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Hindawi Publishing CorporationJournal o Diabetes ResearchVolume , Article ID ,pageshttp://dx.doi.org/.//

Review ArticleEarly Life Factors and Type 2 Diabetes Mellitus

Xinli Jiang,1 Huijie Ma,2 Yan Wang,3,4 and Yan Liu3

Department of Ophthalmology, Te Tird Hospital of Hebei Medical University, Ziqiang Road , Shijiazhuang, Hebei , China Department of Physiology, Hebei Medical University, Zhongshan Road , Shijiazhuang, Hebei , China Department of Endocrinology, Te Tird Hospital of Hebei Medical University, Ziqiang Road , Shijiazhuang, Hebei , China Orthopaedic Biomechanical Laboratory of Hebei Province, Te Tird Hospital of Hebei Medical University, Ziqiang Road ,

Shijiazhuang, Hebei , China

Correspondence should be addressed to Yan Liu; [email protected]

Received October ; Accepted November

Academic Editor: Joseph Fomusi Ndisang

Copyright Xinli Jiang et al. Tis is an open access article distributed under the Creative Commons Attribution License,which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

ype diabetes mellitus (DM) is a multiactorial disease, and its aetiology involves a complex interplay between genetic,epigenetic, and environmental actors. In recent years, evidences rom both human and animal experiments have correlatedearly lie actors with programming diabetes risk in adult lie. Fetal and neonatal period is crucial or organ development. Manymaternal actors during pregnancy may increase the risk o diabetes o offsprings in later lie, which include malnutrition, healthy(hyperglycemia and obesity), behavior (smoking, drinking, and junk ood diet), hormone administration, and even stress. In

neonates, catch-up growth, lactation, glucocorticoids administration, and stress have all been ound to increase the risk o insulinresistance or DM. Unavorableenvironments (socioeconomic situation and amine) or obesity also has long-termnegativeeffectson children by causing increased susceptibility to DM in adults. We also address the potential mechanisms that may underlie thedevelopmental programming o DM. Tereore, it might be possible to prevent or delay the risk or DM by improving pre-and/or postnatal actors.

1. Introduction

ype diabetes (DM) is a metabolic disease caused bygenetic and multiple environmental actors. Epidemical andexperimental studies have ound that detrimental early lieactors may predispose high incidence o cardiovascular

disease and metabolic diseases in later lie, which is alsotermed as barker hypothesis. Organs are under develop-ment and unctional maturation rom etal stage to child-hood; disturbance o the homeostasis during crucial periodsmight predispose increased risk o insulin resistance andevenDM in late lie.

2. Part I: Prenatal Factors (Figure 1)

.. Diet and Nutrition. It has been suggested that the qualityand quantity o the nutrition during pregnancy may causestrong and permanent effects on the etus. Te alteredstructure o chromosome during this procedure might be

the cause o cell dysunction and increased susceptibility todiseases through altered gene expression [].

... Malnutrition and Low Protein Diet. Te associationsbetween maternal malnutrition, low protein diet, and DMhave been widely studied. ypical epidemical studies romthe population born during the Dutch amine period [] orin some poor countries [] have ound that those who hadbeen exposed to maternal malnutrition may have increasedmorbidity o metabolic diseases including DM in adult lie.

Te mechanisms responsible or the prenatal malnu-trition programming insulin resistance or DM remainunclear. Orozco-Sols et al. [] have ound that low pro-tein diet during pregnancy and lactating may cause per-manent altered hypothalamic expression o genes in ratoffspring involved in insulin signaling and lipid and glucosemetabolism, which may programme metabolic diseases.

In addition, the effect o low protein diet during preg-nancy on postnatal cell has also been noticed recently.

