of Neurology, Donostia University Hospital, Paseo Dr Begiristain sn, CP 20014, San Sebastian, Gipuzkoa, Spain Center for Networked Biomedical Research on Neurodegenerative Disease (CIBERNED), area 6, Carlos III Health Institute, Spain Neuroscience Area, Biodonostia Health Research Institute, Paseo Dr Begiristain sn, CP 20014, San Sebastian, Gipuzkoa, Spain
Fermín Moreno*
Affiliation:
Cognitive Disorders Unit, Department of Neurology, Donostia University Hospital, Paseo Dr Begiristain sn, CP 20014, San Sebastian, Gipuzkoa, Spain Center for Networked Biomedical Research on Neurodegenerative Disease (CIBERNED), area 6, Carlos III Health Institute, Spain Neuroscience Area, Biodonostia Health Research Institute, Paseo Dr Begiristain sn, CP 20014, San Sebastian, Gipuzkoa, Spain
María de Arriba
Affiliation:
Cognitive Disorders Unit, Department of Neurology, Donostia University Hospital, Paseo Dr Begiristain sn, CP 20014, San Sebastian, Gipuzkoa, Spain Center for Networked Biomedical Research on Neurodegenerative Disease (CIBERNED), area 6, Carlos III Health Institute, Spain Neuroscience Area, Biodonostia Health Research Institute, Paseo Dr Begiristain sn, CP 20014, San Sebastian, Gipuzkoa, Spain
Begoña Indakoetxea
Affiliation:
Cognitive Disorders Unit, Department of Neurology, Donostia University Hospital, Paseo Dr Begiristain sn, CP 20014, San Sebastian, Gipuzkoa, Spain Center for Networked Biomedical Research on Neurodegenerative Disease (CIBERNED), area 6, Carlos III Health Institute, Spain Neuroscience Area, Biodonostia Health Research Institute, Paseo Dr Begiristain sn, CP 20014, San Sebastian, Gipuzkoa, Spain
Irati Boda
Affiliation:
Department of Computer Science, Multimedia and Telecommunications, Universitat Oberta de Catalunya, Barcelona, Spain
Alazne Gabilondo
Affiliation:
Center for Networked Biomedical Research on Neurodegenerative Disease (CIBERNED), area 6, Carlos III Health Institute, Spain Neuroscience Area, Biodonostia Health Research Institute, Paseo Dr Begiristain sn, CP 20014, San Sebastian, Gipuzkoa, Spain Department of Neurology, Hospital de Bidasoa, Irun, Spain
Mikel Tainta
Affiliation:
Center for Networked Biomedical Research on Neurodegenerative Disease (CIBERNED), area 6, Carlos III Health Institute, Spain Neuroscience Area, Biodonostia Health Research Institute, Paseo Dr Begiristain sn, CP 20014, San Sebastian, Gipuzkoa, Spain CITA Alzheimer, San Sebastian, Spain
Adolfo López de Munain
Affiliation:
Cognitive Disorders Unit, Department of Neurology, Donostia University Hospital, Paseo Dr Begiristain sn, CP 20014, San Sebastian, Gipuzkoa, Spain Center for Networked Biomedical Research on Neurodegenerative Disease (CIBERNED), area 6, Carlos III Health Institute, Spain Neuroscience Area, Biodonostia Health Research Institute, Paseo Dr Begiristain sn, CP 20014, San Sebastian, Gipuzkoa, Spain
*
Correspondence and reprint requests to: Fermin Moreno, Department of Neurology, Hospital Universitario Donostia, Paseo Dr Begiristain sn, CP 20014, San Sebastian, Gipuzkoa, Spain. E-mail: [email protected]
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Abstract

Objective: The assessment of individuals from families affected by familial frontotemporal dementia (FTD) allows the evaluation of preclinical or pre-diagnosis disease markers. The current work aims to investigate the existence of a cognitive phase in GRN mutation carriers before overt clinical symptoms begin. Methods: We performed a longitudinal neuropsychological analysis (three assessments in 4 years) in a group of presymptomatic c.709-1G>A progranulin (GRN) (n=15) mutation carriers and non-carrier relatives (n=25) from seven FTD families. Results:GRN mutation carriers showed subtle decline over the longitudinal follow-up in several different domains (namely, attention, facial affect recognition, decision-making, language, and memory). The differences between groups were most marked in the facial affect recognition test, with improvement in the non-carrier group and decline in the GRN mutation carrier group, with very large effect sizes. Conclusions: Facial affect recognition may decline before clinical diagnosis and makes the adapted version of the Picture of Facial Affect a potential candidate for early detection of GRN-associated FTD. (JINS, 2019, 25, 39–47)

Keywords

Asymptomatic diseasesFrontotemporal dementiaFrontotemporal lobar degenerationLongitudinal studiesNeuropsychological testsprogranulin proteinhuman
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 25 , Issue 1 , January 2019 , pp. 39 - 47
Copyright
Copyright © The International Neuropsychological Society 2018 

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Footnotes

*

These authors contributed equally to this work.

