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A meta-analysis of neuropsychological, social cognitive, and olfactory functioning in the behavioral and language variants of frontotemporal dementia

Published online by Cambridge University Press:  06 December 2018

Vidyulata Kamath*
Affiliation:
Department of Psychiatry and Behavioral Sciences, Baltimore, MD, USA
Grace-Anna S. Chaney
Affiliation:
Department of Psychiatry and Behavioral Sciences, Baltimore, MD, USA
Jonathan DeRight
Affiliation:
Department of Psychiatry and Behavioral Sciences, Baltimore, MD, USA
Chiadi U. Onyike
Affiliation:
Department of Psychiatry and Behavioral Sciences, Baltimore, MD, USA Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD, USA
*
Author for correspondence: Vidyulata Kamath, E-mail: [email protected]

Abstract

Background

Though meta-analyses of neuropsychological and social cognitive deficits in behavioral variant frontotemporal dementia (bvFTD) have been conducted, no study has comprehensively characterized and compared the neuropsychological, social cognitive, and olfactory profiles in the behavioral and language variants of FTD.

Methods

Our search yielded 470 publications meeting inclusion criteria representing 11 782 FTD patients and 19 451 controls. For each domain, we calculated Hedges’ g effect sizes, which represent the mean difference between the patient and control group divided by the pooled standard deviation. The heterogeneity of these effects was assessed with Cochran's Q-statistic using a random-effects model. Meta-regressions were employed to analyze the influence of demographic and disease characteristics.

Results

Though semantic variant primary progressive aphasia patients showed the greatest impairment across all task types, the three groups showed similar cognitive effect sizes once contributions from the language subdomain were excluded from analysis. Contrary to expectation, the magnitude of deficits in executive functioning, social cognition and olfaction were comparable between the three subgroups. Among indices, a metric of executive errors distinguished the behavioral variant of FTD from the language phenotypes.

Conclusions

These data indicate that social cognitive and traditional executive functioning measures may not capture differences between FTD syndromes. These results have important implications for the interpretation of neuropsychological assessments, particularly when applied to the differential diagnosis of FTD. It is hoped that these findings will guide clinical and research assessments and spur new studies focused on improving the measurement of FTD syndromes.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2018 

