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Original Investigation |

Assessment of Eating Behavior Disturbance and Associated Neural Networks in Frontotemporal Dementia

Rebekah M. Ahmed, MBBS1,2,3,4; Muireann Irish, PhD1,2,3; Elana Henning, BSc5; Nadene Dermody, BSc1; Lauren Bartley, BSc1; Matthew C. Kiernan, DSc4; Olivier Piguet, PhD1,2,3; Sadaf Farooqi, MB, ChB, PhD5; John R. Hodges, MD1,2,3
[+] Author Affiliations
1Neuroscience Research Australia, Sydney
2University of New South Wales, Sydney, Australia
3Australian Research Council Centre of Excellence in Cognition and Its Disorders, University of New South Wales, Sydney, Australia
4Brain and Mind Centre, Sydney Medical School, University of Sydney, Sydney, Australia
5University of Cambridge Metabolic Research Laboratories and National Institute for Health Research Cambridge Biomedical Research Centre, Wellcome Trust–Medical Research Council Institute of Metabolic Science, Cambridge, United Kingdom
JAMA Neurol. 2016;73(3):282-290. doi:10.1001/jamaneurol.2015.4478.
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Importance  Abnormal eating behaviors are common in patients with frontotemporal dementia (FTD), yet their exact prevalence, severity, and underlying biological mechanisms are not understood.

Objective  To define the severity of abnormal eating behavior and sucrose preference and their neural correlates in patients with behavioral variant FTD (bvFTD) and semantic dementia.

Design, Setting, and Participants  Forty-nine patients with dementia (19 with bvFTD, 15 with semantic dementia, and 15 with Alzheimer disease) were recruited, and their eating behavior was compared with that of 25 healthy controls. The study was conducted from November 1, 2013, through May 31, 2015, and data analyzed from June 1 to August 31, 2015.

Main Outcomes and Measures  Patients participated in an ad libitum breakfast test meal, and their total caloric intake and food preferences were measured. Changes in eating behavior were also measured using the Appetite and Eating Habits Questionnaire (APEHQ) and the Cambridge Behavioral Inventory (CBI). Sucrose preference was tested by measuring liking ratings of 3 desserts of varying sucrose content (A: 26%, B: 39%, C: 60%). Voxel-based morphometry analysis of whole-brain 3-T high-resolution brain magnetic resonance imaging was used to determine the gray matter density changes across groups and their relations to eating behaviors.

Results  Mean (SD) ages of patients in all 4 groups ranged from 62 (8.3) to 66 (8.4) years. At the ad libitum breakfast test meal, all patients with bvFTD had increased total caloric intake (mean, 1344 calories) compared with the Alzheimer disease (mean, 710 calories), semantic dementia (mean, 573 calories), and control groups (mean, 603 calories) (P < .001). Patients with bvFTD and semantic dementia had a strong sucrose preference compared with the other groups. Increased caloric intake correlated with atrophy in discrete neural networks that differed between patients with bvFTD and semantic dementia but included the cingulate cortices, thalami, and cerebellum in patients with bvFTD, with the addition of the orbitofrontal cortices and nucleus accumbens in patients with semantic dementia. A distributed network of neural correlates was associated with sucrose preference in patients with FTD.

Conclusions and Relevance  Marked hyperphagia is restricted to bvFTD, present in all patients with this diagnosis, and supports its diagnostic value. Differing neural networks control eating behavior in patients with bvFTD and semantic dementia and are likely responsible for the differences seen, with a similar network controlling sucrose preference. These networks share structures that control cognitive-reward, autonomic, neuroendocrine, and visual modulation of eating behavior. Delineating the neural networks involved in mediating these changes in eating behavior may enable treatment of these features in patients with complex medical needs and aid in our understanding of structures that control eating behavior in patients with FTD and healthy individuals.

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Figure 1.
Eating Behavior in Patients With Frontotemporal Dementia: Results of the Ad Libitum Breakfast Test Meal and Dessert Experiment

Panel A, Box plot showing total caloric intake for the ad libitum breakfast test meal. Ends of boxes represent the first and third quartiles. Lines in the boxes represent median values. Whiskers represent the minimum and maximum values. Panels B and C, For the dessert experiment, patients’ mean liking scores for desserts A (26% sucrose), B (39% sucrose), and C (60% sucrose) and patients’ mean perceived sweetness scores for desserts A, B, and C are shown.

aFor the ad libitum breakfast test meal, mean intake in the behavioral variant frontotemporal dementia (bvFTD) group was greater than for all other groups (P < .001). For the dessert A, liking ratings of the patients with bvFTD were less than the ratings of all other groups (P < .01).

bFor the dessert C, liking ratings of the patients with bvFTD and semantic dementia were greater than the ratings of all other groups (P < .001).

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Figure 2.
Voxel-Based Morphometry Analyses for Total Intake and Sucrose Preference and Visual Representation of Proposed Networks That Control Total Intake and Sucrose Preference in Frontotemporal Dementia (FTD)

Voxel-based morphometry analyses revealed brain regions in which gray matter intensity correlates significantly with total caloric intake in patients with behavioral variant FTD (bvFTD) (Montreal Neurological Institute [MNI] coordinates: x = 18, y = 40): higher total caloric intake on the ad libitum breakfast test meal correlated with gray matter intensity decrease in a number of brain regions likely involving a network connecting the anterior cingulate, which connects to the thalamus and is involved in taste via connections to the insula and reward via connections to the basal ganglia. The thalamus also likely connects to the hypothalamus, with neuroendocrine modulation of reward, and the lingual gyrus and visual cortex, for visual input to reward processing. The cerebellum also likely modulates eating behavior through autonomic input and cerebellar hypothalamic connections. In patients with semantic dementia (MNI coordinates: x = 18, y = 40), the orbitofrontal cortex is likely involved in decision making regarding preferences that may explain the rigid eating behavior in this group. This then aligns with a similar network in bvFTD involving reward and taste (left thalamus, insula, amygdala, bilateral nucleus accumbens). Additional contributions of lingual gyrus and cerebellar inputs are likely in semantic dementia eating behavior. Significant associations were found between sucrose preference (liking of most sweet dessert [60% sucrose]) in patients with bvFTD and semantic dementia combined (MNI coordinates: x = 20, y = −8). The network for sucrose involves the orbitofrontal cortex connecting right insula-striatal reward structures and nucleus accumbens. Again the cerebellum and lingual gyrus are involved in this network. Colored voxels show regions that were significant in the covariate analyses with P < .05 corrected for false discovery rate. Clusters are overlaid on the MNI standard brain. Age is included as a covariate in the analyses. L indicates left.

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