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Journal o Diabetes Research

Insulin resistance, diabetes in adult

Fetus

Low protein

High fat

Overnutrition

TFA

Alcohol

Smoking

Hypoxia

BPA

Stress

Hyperglycemia

Obesity

Glucocorticoids

Testosterone

Placenta

Maternal

F : Prenatal actors mentioned in recent years that might correlate with insulin resistance and/or DM. Data rom human andanimal studies have shown that malnutrition or overnutrition, metabolic disorders, exposure to hypoxia, some chemicals and hormones,and unhealthy liestyle such as smoking and alcohol drinking duringpregnancy might predispose detrimental long-term effects on offspring,leading to increased risk o insulin resistance or DM. FA: transatty acids; BPA: biophenol A.

Low protein diet

DNA methylation in P2

promoters

Mitochondria dysfunction

HNF4a expression

Increased cell differentiation

Oxidative stressFibrosis

F : Te effect o low protein diet during pregnancy on postnatal cell. Low protein diet during pregnancy may lead to increasedoxidative stress, brosis, decreased HNFa expression, deected mitochondriogenesis, and mitochondria dysunction, and increased cell

differentiation instead o prolieration was ound in cell o adult animal offspring, which may participate in -cell dysunction andconsequently increase the incidence o DM.

Increased oxidative stress and brosis [], decreased HNFaexpression with increased DNA methylation in P promoters[], deected mitochondriogenesis and mitochondria dys-unction [], and increased cell differentiation instead oprolieration [] were ound in cell o adult animal offspringwhose mothers were under low protein diet during preg-nancy. Tese may cause -cell dysunction and consequentlyincrease the incidence o DM in postnatal lie (Figure ).

... Overnutrition

High Protein.A study rom Maurer and Reimer [] in Wistarrats has ound that high protein diet during pregnancy andlactating may cause increased resistin and IL- mRNA levelsin brown at tissue in -day-old offspring; both actors wereincluded in the pathogenesis o insulin resistance [,].

High Fat Diet. Both human and animal studies have identiedthat at diet may cause obesity and insulin resistance [,].Intriguingly, the effect o high at diet on metabolic disordersseemed to be programmative. Te prenatal period is a keydevelopmental window or nutrition status. Masuyama and

Hiramatsu [] ound that mice offspring exposed to highat diet during pregnancy developed insulin resistance andhyperlipidemia at wks o age, which was associated withaltered levels o leptin in adipose tissue. Te experimentconducted in CBL/ mice by Liang et al. [] has alsoshowed that high saturated atty acids diet during pregnancyled to insulin resistance, hyperglycemia in adult offspringundernormal dietcondition.Te mechanismsunderlying arestill under investigation. Evidences rom animal study have

indicated that overexposure to high at diet in utero may leadto elevated mRNA level o hypothalamic signal transducerand activator o transcription- and suppressor o cytokinesignalling- in the offspring []. Both o these two actorsare ound to participate in obese and insulin resistance cases[]. In addition, prenatal exposure to high saturated ats maycause increased hepatic phosphoenolpyruvate carboxykinaseexpression, atty liver, reduced basal acetyl CoA carboxy-lase phosphorylation, and insulin signalling []. ImpairedWnt/-catenin signaling pathway in skeletal muscle has alsobeen ound [], which may also participate in pathogenesiso insulin resistance in adult lie, since the insulin sensitivitycan be improved by activating Wnt/-catenin [].

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... ransfatty Acids and Junk Food. ransatty acids areunsaturated atty acids that contain nonconjugated doublebond in the trans-conguration. So ar, data that correlatedtransatty acids diet with insulin resistance or diabetes is weakand inconsistent []. However, it is still worth noting thatprenatal exposure to transatty acids might cause impaired

insulin resistance and increased content o abdominal atafer birth []. No similar effects can be observed in miceexposed to transatty acid during lactating.

Data about long-term effects o prenatal junk oodtaking is quite limited; experiment rom Bayol et al. []has indicated that junk ood taking during prenatal andlactating period may cause reduced insulin sensitivity inemale offspring rats. More intensive studies still need to beperormed or the convincing conclusion.