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References

Bang, J, Spina, S and Miller, BL (2015) Frontotemporal dementia. Lancet 386, 16721682.Google Scholar
Beeldman, E, Raaphorst, J, Klein Twennaar, M, Govaarts, R, Pijnenburg, YAL, de Haan, RJ, de Visser, M and Schmand, BA (2018) The cognitive profile of behavioural variant FTD and its similarities with ALS: a systematic review and meta-analysis. Journal of Neurology, Neurosurgery, and Psychiatry 89, 9951002.Google Scholar
Begg, CB and Mazumdar, M (1994) Operating characteristics of a rank correlation test for publication bias Biometrics 50, 10881101.Google Scholar
Binney, RJ, Henry, ML, Babiak, M, Pressman, PS, Santos-Santos, MA, Narvid, J, Mandelli, ML, Strain, PJ, Miller, BL, Rankin, KP, Rosen, HJ and Gorno-Tempini, ML (2016) Reading words and other people: a comparison of exception word, familiar face and affect processing in the left and right temporal variants of primary progressive aphasia. Cortex 82, 147163.Google Scholar
Bird, CM, Chan, D, Hartley, T, Pijnenburg, YA, Rossor, MN and Burgess, N (2009) Topographical short-term memory differentiates Alzheimer's disease from frontotemporal lobar degeneration. Hippocampus 20, 11541169.Google Scholar
Bora, E, Walterfang, M and Velakoulis, D (2015) Theory of mind in behavioural-variant frontotemporal dementia and Alzheimer's disease: a meta-analysis. Journal of Neurology, Neurosurgery, and Psychiatry 86, 714719.Google Scholar
Bora, E, Velakoulis, D and Walterfang, M (2016) Meta-analysis of facial emotion recognition in behavioral variant frontotemporal dementia: comparison with Alzheimer disease and healthy controls. Journal of Geriatric Psychiatry and Neurology 29, 205211.Google Scholar
Borenstein, M, Hedges, LV, Higgins, JPT, Rothstein, HR (2009) Introduction to Meta-Analysis. Wiley: Chichester.Google Scholar
Carey, CL, Woods, SP, Damon, J, Halabi, C, Dean, D, Delis, DC, Miller, BL, Kramer, JH (2008) Discriminant validity and neuroanatomical correlates of rule monitoring in frontotemporal dementia and Alzheimer's disease. Neuropsychologia 46, 10811087.Google Scholar
Curtis, AF, Masellis, M, Hsiung, G-YR, Moineddin, R, Zhang, K, Au, B, Millett, G, Mackenzie, I, Rogaeva, E and Tierney, MC (2017) Sex differences in the prevalence of genetic mutations in FTD and ALS: a meta-analysis. Neurology 89, 16331642.Google Scholar
Devanand, DP, Michaels-Marston, KS, Liu, X, Pelton, GH, Padilla, M, Marder, K, Bell, K, Stern, Y and Mayeux, R (2000) Olfactory deficits in patients with mild cognitive impairment predict Alzheimer's disease at follow-up. American Journal of Psychiatry 157, 13991405.Google Scholar
Devanand, DP, Lee, S, Manly, J, Andrews, H, Schupf, N, Doty, RL, Stern, Y, Zahodne, LB, Louis, ED and Mayeux, R (2015) Olfactory deficits predict cognitive decline and Alzheimer dementia in an urban community. Neurology 84, 182189.Google Scholar
Egger, M, Davey Smith, G, Schneider, M and Minder, C (1997) Bias in meta-analysis detected by a simple, graphical test. The BMJ 315, 629634.Google Scholar
Eslinger, PJ, Dennis, K, Moore, P, Antani, S, Hauck, R and Grossman, M (2005) Metacognitive deficits in frontotemporal dementia. Journal of Neurology, Neurosurgery & Psychiatry 76, 16301635.Google Scholar
Eslinger, PJ, Moore, P, Troiani, V, Antani, S, Cross, K, Kwok, S and Grossman, M (2007) Oops! Resolving social dilemmas in frontotemporal dementia. Journal of Neurology, Neurosurgery & Psychiatry 78, 457460.Google Scholar
Gorno-Tempini, ML, Hillis, AE, Weintraub, S, Kertesz, A, Mendez, M, Cappa, SF, Ogar, JM, Rohrer, JD, Black, S, Boeve, BF, Manes, F, Dronkers, NF, Vandenberghe, R, Rascovsky, K, Patterson, K, Miller, BL, Knopman, DS, Hodges, JR, Mesulam, MM and Grossman, M (2011) Classification of primary progressive aphasia and its variants. Neurology 76, 10061014.Google Scholar
