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Overnutrition, Ectopic Lipid and the Metabolic Syndrome Scott M Grundy

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Overnutrition, Ectopic Lipid and the Metabolic Syndrome Scott M Grundy Review J Investig Med: first published as 10.1136/jim-2016-000155 on 18 May 2016. Downloaded from Overnutrition, ectopic lipid and the metabolic syndrome Scott M Grundy Correspondence to ABSTRACT metabolic processes and predisposes to meta- Dr Scott M Grundy, Internal The metabolic syndrome is a constellation of bolic risk factors.6 Excess lipid in adipose tissue Medicine, UT Southwestsern Medical Center, Dallas, TX metabolic risk factors including atherogenic is called obesity; in other tissues, it is called 75390-9052, USA; scott. dyslipidemia (elevated serum triglycerides, reduced ectopic lipid. In this document, overnutrition [email protected] high-density lipoprotein (HDL) cholesterol), elevated will be defined as the any excess of nutrient blood pressure, dysglycemia (insulin resistance and energy that causes ectopic lipid accumulation Accepted 29 April 2016 elevated serum glucose), a pro-inflammatory state, outside adipose tissue. The essential pathways Published Online First 18 May 2016 and a prothrombotic state. Most persons with whereby overnutrition drives development of metabolic syndrome are obese, and usually have ectopic lipid are shown in figure 1. Excess Copyright © 2016 American fl Federation for Medical abdominal obesity. Generally, obesity is a re ection nutrients come from either dietary triglyceride Research of overnutrition. A current view is that when adipose or carbohydrate. Dietary triglyceride enters the tissue fails to store all excess nutrients as circulation with chylomicrons. Triglycerides are triglyceride, lipid begins to accumulate in various hydrolyzed to fatty acids by lipoprotein lipase tissues (eg, muscle, liver, pancreas, and heart). (LPL); and most of released fatty acids enter This accumulation is called ectopic lipid. Various adipose tissue, where they are re-esterified to mechanisms have been proposed whereby ectopic triglyceride. A portion of fatty acids released by lipid is detrimental in different tissues; these LPL bypasses adipose tissue and enters a variety derangements induce metabolic risk factors. The of tissues. Adipose tissue releases non-esterified foundation of the metabolic syndrome thus appears fatty acids (NEFA), which pass into the circula- to be overnutrition, that is, more nutrient intake tion and likewise reach many tissues. Glucose than can be safely disposed by lipid oxidation. derived from dietary carbohydrate goes directly Excess dietary carbohydrate also induces ectopic into the same tissues. When excess glucose is lipid. Of interest, less than half of obese individuals consumed, it can be converted to fatty acids develop metabolic syndrome. Through various through a process known as lipogenesis. All car- mechanisms they adapt to overnutrition so as to bohydrates and lipids are ultimately disposed minimize lipid overload in tissues, and consequently, by oxidation. At constant body weight, oxida- prevent the syndrome. tion rates of triglyceride and carbohydrate http://jim.bmj.com/ equal their intakes, and lipid content of adipose tissue remains unchanged. An imbalance The metabolic syndrome is a constellation of between intake and oxidation occurs only metabolic risk factors including atherogenic dys- during periods of weight gain or loss. These lipidemia (elevated serum triglycerides, reduced facts are well known, but often are forgotten high-density lipoprotein (HDL) cholesterol), when the mechanisms for ectopic lipid and elevated blood pressure, dysglycemia (insulin metabolic syndrome are discussed. on September 28, 2021 by guest. Protected copyright. resistance and elevated serum glucose), a Whereas tissue overload by lipid predisposes pro-inflammatory state and a prothrombotic to metabolic syndrome, and may be necessary fi state.12When present in combination, these for its development, it seemingly is not suf - factors essentially double the risk for athero- cient. Other factors, acting in local tissues, – sclerotic cardiovascular disease (ASCVD);3 5 appear necessary for the clinical syndrome to fl they also increase risk for type 2 diabetes about present. The following brie y discusses the fivefold.2 Most persons with metabolic syn- origins of ectopic lipid, and considers add- drome are obese. This implies that overnutrition itional factors that bring out the syndrome. contributes to the syndrome.6 Still, less than half of obese individuals manifest multiple metabolic ADIPOSE TISSUE risk factors.7 Many persons seemingly are able One emerging view holds that adipose tissue to adapt to overnutrition so as to prevent the protects against accumulation of ectopic lipid syndrome. The following discussion examines and hence prevents metabolic syndrome – potential