References

REFERENCES

Acosta-Baena, N., Sepulveda-Falla, D., Lopera-Gómez, C.M., Jaramillo-Elorza, M.C., Moreno, S., Aguirre-Acevedo, D.C., Lopera, F. (2011). Pre-dementia clinical stages in presenilin 1 E280A familial early-onset Alzheimer’s disease: A retrospective cohort study. The Lancet. Neurology, 10, 213–220. doi:10.1016/S1474-4422(10)70323-9 Google Scholar
Allison, T., Puce, A., & McCarthy, G. (2000). Social perception from visual cues: Role of the STS region. Trends in Cognitive Sciences, 4, 267–278. doi:10.1016/S1364-6613(00)01501-1 Google Scholar
Ardila, A., Lopera, F., Rosselli, M., Moreno, S., Madrigal, L., Arango-Lasprilla, J.C., Ossa, J. (2000). Neuropsychological profile of a large kindred with familial Alzheimer’s disease caused by the E280A single presenilin-1 mutation. Archives of Clinical Neuropsychology, 15, 515–528.Google Scholar
Barandiaran, M., Estanga, A., Moreno, F., Indakoetxea, B., Alzualde, A., Balluerka, N., Lopez de Munain, A. (2012). Neuropsychological features of asymptomatic c.709-1G>A progranulin mutation carriers. Journal of the International Neuropsychological Society, 18, 1086–1090. doi:10.1017/S1355617712000823 A+progranulin+mutation+carriers.+Journal+of+the+International+Neuropsychological+Society,+18,+1086–1090.+doi:10.1017/S1355617712000823>Google Scholar
Bateman, R.J., Xiong, C., Benzinger, T.L., Fagan, A.M., Goate, A., Fox, N.C., Blazey, T.M. (2012). Clinical and biomarker changes in dominantly inherited Alzheimer’s disease. New England Journal of Medicine, 367, 795–804. doi:10.1056/NEJMoa1202753 Google Scholar
Bechara, A. (2007). Iowa Gambling Task. Lutz, FL: Psychological Assessment Resources.Google Scholar
Bertoux, M., de Souza, L.C., Sarazin, M., Funkiewiez, A., Dubois, B., & Hornberger, M. (2015). How preserved is emotion recognition in Alzheimer disease compared with behavioral variant frontotemporal dementia? Alzheimer Disease and Associated Disorders, 29, 154–157. doi:10.1097/WAD.0000000000000023 Google Scholar
Borroni, B., Alberici, A., Cercignani, M., Premi, E., Serra, L., Cerini, C., … Bozzali, M. (2012). Granulin mutation drives brain damage and reorganization from preclinical to symptomatic FTLD. Neurobiology of Aging, 33, 2506–2520. doi:10.1016/j.neurobiolaging.2011.10.031.Google Scholar
Caroppo, P., Habert, M.O., Durrleman, S., Funkiewiez, A., Perlbarg, V., Hahn, V., Le Ber, I. (2015). Lateral temporal lobe: An early imaging marker of the presymptomatic GRN disease?. Journal of Alzheimers Disease, 47, 751–759. doi:10.3233/JAD-150270 Google Scholar
Chen-Plotkin, A.S., Martinez-Lage, M., Sleiman, P.M., Hu, W., Greene, R., Wood, E.M., Van Deerlin, V.M. (2011). Genetic and clinical features of progranulin-associated frontotemporal lobar degeneration. Archives of Neurology, 68, 488–497. doi:10.1001/archneurol.2011.53 Google Scholar
Conners, C.K., & Staff, M. (2000). Conners’ Continuous Performance Test II (CPT II V. 5) (pp. 1–16). North Tonawanda, NY: Multi-Health Systems Inc.Google Scholar
Diehl-Schmid, J., Pohl, C., Ruprecht, C., Wagenpfeil, S., Foerstl, H., & Kurz, A. (2007). The Ekman 60 Faces Test as a diagnostic instrument in frontotemporal dementia. Archives of Clinical Neuropsychology, 22, 459–464.Google Scholar
Dopper, E.G.P., Rombouts, S.A.R.B., Jiskoot, L.C., den Heijer, T., de Graaf, J.R.A., de Koning, I., … van Swieten, J.C. (2013). Structural and functional brain connectivity in presymptomatic familial frontotemporal dementia. Neurology, 80, 814–823.Google Scholar