Grossman, M, Xie, SX, Libon, DJ, Wang, X, Massimo, L, Moore, P, Vesely, L, Berkowitz, R, Chatterjee, A, Coslett, HB, Hurtig, HI, Forman, MS, Lee, VM-Y and Trojanowski, JQ (2008) Longitudinal decline in autopsy-defined frontotemporal lobar degeneration. Neurology 70, 20362045.Google Scholar
Harciarek, M and Cosentino, S (2013) Language, executive function and social cognition in the diagnosis of frontotemporal dementia syndromes. International Review of Psychiatry 25, 178196.Google Scholar
Hodges, JR, Patterson, K, Ward, R, Garrard, P, Bak, T, Perry, R and Gregory, C (1999) The differentiation of semantic dementia and frontal lobe dementia (temporal and frontal variants of frontotemporal dementia) from early Alzheimer's disease: a comparative neuropsychological study. Neuropsychology 13, 3140.Google Scholar
Hornberger, M and Piguet, O (2012) Episodic memory in frontotemporal dementia: a critical review. Brain 135, 678692.Google Scholar
Hornberger, M, Savage, S, Hsieh, S, Mioshi, E, Piguet, O, Hodges, JR (2010) Orbitofrontal dysfunction discriminates behavioral variant frontotemporal dementia from Alzheimer's disease. Dementia and Geriatric Cognitive Disorders 30, 547552.Google Scholar
Hutchinson, AD and Mathias, JL (2007) Neuropsychological deficits in frontotemporal dementia and Alzheimer's disease: a meta-analytic review. Journal of Neurology Neurosurgery & Psychiatry 78, 917928.Google Scholar
Jiskoot, LC, Panman, JL, van Asseldonk, L, Franzen, S, Meeter, LHH, Donker Kaat, L, van der Ende, EL, Dopper, EGP, Timman, R, van Minkelen, R, van Swieten, JC, van den Berg, E and Papma, JM (2018) Longitudinal cognitive biomarkers predicting symptom onset in presymptomatic frontotemporal dementia. Journal of Neurology 265, 13811392.Google Scholar
Kamath, V, Moberg, PJ, Kohler, CG, Gur, RE and Turetsky, BI (2011) Odor hedonic capacity and anhedonia in schizophrenia and unaffected first-degree relatives of schizophrenia patients. Schizophrenia Bulletin 39, 5667.Google Scholar
Kertesz, A, Jesso, S, Harciarek, M, Blair, M and McMonagle, P (2010) What is semantic dementia? A cohort study of diagnostic features and clinical boundaries. Archives of Neurology 67, 483489.Google Scholar
Kramer, JH, Jurik, J, Sha, SJ, Rankin, KP, Rosen, HJ, Johnson, JK and Miller, BL (2003) Distinctive neuropsychological patterns in frontotemporal dementia, semantic dementia, and Alzheimer disease. Cognitive and Behavioral Neurology 16, 211218.Google Scholar
Kumfor, F, Miller, L, Lah, S, Hsieh, S, Savage, S, Hodges, JR, Piguet, O (2011) Are you really angry? The effect of intensity on facial emotion recognition in frontotemporal dementia. Social Neuroscience 6, 502514.Google Scholar
Laisney, M, Matuszewski, V, Mézenge, F, Belliard, S, de la Sayette, V, Eustache, F and Desgranges, B (2009) The underlying mechanisms of verbal fluency deficit in frontotemporal dementia and semantic dementia. Journal of Neurology 256, 10831094.Google Scholar
LaMarre, AK and Kramer, JH (2013) Accurate assessment of behavioral variant frontotemporal dementia. In Ravdin, LD and Katzen, HL (eds), Handbook on the Neuropsychology of Aging and Dementia. New York, NY pp. 313332.Google Scholar
Lenehan, ME, Summers, MJ, Saunders, NL, Summers, JJ and Vickers, JC (2015) Relationship between education and age-related cognitive decline: a review of recent research. Psychogeriatrics 15, 154162.Google Scholar
Libon, DJ, Xie, SX, Wang, X, Massimo, L, Moore, P, Vesely, L, Khan, A, Chatterjee, A, Coslett, HB, Hurtig, HI, Liang, T-W and Grossman, M (2009) Neuropsychological decline in frontotemporal lobar degeneration: a longitudinal analysis. Neuropsychology 23, 337346.Google Scholar
Lund and Manchester Groups (1994) Clinical and neuropathological criteria for frontotemporal dementia. Journal of Neurology, Neurosurgery, and Psychiatry 57, 416418.Google Scholar