... Alcohol. Studies have already correlated chronic alco-hol intake with insulin resistance even DM [, ]. Inthe series o studies perormed by Chen and Nyomba they

have ound that SD rats with alcohol intake ( g/kg/day)during pregnancy may have hyperglycemia and reducedglucose transporter type (GLU) content in musclein adult offspring afer a reduced birth weight and thencatch up growth []. In addition, in this animal model,impaired inhibition effects o insulin on hepatic gene expres-sion o phosphoenolpyruvate carboxykinase and peroxisomeprolierator activated receptor gamma coactivator- mRNA[] and reduced phosphorylation o protein kinase C zetaisoorm [] were exhibited in the offspring. Yao et al. []have ound prenatal alcohol intake elevated expression oribbles and phosphatase and tensin homolog deleted onchromosome in both liver and muscle [,], leading toimpaired insulin sensitivity [, ]. In addition, increasedbeta-hydroxysteroid dehydrogenase type- level in liver andadipose tissue [] may also partly contribute to the insulinresistance caused by prenatal alcohol taking though elevatinglocal glucocorticoid levels.

.. Environmental Factors

... Biophenol A. Biophenol A, a biochemical material usedin plastic containers that are widely used in daily lie [], hasbeen ound that it may achieve similar effects with estrogen[,]. Studies have supported that biophenol A might becorrelated with the pathogenesis o DM [,]. A humanstudy perormed by Lang et al. [] has shown that the

biophenol A concentration in urine positively correlated withcardiovascular diseases and diabetes.

In rats, g/kgd biophenol A intake during pregnancyand lactating period may lead to insulin resistance in adultoffspring, and this effect can be largely enhanced by high atdiet afer birth []. Similar results have also been describedby Alonso-Magdalena et al. [] who urther ound that thealtered Ca+ signaling pathway and reduced cell numbersin pancreas might contribute to reduced insulin sensitivity.However, controversial conclusions have also been raisedout by Ryan et al. [] in CD- mice, which indicate thatperinatal exposure to ecologically relevant dose o BPA couldnot impair the glucose tolerance in the offspring. Tereore,

different biophenol A dosages applied in different animalmodels may vary the conclusion.

... Maternal Hypoxia. Data rom animal experiment hasound that exposure to hypoxia during pregnancy leads toinsulin resistance, impaired glucose homeostasis, and altered

expression o genes involved in insulin-signaling pathways inthe offspring []. Mechanisms underlying this relationshipare unclear since intrauterine hypoxia may partly correlatewith undernutrition. However, Camm et al. [] ound that,compared to prenatal undernutrition, prenatal hypoxia maycause different gene expression patterns in the liver andmuscle in adult offspring, including reduced expression ohepatic insulin receptorsubstrate , phospho-Akt, and muscleAkt, indicating that prenatal hypoxia may promote markerso insulin resistance independent o undernutrition.

... Maternal Smoking. Studies have reported the una-vorable effects o smoking on diabetes in adult [, ].However, a clearly causal relationship has only been oundbetween maternalsmoking and increasedrisk o DM in theoffspring. A human study perormed by Tiering et al. []had ound increased insulin levels in -year-old childrenafer prenatal smoking, and breast milk eeding made thisalteration even more magnicent. Tis nding is consistentwith the study perormed previously by Bruin et al. [ ] inanimals which indicated that both conception and lactationperiods were needed or nicotine exposure that may resultin permanent-cell loss and subsequent impaired glucosetolerance. In addition, Holloway et al. [] ound that etaland neonatal exposure to nicotine has transgenerationaleffects and insulin resistance can be ound in the F offspring.

Exact mechanism still remains largely unknown; reducedpancreas cell numbers and size and reduced expression o-cell marker genes such as pdx-, Pax-, and Nkx. []all have been addressed. In addition, data rom Chen et al.have indicated that nicotine may also downregulate geneexpression o appetite regulators neuropeptide Y and pro-opiomelanocortinin the arcuate nucleus o the hypothalamusin etal brain, which may consequently lead to unhealthyeating habits in the offspring and predispose high risk oobesity or diabetes [].