mechanisms underlying the metabolic through fat storage.8 11 If excess dietary nutri- syndrome and considers how the body defends ents could be stored fully in adipose tissue, against overload of nutrient energy. ectopic lipid should not occur. Thus the meta- The most plausible, unifying hypothesis for bolic syndrome may reflect insufficient adipose To cite: Grundy SM. J the pathogenesis of metabolic syndrome is that tissue to store the load of fat imposed upon it Investig Med overnutrition drives accumulation of excess by a high-calorie diet. The best example of this – 2016;64:1082 1086. lipid in organs or tissues; this in turn deranges mechanism is the rare condition called 1082 Grundy SM. J Investig Med 2016;64:1082–1086. doi:10.1136/jim-2016-000155 Review J Investig Med: first published as 10.1136/jim-2016-000155 on 18 May 2016. Downloaded from adipose-tissue compartment can be discussed briefly relative to metabolic syndrome. Figure 2 shows apparent magni- tudes of flow of fatty acids through these compartments. Truncal adipose tissue correlates better with metabolic – syndrome than does lower body adipose tissue.18 20 UBSQ-AT is the largest component of truncal adipose – tissue.21 23 It predominates in release of NEFA into the sys- – temic and splanchnic circulations;21 23 thus UBSQ-AT could be a major source of ectopic lipid. Compared to LBSQ-AT, UBSQ-AT appears to be more insulin resist- – ant;24 26 this means that UBSQ-AT more readily releases its fatty acids into the circulation, that is, it has higher turn- over rates of fatty acids.27 Although UBSQ obesity is often implicated in causation of ectopic lipid, more likely, it just Figure 1 Major pathways for triglyceride (TG) and carbohydrate acts as a conduit for transfer of excess nutrient fatty acids (CHO), in the form of glucose, derived from the diet. These to the circulation, as suggested in figure 1. pathways are described in detail in the text. NEFA, non-esterified A high VAT likewise has been strongly associated with fatty acids. – metabolic syndrome.28 34 It is particularly correlated with hepatic ectopic lipid.35 Fatty acids entering the splanchnic lipodystrophy.12 13 This is a condition of severe deficiency circulation are destined for the liver. These can come from in adipose tissue; hence, consumed lipids cannot be UBSQ-AT or directly from splanchnic lipolysis of TGRLP.36 adequately stored in adipose tissue and other tissues Presumably, visceral obesity is a response to a greater flux become overloaded. This precipitates the metabolic syn- of NEFA through the splanchnic bed. drome. Theoretically, even in the absence of lipodystrophy, Compared to upper body compartments, LBSQ-AT the syndrome could occur if adipose tissue storage capacity seems to possess a lower rate of turnover of fatty acids. is exceeded, even in the presence of clinical obesity. Individuals with predominant lower body obesity have rela- Adipose tissue is the major site of uptake for lipid tively normal plasma levels and turnover rates for NEFA.27 released during lipolysis of triglyceride-rich lipoproteins Lower body obesity has been postulated to be protective (TGRLP). These lipoproteins consist of chylomicrons, against the metabolic syndrome.37 More likely, it is rela- derived from dietary fat, and of very low-density lipopro- tively neutral, rather than being protective, because of its teins (VLDL), produced by the liver. Fatty acids freed relatively low turnover rate for fatty acids.27 during lipolysis of TGRLP are taken up by adipose tissue When obesity is present, adipose tissue becomes and are re-esterified as triglycerides. In turn, adipose-tissue inflamed. This inflammation results from invasion by triglyceride undergoes lipolysis and releases NEFA into the macrophages secondary to adipose-tissue dysfunction.38 circulation. During weight gain, fat storage is positive; at Consequently, the adipose-tissue bed releases inflammatory http://jim.bmj.com/ constant weight, no net storage of triglyceride occurs. cytokines and prothrombotic factors into the systemic cir- NEFA release occurs mainly, but not exclusively, in the culation. Release of excess cytokines may induce a general- fasting state. Its release is regulated mainly by insulin. ized proinflammatory state, which could contribute to both During fasting, when insulin levels are low, NEFA release is ASCVD39 and diabetes.40 Release of prothrombotic factors high; conversely, in the postprandial state, when insulin may likewise predispose to acute ASCVD events. A host of levels are high, NEFA release is suppressed. Thus, when other ‘adipokines’ has been identified.41 Whether these excess calories are consumed, increased quantities of fatty on September 28, 2021 by guest. Protected copyright. acids cycle through adipose tissue. Increased release of NEFA from adipose tissue in obese persons is commonly believed to be
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