Clinical and imaging correlates of hyperorality in syndromes associated with frontotemporal lobar degeneration.
behavioral symptoms
dietary habits
eating behavior
frontotemporal lobar degeneration
hyperorality
Journal
Psychiatry and clinical neurosciences
ISSN: 1440-1819
Titre abrégé: Psychiatry Clin Neurosci
Pays: Australia
ID NLM: 9513551
Informations de publication
Date de publication:
07 Oct 2024
07 Oct 2024
Historique:
revised:
04
09
2024
received:
26
06
2024
accepted:
11
09
2024
medline:
8
10
2024
pubmed:
8
10
2024
entrez:
8
10
2024
Statut:
aheadofprint
Résumé
Empirical research investigating hyperorality in syndromes associated with frontotemporal lobar degeneration (FTLD) is limited. The present study aims to assess and describe hyperorality and its clinical and imaging correlates in patients with FTLD-associated syndromes. This retrospective longitudinal study included consecutive patients with FTLD who underwent a clinical, cognitive, and behavioral assessment. The presence and severity of hyperorality was assessed using the Frontal Behavior Inventory. A total of 712 patients with FTLD were included in the study. Hyperorality was reported by 29% (204 of 712 [95% CI: 25-32%]) of patients; was more frequent in those with severe dementia than in those with prodromal or mild to moderate dementia (P < 0.05); was associated with younger age (odds ratio [OR] = 0.96 [95% CI: 0.94-0.99]), (P = 0.003) and positive family history for dementia (OR = 2.03 [95% CI: 1.18-3.49], P = 0.010); was overall more probable in the behavioral variant of frontotemporal dementia (bvFTD) and frontotemporal dementia with amyotrophic lateral sclerosis phenotypes, and less probable in other language or motor phenotypes; and was associated with higher severity of neuropsychiatric symptoms (OR = 1.08 [95% CI: 1.06-1.10], P < 0.001) and with the presence of several behavioral symptoms (P < 0.05). Moreover, hyperorality severity increased over time only in patients with bvFTD (β = +0.15, P = 0.011) or semantic variant of primary progressive aphasia (β = +0.34, P = 0.010). Finally, the presence of hyperorality was significantly associated with greater atrophy in the right anterior insula and right orbitofrontal region (false discovery rate-corrected P < 0.05). Hyperorality is common in certain FTLD-associated syndromes. Understanding its correlates can help clinicians define pharmacological and educational interventions and clarify related anatomical circuits.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024 The Author(s). Psychiatry and Clinical Neurosciences published by John Wiley & Sons Australia, Ltd on behalf of Japanese Society of Psychiatry and Neurology.
Références
Cipriani G, Carlesi C, Lucetti C, Danti S, Nuti A. Eating behaviors and dietary changes in patients with dementia. Am. J. Alzheimers Dis. Other Demen. 2016; 31: 706–716.
Manoochehri M, Huey ED. Diagnosis and management of behavioral issues in frontotemporal dementia. Curr. Neurol. Neurosci. Rep. 2012; 12: 528–536.
Grossman M, Seeley WW, Boxer AL et al. Frontotemporal lobar degeneration. Nat. Rev. Dis. Primers. 2023; 9: 40.
Rascovsky K, Hodges JR, Knopman D et al. Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain 2011; 134: 2456–2477.
Gorno‐Tempini ML, Hillis AE, Weintraub S et al. Classification of primary progressive aphasia and its variants. Neurology 2011; 76: 1006–1014.
Armstrong MJ, Litvan I, Lang AE et al. Criteria for the diagnosis of corticobasal degeneration. Neurology 2013; 80: 496–503.
Höglinger GU, Respondek G, Stamelou M et al. Clinical diagnosis of progressive supranuclear palsy: The movement disorder society criteria. Mov. Disord. 2017; 32: 853–864.
Strong MJ, Abrahams S, Goldstein LH et al. Amyotrophic lateral sclerosis ‐ frontotemporal spectrum disorder (ALS‐FTSD): Revised diagnostic criteria. Amyotroph Lateral Scler Frontotemporal Degener. 2017; 18: 153–174.
Morrow CB, Chaney GAS, Capuzzi D, Bakker A, Onyike CU, Kamath V. Hyperorality in frontotemporal dementia: Cognitive and psychiatric symptom profiles in early‐stage disease. J. Alzheimers Dis. 2022; 89: 1203–1209.
Perry DC, Sturm VE, Seeley WW, Miller BL, Kramer JH, Rosen HJ. Anatomical correlates of reward‐seeking behaviours in behavioural variant frontotemporal dementia. Brain 2014; 137: 1621–1626.
Ahmed RM, Irish M, Henning E et al. Assessment of eating behavior disturbance and associated neural networks in frontotemporal dementia. JAMA Neurol. 2016; 73: 282–290.
Woolley JD, Gorno‐Tempini ML, Seeley WW et al. Binge eating is associated with right orbitofrontal‐insular‐striatal atrophy in frontotemporal dementia. Neurology 2007; 69: 1424–1433.