.. Prenatal Psychological Stress. It is already known thatexposure to high levels o maternal stress hormones during

pregnancy may produce detrimental effects on the offspring[]. Te effect o prenatal stress in programming DMhas been ound in both human and animal studies [].A retrospective study has shown that children exposed tostress caused by bereavement during their prenatal lie hadmore risk to DM later in lie []. Another human datarom Entringer et al. [] ound that maternal stressul lieexperiences may cause signicantly elevated -hour insulinand C-peptide levels under glucose tolerance test in youngadult offspring, indicating insulin resistance, which is inde-pendent o birth weight and amily history o diabetes. Teelucidation o the mechanism underlying this relationship isstill not clear. A nding rom a human study has shown that

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prenatal stress leads to shorter leukocyte telomere length inadult offspring [], which has also been ound to positivelycorrelate with the pathogenesis diabetes [] and childrenobese [].

.. Te Metabolic Situation during Pregnancy

... Obesity. Maternal obesity has risen dramatically overthe past years. Evidences rom human and animal stud-ies suggest that maternal obesity in pregnancy predisposeshyperinsulinemia, insulin resistance, and DM in the off-spring []. Shankar et al. [] have ound in mice thatthe male offspring with overweight mother may exhibit mag-nicent increase in body weight and adipose tissue content,which also combined with insulin resistance and increasedlevels o insulin, leptin, and resistin. Te precise underlyingmechanisms that contribute to increased susceptibility ooffspring to develop insulin resistance in later lie remainpoorly understood. Both increased number o apoptosis o

the etal pancreas cell [] and accelerated etal -cellgrowth andcell prolieration (which wasregardedas overloadworking and consequently end up to cell ailure) []were observed in animal offsprings with obese mother, whichmay all contribute to the increased blood glucose level aferbirth.In addition,increased hepatic lipogenesisand atty liverdisease [,] ound in the offspring exposed to maternalobesity also contribute to hepatic insulin resistance.

... High Gestational Glucose Concentration. Exposure toelevated intrauterine glucose environment has been oundto cause alterations in etal growth patterns, which predis-pose these inants to developing obesity, insulin resistance,and diabetes later in lie. So ar the effects o intrauter-ine hyperglycemia on the offspring have been studied inhuman in pregnant mothers with DM or with gestationaldiabetes and in diabetic animal models mainly caused bystreptozotocin treatment. Data accumulated rom thesesstudies uniormly show glucose intolerance in the offspring.Human study perormed by Boerschmann et al. [] hasindicated that, compared with those children with DM andnormal glycemia mothers, children with mothers with ges-tational diabetes mellitus exhibit overweight and increasedHOMA-IR. Another study rom Bush et al. [] in -year-old children also ound that maternal gestationalglucose concentration was inversely associated with offspringinsulin sensitivity. Insulin resistance was also observed in

rodent offspring prenatally under hyperglycemia environ-ment caused by streptozotocin injection [, ]. It seemsthat in utero diabetic environment in which the etusdevelops can increase the risk o diabetes in the child. Inaddition to genetic susceptibility, blunted insulin sensitivityin the offspring might largely contribute to this correlation.Relative gene expression was only explored in animal modelswhich indicated that intrauterine hyperglycemia inducedby streptozotocin injection resulted in increased hepaticgluconeogenic gene expression o glucose--phosphatase andphosphoenolpyruvate carboxykinase in the offspring []and the adult offspring o this cohort are prone to developinsulin resistance under high at diet []. A human study

ound that maternal diabetes might cause an inherent deectin-cell glucose sensitivity in the adult offspring [].

.. Maternal Hormone Levels during Pregnancy

... Prenatal estosterone. Prenatal testosterone overexpo-

sure has been considered to be correlated with polycysticovary syndrome in adult emale and was widely studied [,]. Animalexperiments perormed in sheep [, ], rodents[], and even monkeys [] have all conrmed thatprenatal testosterone overexposure leads to insulin resistancein the offspring. estosterone overexposure during etaldevelopment may impair insulin sensitivity pathways in bothliver and muscle [], increase hepatic gluconeogenesis [],and impair pancreas islet response to glucose [] in theoffspring.

