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Tain, Y. Early-Life Origins of Metabolic Syndrome. Encyclopedia. Available online: https://encyclopedia.pub/entry/15796 (accessed on 20 November 2024).
Tain Y. Early-Life Origins of Metabolic Syndrome. Encyclopedia. Available at: https://encyclopedia.pub/entry/15796. Accessed November 20, 2024.
Tain, You-Lin. "Early-Life Origins of Metabolic Syndrome" Encyclopedia, https://encyclopedia.pub/entry/15796 (accessed November 20, 2024).
Tain, Y. (2021, November 08). Early-Life Origins of Metabolic Syndrome. In Encyclopedia. https://encyclopedia.pub/entry/15796
Tain, You-Lin. "Early-Life Origins of Metabolic Syndrome." Encyclopedia. Web. 08 November, 2021.
Early-Life Origins of Metabolic Syndrome
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This entry is adapted from the peer-reviewed paper 10.3390/ijms222111872

Metabolic syndrome (MetS) is not a single disease but a collection of medical conditions that occur together and increase the risk of cardiovascular disease (CVD). Although MetS had been defined slightly differently by various organizations, the main components of MetS include obesity, hypertension, dyslipidemia and insulin resistance. The prevalence estimates vary, based on the criteria used for the diagnosis of MetS. 

metabolic syndrome

1. Introduction

Metabolic syndrome (MetS) is not a single disease but a collection of medical conditions that occur together and increase the risk of cardiovascular disease (CVD). Although MetS had been defined slightly differently by various organizations [1], the main components of MetS include obesity, hypertension, dyslipidemia and insulin resistance. The prevalence estimates vary, based on the criteria used for the diagnosis of MetS. Thus far, global MetS prevalence is estimated to affect approximately one quarter of the world population [2]. More importantly, MetS-related disorders account for two thirds of the non-communicable disease (NCDs) deaths [3]. Also important is that it displays multiple and diverse phenotypes with indications for differing treatment strategies. In the absence of specific therapeutic regimens, the prevalence of MetS remains on the increase globally [2]. Therefore, a superior strategy to stop the spread of the MetS epidemic is required to for prevention, in addition to treatment.
Most NCDs may start in early life [4]. The establishment of various adverse environmental conditions, which takes place during pregnancy and lactation, could be involved in the early-life programming of health. This concept is now known as the developmental origin of health and disease (DOHaD) [5], which is supported by evidence coming from a large number of epidemiological and experimental observations.
Various early-life risk factors often linked to nutritional imbalance may lead to vulnerability to later MetS [6][7][8][9][10]. Remarkably, there is evidence for the programming of some similar features of MetS from different early-life insults, possibly suggesting a commonality of mechanism and highlighting that identifying underlying mechanistic pathways is vital to develop ideal prevention interventions [6]. By intervening before disease ever occurs, we have the potential to stop undesirable programming processes resulting in MetS, which is referred to as reprogramming [11].

2. Epidemiological Evidence Linked Early-Life Insults with Offspring MetS

Extensive epidemiological studies have linked adverse early-life conditions with the risk of MetS in the offspring in later life. First, there is evidence from severe famines [12][13][14][15][16]. The Dutch Famine Birth Cohort Study demonstrated that the children of pregnant women exposed to famine displayed various characteristics of MetS, like obesity, dyslipidemia, hypertension, insulin resistance and CVDs [12][13]. Findings similar to those of the Dutch famine were also established in other famine studies [14][15][16]. Of particular interest, maternal undernutrition during early gestation had greater effects in increasing cardiometabolic risk in adult offspring, compared to maternal undernutrition during middle- or late-gestation [12]. Another line of evidence comes from research in twin pregnancy. These studies reported there were associations between low birth weight (LBW) and different characteristics of MetS, including hypertension, type 2 diabetes and insulin resistance [17][18]. Third, a prior systematic review of 39 studies revealed that rapid postnatal catch-up growth of LBW neonate had an approximately 80% increased risk for CVDs, a major complication of MetS [19]. The risk factors for MetS of developmental origins have been assessed in a number of observational studies. Risk factors reported in these cohorts relating to adverse cardiometabolic outcomes in adult offspring include maternal obesity [20][21], gestational diabetes [21][22], excessive postnatal weight gain, [23] and environmental chemicals exposure [16]. To date, literature on paternal risk factors is scare. There is emerging evidence that paternal risk factors, such as obesity, diabetes mellitus, advanced age, and cigarette smoke are associated with adverse metabolic and cardiovascular outcomes in their offspring [24][25]. All of these observations provide links between the suboptimal early-life environment and the risks for developing MetS in adulthood.
However, these epidemiological studies do not propose molecular mechanisms underlying programming processes for the development of potential reprogramming interventions. Therefore, animal models have been established to demonstrate the biological plausibility of the associations observed in epidemiological studies, providing proof of causality.

