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      Imaging of brain glucose uptake by PET in obesity and cognitive dysfunction: life-course perspective

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          Abstract

          The prevalence of obesity has reached epidemic proportions and keeps growing. Obesity seems implicated in the pathogenesis of cognitive dysfunction, Alzheimer’s disease and dementia, and vice versa. Growing scientific efforts are being devoted to the identification of central mechanisms underlying the frequent association between obesity and cognitive dysfunction. Glucose brain handling undergoes dynamic changes during the life-course, suggesting that its alterations might precede and contribute to degenerative changes or signaling abnormalities. Imaging of the glucose analog 18F-labeled fluorodeoxyglucose ( 18FDG) by positron emission tomography (PET) is the gold-standard for the assessment of cerebral glucose metabolism in vivo. This review summarizes the current literature addressing brain glucose uptake measured by PET imaging, and the effect of insulin on brain metabolism, trying to embrace a life-course vision in the identification of patterns that may explain (and contribute to) the frequent association between obesity and cognitive dysfunction. The current evidence supports that brain hypermetabolism and brain insulin resistance occur in selected high-risk conditions as a transient phenomenon, eventually evolving toward normal or low values during life or disease progression. Associative studies suggest that brain hypermetabolism predicts low BDNF levels, hepatic and whole body insulin resistance, food desire and an unfavorable balance between anticipated reward from food and cognitive inhibitory control. Emerging mechanistic links involve the microbiota and the metabolome, which correlate with brain metabolism and cognition, deserving attention as potential future prevention targets.

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          Most cited references80

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          Brain insulin resistance in type 2 diabetes and Alzheimer disease: concepts and conundrums

          Considerable overlap has been identified in the risk factors, comorbidities and putative pathophysiological mechanisms of Alzheimer disease and related dementias (ADRDs) and type 2 diabetes mellitus (T2DM), two of the most pressing epidemics of our time. Much is known about the biology of each condition, but whether T2DM and ADRDs are parallel phenomena arising from coincidental roots in ageing or synergistic diseases linked by vicious pathophysiological cycles remains unclear. Insulin resistance is a core feature of T2DM and is emerging as a potentially important feature of ADRDs. Here, we review key observations and experimental data on insulin signalling in the brain, highlighting its actions in neurons and glia. In addition, we define the concept of 'brain insulin resistance' and review the growing, although still inconsistent, literature concerning cognitive impairment and neuropathological abnormalities in T2DM, obesity and insulin resistance. Lastly, we review evidence of intrinsic brain insulin resistance in ADRDs. By expanding our understanding of the overlapping mechanisms of these conditions, we hope to accelerate the rational development of preventive, disease-modifying and symptomatic treatments for cognitive dysfunction in T2DM and ADRDs alike.
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            Glucose clamp technique: a method for quantifying insulin secretion and resistance.

            Methods for the quantification of beta-cell sensitivity to glucose (hyperglycemic clamp technique) and of tissue sensitivity to insulin (euglycemic insulin clamp technique) are described. Hyperglycemic clamp technique. The plasma glucose concentration is acutely raised to 125 mg/dl above basal levels by a priming infusion of glucose. The desired hyperglycemic plateau is subsequently maintained by adjustment of a variable glucose infusion, based on the negative feedback principle. Because the plasma glucose concentration is held constant, the glucose infusion rate is an index of glucose metabolism. Under these conditions of constant hyperglycemia, the plasma insulin response is biphasic with an early burst of insulin release during the first 6 min followed by a gradually progressive increase in plasma insulin concentration. Euglycemic insulin clamp technique. The plasma insulin concentration is acutely raised and maintained at approximately 100 muU/ml by a prime-continuous infusion of insulin. The plasma glucose concentration is held constant at basal levels by a variable glucose infusion using the negative feedback principle. Under these steady-state conditions of euglycemia, the glucose infusion rate equals glucose uptake by all the tissues in the body and is therefore a measure of tissue sensitivity to exogenous insulin.
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              Normal brain development and aging: quantitative analysis at in vivo MR imaging in healthy volunteers.

              To quantitate neuroanatomic parameters in healthy volunteers and to compare the values with normative values from postmortem studies. Magnetic resonance (MR) images of 116 volunteers aged 19 months to 80 years were analyzed with semiautomated procedures validated by means of comparison with manual tracings. Volumes measured included intracranial space, whole brain, gray matter (GM), white matter (WM), and cerebrospinal fluid (CSF). Results were compared with values from previous postmortem studies. Whole brain and intracranial space grew by 25%-27% between early childhood (mean age, 26 months; age range, 19-33 months) and adolescence (mean age, 14 years; age range, 12-15 years); thereafter, whole-brain volume decreased such that volunteers (age range, 71-80 years) had volumes similar to those of young children. GM increased 13% from early to later (6-9 years) childhood. Thereafter, GM increased more slowly and reached a plateau in the 4th decade; it decreased by 13% in the oldest volunteers. The GM-WM ratio decreased exponentially from early childhood through the 4th decade; thereafter, it gradually declined. In vivo patterns of change in the intracranial space, whole brain, and GM-WM ratio agreed with published postmortem data. MR images accurately depict normal patterns of age-related change in intracranial space, whole brain, GM, WM, and CSF. These quantitative MR imaging data can be used in research studies and clinical settings for the detection of abnormalities in fundamental neuroanatomic parameters.
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                Author and article information

                Journal
                Endocr Connect
                Endocr Connect
                EC
                Endocrine Connections
                Bioscientifica Ltd (Bristol )
                2049-3614
                November 2019
                07 October 2019
                : 8
                : 11
                : R169-R183
                Affiliations
                [1 ]Institute of Clinical Physiology , National Research Council (CNR), Pisa, Italy
                Author notes
                Correspondence should be addressed to P Iozzo: patricia.iozzo@ 123456ifc.cnr.it
                Article
                EC-19-0348
                10.1530/EC-19-0348
                6865363
                31590145
                4d8fa934-a072-4417-9d89-a78b2177512d
                © 2019 The authors

                This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

                History
                : 27 September 2019
                : 07 October 2019
                Product
                Categories
                Review

                obesity,metabolism,development/fetal nutrition,cognitive dysfunction,brain pet imaging

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