... Prenatal Glucocorticoids. Synthetic glucocorticoidshave been used in pregnant women who are at risk o

preterm delivery to promote etal lung maturation. How-ever, concerns have already emerged about the metabolicdisorders caused by prenatal glucocorticoids excess. Studiesrom animal models have ound that prenatal glucocorticoidstreatment leads to increased hepatic gene expression ohepatocyte nuclear actor alpha [], phosphoenolpyruvatecarboxykinase [], and glucose--phosphatase [] in theoffspring, indicating elevated hepatic gluconeogenesis andhepatic insulin resistance. Nyirenda et al. also ound thatprenatal dexamethasone administration during late gestationmay result in elevated beta-HSD [] and glucocorticoidsreceptor [] expression in the liver, which may cause insulinresistance by increasing local glucocorticoids level [] or

activity.Similar phenomenon hasalso been ound whenincreased

endogenous glucocorticoids pass through maternal to etus.So ar, maternal nicotine [], ood or energy restriction [],and alcohol intake [] have all been ound to impair pla-cental barrier and consequently cause increased endogenousglucocorticoids in utero.

3. Part II: Postnatal Factors

.. New Born

... Catch-Up Growth. Catch-up growth, which appeared

afer lower birth body weight, is the issue that has beenstudied or years. Accumulated data suggest that low birthweight and catch-up growth are strongly associated withincreased risk o insulin resistance and type diabetes[]. Intriguingly, different periods o catch-up growthseem to cause different effects on glucose tolerance andinsulin sensitivity. Catch-up growth only in the rst yearafer birth seems to have no effect on insulin sensitivityin -year-old child [], while sustained catch-up growth(more than year afer birth) leads to higher insulin levelsin -year-old child [] or insulin resistance in -year-oldchild []. Compelling evidences raise the thrify catch-upat mechanisms, indicating that this growth trajectory is

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Obesity

Insulin resistance

Offspring

Stress

Obesity

Smoking

Hyperglycemia

Lactating mother

Early weaning

Overnutrition

Milk

F : Lactation and insulin resistance. It has been ound thatboth early weaning and overeeding by more milk intake maylead to insulin resistance in later lie. Maternal stress, obesity,hyperglycemia, and even smoking during lactation might also causereduced insulin sensitivity in the offspring, which suggest thatthe breast milk can be the agent, transerring altered levels ohormones, insulin, or atty acid contents rom maternal circulationto neonate.

characterized by a disproportionately higher rate o at gainand redistribution o glucose rom skeletal muscle to adiposetissue, contributing to insulin resistance in skeletal musclewhile hyperresponsiveness to insulin in adipose tissue [].

... Lactation. Lactation is also a sensitive period or theprogramming o later metabolic disorders (Figure ).

Early Weaning. Early weaning may lead to undernutrition,which consequently program metabolic disorders later inlie. Hyperglycaemia, higher insulin resistance index, andhyperleptinemia wereobserved in -month-old ratsthat wereweaned early, which were accompanied with central leptinresistance [].

Overnutrition.Overnutrition during lactation period is asso-ciated with metabolic disorders in later lie. An experimentconducted in male mice by Pentinat et al. [] has oundthat overgrowth mice caused by reduced pups per damsduring lactation may develop metabolic disorders at theage o months, including obesity, insulin resistance, andglucose intolerance. Similar results have also been ound byPlagemann et al. in their serial experiments perormed onrats [,]. Strikingly, the effect o neonatal overnutritionon diabetes risk can be inherent to subsequent generations.

Impaired glucose tolerance was ound in the adult male miceoffspring with the ather overed neonatally, and periph-eral insulin resistance was ound in the grand offspring,although these two generations o animals were not exposedto overnutrition during the neonatal time []. Increasedoxidative stress in liver and reduced hepatic insulin signalingpathways [] may underlie effects o neonatal overeeding.Moreover, early overeeding leads to permanent dysregula-tion o hypothalamic circuits in animal models, includingreduced negative eedback to the satiety signal insulin onmedial arcuate neurons in juvenile as well as adult rats[] and increased hypothalamic insulin receptor promotermethylation ratio []. Tis maylead to unctional resistance

to insulin and leptin, which may underlie permanently anincrease in ood intake, overweight, and insulin resistance.