3. Animal Models for Developmental Origins of MetS

In view of the difficulties in establishing animal models that manifest all the characteristics of MetS, most investigations into MetS of developmental origin are done using models that display certain hallmarks of MetS [6][7][8]. To date, a broad range of adverse early-life environmental factors are associated with certain features of MetS in adult offspring, including nutrition imbalance, maternal conditions or disease, chemical exposure, medication use, etc. [6][7][8][9][10][26][27][28][29]. However, excessive information is available based on only one characteristic of MetS, and in the interest of brevity, we have limited this review to at least two of the listed components that are present [30][31][32][33][34][35][36][37][38][39][40][41][42][43][44][45][46][47][48][49][50][51][52][53][54][55][56][57][58][59][60][61][62][63][64][65][66][67][68][69][70][71][72] (See Table 1). Diverse small- and large-animal models have been developed for DOHaD research [29][73], each with its own natural advantages and disadvantages. This review was restricted to rodent models for appropriate comparisons of major characteristics of MetS appear through a lifetime. Table 1 reveals the outcomes relating to MetS determined in rats ranging from eight weeks to one year of age. Considering one human year is almost equivalent to two rat weeks in adulthood [74], most outcomes are determined from childhood to middle adulthood in terms of human age. Each category is discussed in turn.
Table 1. Rodent models of MetS of developmental origins, categorized according to environmental factors.
Animal Models Timing Experimental
Animal		 Offspring Outcomes Relating to MetS
Nutritional imbalance
Caloric restriction Pregnancy and lactation SD rats [30]/Wistar rats [31][32] ↑BP 12-16 wk [30][31], ↓insulin levels and exhibit insulin resistance 14 wk [32]
Protein restriction Pregnancy Wistar rats ↑BP 12 wk [33], exhibit insulin resistance 12 wk [34]
High-fat diet Pregnancy and lactation SD rats ↑BP 16 wk [35], ↑adiposity 16 wk [36], dyslipidemia 16 wk [37], ↑BW, exhibit dyslipidemia and hyperinsulinemia 100 day [38]
High-fructose diet Pregnancy and lactation SD rats/C57BL6J mice ↑BP [39], exhibit insulin resistance and dyslipidemia 12 wk [40], ↑BP, exhibit insulin resistance and obesity 1 year [41]
High-fructose diet plus high-fat diet Pregnancy and lactation SD rats [42]/Wistar rats [43] ↑BP 16 wk [42], ↑BW and adiposity 150 days [43]
Calcium-deficient diet Pregnancy WKY rats [44]/SD rats [45] ↑BP 1 year [44], ↑adiposity, exhibit insulin resistance and dyslipidemia [45]
Zinc-deficient diet Pregnancy and lactation Wistar rats [46]/SD rats [47] ↑BP 12 wk [46], ↑BW, exhibit insulin resistance 15 wk [47]
Vitamin D restricted diet Pregnancy and lactation SD rats ↑BP 8 wk [48], exhibit insulin resistance 16 wk [49]
Maternal illness/condition
Uteroplacental insufficiency Pregnancy WKY rats [50]/Wistar rats [51] ↑BP 22 wk [50], exhibit dyslipidemia and insulin resistance 30 wk [51]
Polycystic ovary syndrome Pregnancy Wistar rat [52], SD rats [53] ↑BP 120 days [52], exhibit dyslipidemia 16 wk [53]
Maternal hypoxia Pregnancy Wistar rats [52]/SD rats [54] ↑BP 4 mo [52], ↑BW and adiposity, exhibit insulin resistance 12 wk [54]
Maternal inflammation Pregnancy SD rats [55]/Wistar rats [56] ↑BP 12 wk [55], insulin resistance 75 days [56]
Diabetes Pregnancy SD rats [57]/Wistar rats [58][59] ↑BP 12 wk [57], ↑BW and adiposity 12 wk [58], exhibit insulin resistance and dyslipidemia 16 wk [59]
Chronodisruption Pregnancy and lactation SD rats [60]/Wistar rats [61] ↑BP 12 wk [60], exhibit insulin resistance 18 wk [61]
Chemical/medication exposure
DEHP Pregnancy Wistar rats ↑BP 21 wk [62], exhibit insulin resistance 80 day [63]
BPA Pregnancy and lactation SD rats ↑BP 16 wk [64], exhibit insulin resistance 6 mo [65]
Alcohol Pregnancy SD rats ↑BP 6 mo [66], exhibit insulin resistance 6 mo [67]
Nicotine Pregnancy Wistar rats ↑BP 8 mo [68], ↑BW and adiposity, exhibit insulin resistance [69]
Glucocorticoid Pregnancy and postnatal days1-3 SD rats [70][71]/Wistar rats [72] ↑BP 12 mo [70][71], exhibit insulin resistance 6 mo [72]
SD = Sprague-Dawley rat; WKY = Wistar-Kyoto rat; BP = blood pressure; BW = body weight; wk = week; mo = month; di-DEHP = (2-ethylhexyl) phthalate; BPA = bisphenol A; ↑ = increased; ↓ = decreased.