Ekman, P. (1993). Pictures of facial affect (POFA). 18 min. 1-110. Paul Ekman Group, LLC.Google Scholar
Fernandez-Duque, D., & Black, S.E. (2005). Impaired recognition of negative facial emotions in patients with frontotemporal dementia. Neuropsychologia, 43, 1673–1687.Google Scholar
Fisher, N.J., Tierney, M.C., Snow, W.G., & Szalai, J.P. (1999). Odd/even short forms of the Boston Naming Test: Preliminary geriatric norms. Clinical Neuropsychology, 13, 359–364.Google Scholar
Fusar-Poli, P., Placentino, A., Carletti, F., Landi, P., Allen, P., Surguladze, S., Politi, P. (2009). Functional atlas of emotional faces processing: A voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. Journal of Psychiatry and Neuroscience, 34, 418–432.Google Scholar
Geschwind, D.H., Robidoux, J., Alarcón, M., Miller, B.L., Wilhelmsen, K.C., Cummings, J.L., & Nasreddine Z.S. (2001). Dementia and neurodevelopmental predisposition: cognitive dysfunction in presymptomatic subjects precedes dementia by decades in frontotemporal dementia. Ann Neurol, 50, 741–746.Google Scholar
Hallam, B.J., Jacova, C., Hsiung, G.Y., Wittenberg, D., Sengdy, P., Bouchard-Kerr, P., Mackenzie, I.R. (2014). Early neuropsychological characteristics of progranulin mutation carriers. Journal of the Intrenational Neuropsychological Society, 20, 694–703. doi:10.1017/S1355617714000551 Google Scholar
Heaton, R.K. (1981). Wisconsin Card Sorting Test (WCST). Odessa FL: Psychological Assessment Resources.Google Scholar
Hornberger, M., Yew, B., Gilardoni, S., Mioshi, E., Gleichgerrcht, E., Manes, F., & Hodges, J.R. (2014). Ventromedial‐frontopolar prefrontal cortex atrophy correlates with insight loss in frontotemporal dementia and Alzheimer’s disease. Human Brain Mapping, 35, 616–626. doi:10.1002/hbm.22200 Google Scholar
Jiskoot, L.C., Dopper, E.G., Heijer, T. d., Timman, R., van Minkelen, R., van Swieten, J.C., & Papma, J.M. (2016). Presymptomatic cognitive decline in familial frontotemporal dementia: A longitudinal study. Neurology, 87, 384–391. doi:10.1212/WNL.0000000000002895 Google Scholar
Kaplan, E., Goodglass, H., & Weintraub, S. (1983). The Boston naming test, (2nd. ed.). Philadelphia: Lea & Febiger.Google Scholar
Le Ber, I., Camuzat, A., Hannequin, D., Pasquier, F., Guedj, E., Rovelet-Lecrux, A., Bakchine, S. (2008). Phenotype variability in progranulin mutation carriers: A clinical, neuropsychological, imaging and genetic study. Brain, 131, 732–746. doi:10.1093/brain/awn012 Google Scholar
Lezak, M.D. (2004). Neuropsychological assessment. New York: Oxford University Press.Google Scholar
López de Munain, A., Alzualde, A., Gorostidi, A., Otaegui, D., Ruiz-Martínez, J., Indakoetxea, B., Martí Massó, J.F. (2008). Mutations in progranulin gene: Clinical, pathological, and ribonucleic acid expression findings. Biological Psychiatry, 63, 946–952. doi:10.1016/j.biopsych.2007.08.015 Google Scholar
Moreno, F., Indakoetxea, B., Barandiaran, M., Alzualde, A., Gabilondo, A., Estanga, A., López de Munain, A. (2009). “Frontotemporoparietal” dementia Clinical phenotype associated with the c. 709-1G> A PGRN mutation. Neurology, 73, 1367–1374. doi:10.1212/WNL.0b013e3181bd82a7 +A+PGRN+mutation.+Neurology,+73,+1367–1374.+doi:10.1212/WNL.0b013e3181bd82a7>Google Scholar
Moreno, F., Sala-Llonch, R., Barandiaran, M., Sánchez-Valle, R., Estanga, A., Bartrés-Faz, D., Indakoetxea, B. (2013). Distinctive age-related temporal cortical thinning in asymptomatic granulin gene mutation carriers. Neurobiology of Aging, 34, 1462–1468. doi:10.1016/j.neurobiolaging.2012.11.005 Google Scholar