Libri I, Altomare D, Bracca V et al. Time to diagnosis and its predictors in syndromes associated with frontotemporal lobar degeneration. Am. J. Geriatr. Psychiatry 2024; 32: 1004–1013.
Kertesz A, Nadkarni N, Davidson W, Thomas AW. The frontal behavioral inventory in the differential diagnosis of frontotemporal dementia. J. Int. Neuropsychol. Soc. 2000; 6: 460–468.
Alberici A, Geroldi C, Cotelli M et al. The frontal Behavioural inventory (Italian version) differentiates frontotemporal lobar degeneration variants from Alzheimer's disease. Neurol. Sci. 2007; 28: 80–86.
Miyagawa T, Brushaber D, Syrjanen J et al. Utility of the global CDR® plus NACC FTLD rating and development of scoring rules: Data from the ARTFL/LEFFTDS consortium. Alzheimers Dement. 2020; 16: 106–117.
International Standard Classification of Education. 2011. [Cited 2024 May 2] Available from: http://www.uis.unesco.org.
Goldman JS, Farmer JM, Wood EM et al. Comparison of family histories in FTLD subtypes and related tauopathies. Neurology 2005; 65: 1817–1819.
Altomare D, Rivolta J, Libri I et al. Neuropsychiatric symptoms in frontotemporal dementia: More than just noise? J. Alzheimers Dis. 2024; 98: 133–144.
Cosseddu M, Benussi A, Gazzina S et al. Progression of behavioural disturbances in frontotemporal dementia: A longitudinal observational study. Eur. J. Neurol. 2020; 27: 265–272.
Benussi A, Premi E, Gazzina S et al. Progression of behavioral disturbances and neuropsychiatric symptoms in patients with genetic frontotemporal dementia. JAMA Netw. Open 2021; 4: e2030194.
Cummings JL. The neuropsychiatric inventory: Assessing psychopathology in dementia patients. Neurology 1997; 48: S10–S16.
Kurth F, Gaser C, Luders E. A 12‐step user guide for analyzing voxel‐wise gray matter asymmetries in statistical parametric mapping (SPM). Nat. Protoc. 2015; 10: 293–304.
Farokhian F, Beheshti I, Sone D, Matsuda H. Comparing CAT12 and VBM8 for detecting brain morphological abnormalities in temporal lobe epilepsy. Front. Neurol. 2017; 8: 428.
Pengo M, Premi E, Borroni B. Dissecting the many faces of frontotemporal dementia: An imaging perspective. Int. J. Mol. Sci. 2022; 23: 12867.
Gordon PH. Amyotrophic lateral sclerosis: An update for 2013 clinical features, pathophysiology, management and therapeutic trials. Aging Dis. 2013; 4: 295–310.
Laforce R. Behavioral and language variants of frontotemporal dementia: A review of key symptoms. Clin. Neurol. Neurosurg. 2013; 115: 2405–2410.
Ulugut H, Stek S, Wagemans LEE et al. The natural history of primary progressive aphasia: Beyond aphasia. J. Neurol. 2022; 269: 1375–1385.
Snowden JS, Bathgate D, Varma A, Blackshaw A, Gibbons ZC, Neary D. Distinct behavioural profiles in frontotemporal dementia and semantic dementia. J. Neurol. Neurosurg. Psychiatry 2001; 70: 323–332.
Ahmed RM, Irish M, Kam J et al. Quantifying the eating abnormalities in frontotemporal dementia. JAMA Neurol. 2014; 71: 1540–1546.
Peterson KA, Jones PS, Patel N et al. Language disorder in progressive supranuclear palsy and Corticobasal syndrome: Neural correlates and detection by the MLSE screening tool. Front. Aging Neurosci. 2021; 13: 675739.
Peterson KA, Patterson K, Rowe JB. Language impairment in progressive supranuclear palsy and corticobasal syndrome. J. Neurol. 2021; 268: 796–809.
Kertesz A, McMonagle P. Behavior and cognition in corticobasal degeneration and progressive supranuclear palsy. J. Neurol. Sci. 2010; 289: 138–143.
Bowman GL, Shannon J, Ho E et al. Reliability and validity of food frequency questionnaire and nutrient biomarkers in elders with and without mild cognitive impairment. Alzheimer Dis. Assoc. Disord. 2011; 25: 49–57.
Ikeda M, Brown J, Holland AJ, Fukuhara R, Hodges JR. Changes in appetite, food preference, and eating habits in frontotemporal dementia and Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 2002; 73: 371–376.
Shinagawa S, Ikeda M, Nestor PJ et al. Characteristics of abnormal eating behaviours in frontotemporal lobar degeneration: A cross‐cultural survey. J. Neurol. Neurosurg. Psychiatry 2009; 80: 1413–1414.
Piguet O, Petersén Å, Yin Ka Lam B et al. Eating and hypothalamus changes in behavioral‐variant frontotemporal dementia. Ann. Neurol. 2011; 69: 69–319.
Ahmed RM, Halliday GM, Kiernan MC, Hodges JR. Eating behavior in frontotemporal dementia peripheral hormones vs hypothalamic pathology. Neurology 2015; 85: 1310–1317.