3.1. Nutritional Imbalance

Studies of nutritional programming linking DOHaD-related disorders using animal models have been ongoing since the early 1990s [73]. Dietary manipulation has been the focus of a large body of work relating to MetS of developmental origins. Table 1 shows insufficient or excessive consumption of a certain nutrient has been used to induce different features of MetS. Following the studies of the Dutch famine [12][13], a number of maternal nutrient restriction models have been established to mimic the undernutrition experienced by pregnant women at that time.
Caloric restriction is defined as an overall reduction in energy and nutrient intake without incurring specific nutrient. In rats, a 50% caloric restriction during gestation and lactation can result in hypertension and insulin resistance in adult offspring [28][29][30]. Restriction of calories by a range of 30% to 70% in pregnant rats has been reported to induce increases of BP in their adult progeny, as reviewed elsewhere [74]. From a general perspective, offspring exposed to a greater degree of caloric restriction are prone to develop hypertension earlier [75]. However, the extent to which the severity of caloric restriction affects other characteristics of MetS in adult offspring remains to be elucidated further.
Similar to caloric restriction, the protein restriction model may mimic the challenge faced in developing nations. Adult rat offspring born to dams exposed to protein restriction during pregnancy develop hypertension [31] and insulin resistance [32]. Although a more severe protein restriction causes an earlier development of hypertension in offspring [75], a previous study reported that two low-protein diet manipulations with the same protein concentration (9%) but different components in pregnant rat provoked different programming effects on BP in adult offspring [76]. It is therefore possible that the balance of specific amino acids and other nutrients may be a critical determinant in programming of MetS-related phenotypes but not protein restriction per se.
Table 1 indicates maternal high-fat diet programs almost all feature of MetS in adult rat offspring at 14–16 weeks of age, such as hypertension [33], obesity [34][36], dyslipidemia [35][36], and insulin resistance [36]. A high-fat diet has been widely used to explore the mechanisms of metabolic disease of both established and developmental origins [77][78]. Nevertheless, the programming effects of maternal high-fat diet on offspring BP are diverse according to age, sex, strains, and different fatty acids compositions [78]. Notably, abnormal regulation of insulin signaling and lipid metabolism programmed by a maternal high-fat diet can be promoted by a post-weaning high-fat diet, leading to development of MetS-related phenotypes in adult offspring [37][79][80]. A maternal high-fructose diet has also been reported as a commonly used animal model for studying MetS of developmental origins [81]. We and others have shown that adult rat offspring of mothers exposed to 60% high-fructose diet during gestation and lactation displayed MetS-related comorbidities [39][40][41][81]. Furthermore, mother rats receiving a high-fructose diet plus a high-fat diet saw an elevation in BP and BW in their offspring [42][43]. These findings suggest that maternal diets containing key components based on the human Western diet may have synergistic effects between fat and sugar on the development of features of MetS in adult offspring. Moreover, deficiencies in micronutrients, including calcium [44][45], zinc [46][47], and vitamin D [48][49] in pregnant mother rats are associated with offspring MetS.