Morris, J.C., Mohs, R.C., Rogers, H., Fillenbaum, G., & Heyman, A. (1988). CERAD: Clinical and neuropsychological assessment of Alzheimer’s disease. Psychopharmacological Bulletin, 24, 641–652.Google Scholar
Papma, J.M., Jiskoot, L.C., Panman, J.L., Dopper, E.G., den Heijer, T., Donker Kaat, L., van Swieten, J.C. (2017). Cognition and gray and white matter characteristics of presymptomatic C9orf72 repeat expansion. Neurology, 89, 1256–1264. doi:10.1212/WNL.0000000000004393 Google Scholar
Peña-Casanova, J., Blesa, R., Aguilar, M., Gramunt-Fombuena, N., Gómez-Ansón, B., Oliva, R., Sol, J.M., for the NEURONORMA Study Team (2009). Spanish multicenter normative studies (NEURONORAM Project): Methods and simple characteristics. Archives of Clinical Neuropsychology, 24, 307–319.Google Scholar
Pievani, M., Paternicò, D., Benussi, L., Binetti, G., Orlandini, A., Cobelli, M., … Frisoni, G.B. (2014). Pattern of structural and functional brain abnormalities in asymptomatic granulin mutation carriers. Alzheimer’s & Dementia, 10, S354–S363. doi: 10.1016/j.jalz.2013.09.009.Google Scholar
Rademakers, R., Baker, M., Gass, J., Adamson, J., Huey, E.D., Momeni, P., Hutton, M. (2007). Phenotypic variability associated with progranulin haploinsufficiency in patients with the common 1477C-->T (Arg493X) mutation: An international intitative. The Lancet. Neurology, 6, 857–868.T+(Arg493X)+mutation:+An+international+intitative.+The+Lancet.+Neurology,+6,+857–868.>Google Scholar
Reitan, R.M. (1958). Validity of the Trail Making Test as an indicator of organic brain damage. Perceptual and Motor Skills, 8(3), 271–276.Google Scholar
Rohrer, J.D., Nicholas, J.M., Cash, D.M., van Swieten, J., Dopper, E., Jiskoot, L., Rossor, M.N. (2015). Presymptomatic cognitive and neuroanatomical changes in genetic frontotemporal dementia in the Genetic Frontotemporal dementia Initiative (GENFI) study: A cross-sectional analysis. The Lancet. Neurology, 14, 253–262. doi:10.1016/S1474-4422(14)70324-2 Google Scholar
Sabatinelli, D., Fortune, E.E., Li, Q., Siddiqui, A., Krafft, C., Oliver, W.T., Jeffries, J. (2011). Emotional perception: Meta–analyses of face and natural scene proecessing. Neuroimage, 54, 2524–2533.Google Scholar
Stokholm, J., Teasdale, T.W., Johannsen, P., Nielsen, J.E., Nielsen, T.T., Isaacs, A., ... Frontotemporal dementia Research in Jutland Association, c. (2013). Cognitive impairment in the preclinical stage of dementia in FTD-3 CHMP2B mutation carriers: A longitudinal prospective study. Journal of Neurology, Neurosurgery, and Psychiatry, 84, 170–176. doi:10.1136/jnnp-2012-303813 Google Scholar
Tirado, V., Muñoz, C., Aguirre, C., Pineda, D., & Lopera, F. (2004). Desempeño de portadores y no portadores de la mutación E280A para la enfermedad de Alzheimer familiar en una prueba de denominación. Revista de Neurología, 39, 322–326.Google Scholar
van Swieten, J.C., & Heutink, P. (2008). Mutations in progranulin (GRN) within the spectrum of clinical and pathological phenotypes of frontotemporal dementia. The Lancet. Neurology 7, 965–974. doi:10.1016/S1474-4422(08)70194-7 Google Scholar
Wechsler, D. (1997). WMS-III: Wechsler memory scale administration and scoring manual. New York: Psychological Corporation.Google Scholar
Winblad, S., Hellström, P., Lindberg, C., & Hansen, S. (2006). Facial emotion recognition in myotonic dystrophy type 1 correlates with CTG repeat expansion. Journal of Neurology, Neurosurgery, & Psychiatry, 77, 219–223. doi:10.1136/jnnp.2005.070763 Google Scholar
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