Luzzi, S, Snowden, JS, Neary, D, Coccia, M, Provinciali, L and Lambon Ralph, MA (2007) Distinct patterns of olfactory impairment in Alzheimer's disease, semantic dementia, frontotemporal dementia, and corticobasal degeneration. Neuropsychologia 45, 18231831.Google Scholar
McKhann, GM, Albert, MS, Grossman, M, Miller, B, Dickson, D and Trojanowski, JQ, Work Group on Frontotemporal Dementia and Pick's Disease (2001) Clinical and pathological diagnosis of frontotemporal dementia: Report of the Work Group on Frontotemporal Dementia and Pick's Disease. Archives of Neurology 58, 18031809.Google Scholar
Mesholam, RI, Moberg, PJ, Mahr, RN and Doty, RL (1998) Olfaction in neurodegenerative disease: a meta-analysis of olfactory functioning in Alzheimer's and Parkinson's diseases. Archives of Neurology 55, 8490.Google Scholar
Mesulam, M-M (2001) Primary progressive aphasia. Annals of Neurology 49, 425432.Google Scholar
Mesulam, M-M, Rogalski, EJ, Wieneke, C, Hurley, RS, Geula, C, Bigio, EH, Thompson, CK and Weintraub, S (2014) Primary progressive aphasia and the evolving neurology of the language network. Nature Reviews Neurology 10, 554569.Google Scholar
Miller, LA, Hsieh, S, Lah, S, Savage, S, Hodges, JR and Piguet, O (2012) One size does not fit all: face emotion processing impairments in semantic dementia, behavioural-variant frontotemporal dementia and Alzheimer's disease are mediated by distinct cognitive deficits. Behavioural Neurology 25, 5360.Google Scholar
Murphy, C, Gilmore, MM, Seery, CS, Salmon, DP and Lasker, BR (1990) Olfactory thresholds are associated with degree of dementia in Alzheimer's disease. Neurobiology of Aging 11, 465469.Google Scholar
Neary, D, Snowden, JS, Gustafson, L, Passant, U, Stuss, D, Black, S, Freedman, M, Kertesz, A, Robert, PH, Albert, M, Boone, K, Miller, BL, Cummings, J and Benson, DF (1998) Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology 51, 15461554.Google Scholar
Ng, AS, Rademakers, R and Miller, B (2015) Frontotemporal dementia: a bridge between dementia and neuromuscular disease. Annals of the New York Academy of Sciences 1338, 7193.Google Scholar
Pal, A, Biswas, A, Pandit, A, Roy, A, Guin, D, Gangopadhyay, G and Senapati, AK (2016) Study of visuospatial skill in patients with dementia. Annals of Indian Academy of Neurology 19, 8388.Google Scholar
Park, LQ, Harvey, D, Johnson, J and Farias, ST (2015) Deficits in everyday function differ in AD and FTD. Alzheimer Disease and Associated Disorders 29, 301306.Google Scholar
Perneczky, R, Diehl-Schmid, J, Drzezga, A and Kurz, A (2007 a) Brain reserve capacity in frontotemporal dementia: a voxel-based 18F-FDG PET study. European Journal of Nuclear Medicine & Molecular Imaging 34, 10821087.Google Scholar
Perneczky, R, Diehl-Schmid, J, Förstl, H, Drzezga, A and Kurz, A (2007 b) Male gender is associated with greater cerebral hypometabolism in frontotemporal dementia: evidence for sex-related cognitive reserve. International Journal of Geriatric Psychiatry 22, 11351140.Google Scholar
Perry, RJ, Graham, A, Williams, G, Rosen, H, Erzinçlioglu, S, Weiner, M, Miller, B and Hodges, J (2006) Patterns of frontal lobe atrophy in frontotemporal dementia: a volumetric MRI study. Dementia and Geriatric Cognitive Disorders 22, 278287.Google Scholar
Piwnica-Worms, KE, Omar, R, Hailstone, JC and Warren, JD (2010) Flavour processing in semantic dementia. Cortex 46, 761768.Google Scholar
Premi, E, Gazzina, S, Bozzali, M, Archetti, S, Alberici, A, Cercignani, M, Bianchetti, A, Gasparotti, R, Turla, M, Caltagirone, C, Padovani, A and Borroni, B (2013) Cognitive reserve in granulin-related frontotemporal dementia: from preclinical to clinical stages. Plos ONE 8, e74762e74762.Google Scholar