3.2. Maternal Illnesses and Conditions

Complications during pregnancy and maternal diseases can affect fetal programming, resulting in intrauterine growth retardation (IUGR) in offspring [82]. As IUGR reflects an abnormal adaptive fetal growth in an adverse intrauterine environment, IUGR animal models are applied to decipher the underlying mechanisms behind MetS of developmental origins [82]. In the model of uteroplacental insufficiency developed by uterine artery ligation in the pregnant rat, IUGR offspring developed hypertension, dyslipidemia and insulin resistance in adulthood [50][51]. Additionally, several animal models resembling maternal conditions and diseases have been evaluated, such as polycystic ovary syndrome (PCOS) [52][53], maternal hypoxia [52][54], maternal inflammation [55][56], diabetes [57][58][59], and chronodisruption [60][61].
Epidemiological observations have established that inflammatory disorders, PCOS, and hypoxia increase the risk of pregnancy complications [83][84]. In the PCOS model, maternal hyperandrogenemia was induced by injection of testosterone cypionate in late gestation for studying cardiometabolic outcomes in adult offspring. Accordingly, adult offspring exhibited hypertension and dyslipidemia at 16–17 weeks of age [52][53]. Likewise, several features of MetS can be programmed by maternal hypoxia and inflammation, including hypertension [52][55], obesity [54], and insulin resistance [54][56].
It is clear from a range of human observational studies that maternal diabetes gives rise to different phenotypes of MetS in offspring, including obesity, insulin resistance, hypertension, dyslipidemia, and CVDs [85]. The majority of rodent studies of maternal diabetes have employed streptozotocin (STZ)-induced diabetes [57][58][59]. When injected into neonates [57][58] or adult rats [57][59], STZ can cause type 1 or type 2 diabetes, respectively. Almost all major characteristics of MetS are present in adult offspring born to diabetic mothers at 12–16 weeks of age [57][58][59], which are largely in line with the findings in humans.
There is now increasing evidence connecting disturbances in the circadian rhythm with the key components of MetS [86]. A meta-analysis including 22 studies showed that overall sleep quality as well as sleep complaints have significant positive associations with MetS [87]. The circadian system is the major regulator of human metabolism [88]. The circadian clock system consists of central and peripheral clocks, which are coordinated to produce daily rhythms [89]. This central clock located in the suprachiasmatic nucleus regulates the body’s metabolism through synchronizing peripheral clocks in our body’s key organs such as the heart, kidney, liver, muscle and adipose tissue [90]. Accordingly, it is not surprising that circadian rhythm sleep disorders have been linked to several components of the MetS [86].
In pregnant women, circadian disruption can lead to a wide range of adverse consequences for their children [91]. Maternal circadian disruption affects not only central and peripheral circadian clocks but also a range of endogenous circadian signals including melatonin and glucocorticoid secretion [92][93]. Although data on maternal sleep disorder programs MetS in offspring remain limited, two animal studies have reported that adult rat offspring born to dams received constant light exposure or pinealectomy developed hypertension [60] and insulin resistance [61].

3.3. Chemical and Medication Exposures

Relatively few studies have investigated early-life chemical and medication exposures on developmental programming of MetS. A broad range of early-life environmental chemical exposures have been related to increased risk for developing hypertension of developmental origins, as we reviewed elsewhere [94]. These chemicals, di-(2-ethylhexyl) phthalate (DEHP) and bisphenol A, have been studied for their impact on insulin resistance in adult progeny [63][65]. These findings are in agreement with epidemiological research data showing that endocrine-disrupting chemical exposure is linked to CVDs later in life [95].
As with chemical effects during development, substance abuse is another risk factor. A high proportion (6–16%) of pregnant women in the United States are cigarette smokers, alcohol abusers, or illicit drug users [96]. In rodent models, maternal nicotine or alcohol exposure causes hypertension [66][68], insulin resistance [67][69], and obesity [69] in adult offspring.
Despite a number of medications (such as cyclosporine [97] and minocycline [98]) administered in pregnancy that have been related to developmentally programmed hypertension in adult offspring [29], only glucocorticoid has been studied for other features of MetS [70][71][72]. During development, the fetus is at risk of glucocorticoid exposure through excess maternal corticosteroids (e.g., stressed pregnancies) or through exogenous administration (e.g., preterm birth). Antenatal or neonatal administration of dexamethasone lead to hypertension [70][71] and insulin resistance [72] in adult rat offspring.
Comparable to maternal programming, reported animal models relating to paternal factors-induced MetS in offspring are rather limited [25]. So far, only adult offspring of paternal low protein intake [99], paternal high-fat diet [100], and paternal hyperglycemia [101] have been evaluated, and these have developed at least two components of MetS.
Considering animal models are in good agreement with the epidemiological observations showing various maternal insults induce similar features of MetS in offspring, it is possible that various insults may mediate common mechanisms culminating in MetS of developmental origins.

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You-Lin Tain
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