Ramanan, S, Flanagan, E, Leyton, CE, Villemagne, VL, Rowe, CC, Hodges, JR and Hornberger, M (2016) Non-verbal episodic memory deficits in primary progressive aphasias are highly predictive of underlying amyloid pathology. Journal of Alzheimer's Disease 51, 367376.Google Scholar
Rankin, KP, Kramer, JH and Miller, BL (2005) Patterns of cognitive and emotional empathy in frontotemporal lobar degeneration. Cognitive and Behavioral Neurology 18, 2836.Google Scholar
Rascovsky, K, Salmon, DP, Hansen, LA, Thal, LJ and Galasko, D (2007) Disparate letter and semantic category fluency deficits in autopsy-confirmed frontotemporal dementia and Alzheimer's disease. Neuropsychology 21, 2030.Google Scholar
Rascovsky, K, Hodges, JR, Knopman, D, Mendez, MF, Kramer, JH, Neuhaus, J, Swieten, JC, Seelaar, H, Dopper, EGP, Onyike, CU, Hillis, AE, Josephs, KA, Boeve, BF, Kertesz, A, Seeley, WW, Rankin, KP, Johnson, JK, Gorno-Tempini, M-L, Rosen, H, Prioleau-Latham, CE, Lee, A, Kipps, CM, Lillo, P, Piguet, O, Rohrer, JD, Rossor, MN, Warren, JD, Fox, NC, Galasko, D, Salmon, DP, Black, SE, Mesulam, M, Weintraub, S, Dickerson, BC, Diehl-Schmid, J, Pasquier, F, Deramecourt, V, Lebert, F, Pijnenburg, Y, Chow, TW, Manes, F, Grafman, J, Cappa, SF, Freedman, M, Grossman, M and Miller, BL (2011) Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain 134, 24562477.Google Scholar
Rosen, HJ, Gorno-Tempini, ML, Goldman, WP, Perry, RJ, Schuff, N, Weiner, M, Feiwell, R, Kramer, JH and Miller, BL (2002) Patterns of brain atrophy in frontotemporal dementia and semantic dementia. Neurology 58, 198208.Google Scholar
Rousseaux, M, Sève, A, Vallet, M, Pasquier, F and Mackowiak-Cordoliani, MA (2010) An analysis of communication in conversation in patients with dementia. Neuropsychologia 48, 38843890.Google Scholar
Seeley, WW, Crawford, R, Rascovsky, K, Kramer, JH, Weiner, M, Miller, BL and Gorno-Tempini, ML (2008) Frontal paralimbic network atrophy in very mild behavioral variant frontotemporal dementia. Archives of Neurology 65, 249255.Google Scholar
Seligman, SC, Kamath, V, Giovannetti, T, Arnold, SE and Moberg, PJ (2013) Olfaction and apathy in Alzheimer's disease, mild cognitive impairment, and healthy older adults. Aging & Mental Health 17, 564570.Google Scholar
Sitek, EJ, Barczak, A and Harciarek, M (2015) Neuropsychological assessment and differential diagnosis in young-onset dementias. The Psychiatric Clinics of North America 38, 265279.Google Scholar
Smeding, HM and de Koning, I (2000) Frontotemporal dementia and neuropsychology: the value of missing values. Journal of Neurology, Neurosurgery, and Psychiatry 68, 726730.Google Scholar
Thompson, JC, Stopford, CL, Snowden, JS and Neary, D (2005) Qualitative neuropsychological performance characteristics in frontotemporal dementia and Alzheimer's disease. Journal of Neurology, Neurosurgery, and Psychiatry 76, 920927.Google Scholar
Tobias, A (1999) Assessing the influence of a single study in the meta-analysis estimate. Stata Technical Bulletin 47, 1517.Google Scholar
Tu, S, Wong, S, Hodges, JR, Irish, M, Piguet, O and Hornberger, M (2015) Lost in spatial translation – A novel tool to objectively assess spatial disorientation in Alzheimer's disease and frontotemporal dementia. Cortex 67, 8394.Google Scholar
Turner, RM, Bird, SM and Higgins, JPT (2013) The impact of study size on meta-analyses: examination of underpowered studies in Cochrane reviews. PloS ONE 8, e59202.Google Scholar
Woolley, JD, Khan, BK, Murthy, NK, Miller, BL and Rankin, KP (2011) The diagnostic challenge of psychiatric symptoms in neurodegenerative disease: rates of and risk factors for prior psychiatric diagnosis in patients with early neurodegenerative disease. Journal of Clinical Psychiatry 72, 126133.Google Scholar
Zald, DH and Andreotti, C (2010) Neuropsychological assessment of the orbital and ventromedial prefrontal cortex. Neuropsychologia 48, 33773391.Google Scholar
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