Maternal Situation during Lactation. Maternal physical orpathological situation during lactation may imprint elevatedrisk o metabolic diseases in the offspring. Experiments

in animals have showed that mother under stress [],with obesity [], and exposed to nicotine [] duringlactating period may lead to obesity and insulin resistance inadult offspring, which implicates that the postnatal maternalenvironment is a major effecter o metabolic outcome inthe offspring. It is also ound that ostering nondiabeticoffspring to diabetic dams may produce smaller offspringwith altered arcuate nucleus neuropeptide Y, agouti-relatedpeptide, and pro-opiomelanocortin expression []. Teunderlying mechanism is still ar more conclusive. Tereore,the breast milk can be the agent; altered levels o hormones,insulin, or atty acid contents may enter the milk rommaternal circulation and then can be transerred to neonate.

... Neonatal Stress. Limited data rom animal studies haveound that stress caused by handling during the neonatalperiod may also be detrimental. Studies have ound thatneonatal mice, which were under maternal separation plussubcutaneous sham injection during the lactation period,developed hyperglycemia, hyperinsulinemia, hyperleptine-mia, and hyperlipidemia in adult under asting [, ].Increased plasma corticosterone and adrenocorticotropinwere ound in these animals [, ] which might beresponsible or the diabetic alteration.

... Neonatal Hormone Exposure. Tere are evidences indi-

cated that exposure to some hormones during neonatal liemay predispose metabolic disorders in adult lie. Glucocor-ticoids treatment in neonatal rats caused increased astingand postprandial blood glucose, which is combined withmagnicent insulin resistance and lipid disorder in later lie[]. In addition, in newborn emale rats, one subcutaneousinjection with . mg oestradiol benzoate led to reducedinsulin sensitivity in adult lie by inducing inammationand disturbance glucose metabolism in skeletal muscle [],while mg testosterone injection to emale neonatal ratscaused insulin resistance and increased mesenteric adiposetissue content in adult lie [].

... Neonatal Monosodium Glutamate Intake. Monosodiumglutamate (MSG) is the sodium salt o glutamic acid, andit is a avor enhancer that is widely used in Chineseood. Te study o neonatal MSG treatment on neonatalanimals has been perormed since the s and so arthere are plenty o animal experiments that have evidenceddetrimental effects o MSG administration during early lietime, including growth retardation, retinal degeneration,and increased proinammation in hippocampus []. In, Hirata et al. ound that MSG-treated animals developedcentral obesity, altered glucose tolerance, and hyperinsuli-naemia []. More similar evidences have been documentedin later experiments [], indicating that neonatal MSG

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treatment may lead to increased risk o diabetes in adult lie.MSG may cause obesity and nonatty liver [, ] andincreased mRNA level o IL-, NF, resistin, and leptin in

visceral at tissue [], which might all predispose insulinresistance in later lie.

.. Childhood

... Low Socioeconomic Status. Socioeconomic status hasa notable impact on health disparities, including type diabetes risk. Low childhood socioeconomic status was oundlinked to type diabetes in some studies [, ] andthe association remained even afer being adjusted or adultsocioeconomic status and obesity. Low childhood socioe-conomic status was considered to be a robust independentactor o incidence o type diabetes in adulthood andthe risk was ound greater when childhood socioeconomicstatus combined with adult obesity. Poornutrition, unhealthybehaviors, and limited access to material goods and limited

socioeconomic opportunities may contribute to altered bodycomposition in laterlie, which might explain the relationshipbetween childhood socioeconomic position and metabolicdisorders in adult.

... Famine. Undernutrition during childhood has beenound to be associated with an increased type diabetes riskin adulthood. Study in women who had experienced Dutchamine has shown that short period o moderate or severeundernutrition during childhood increases type diabetesrisk in adulthood [].

... Obesity. Childhood obesity is an issue o serious

medical and social concern. Many studies have demonstratedthe positive correlations between childhood obesity andadult metabolic disorders, including type diabetes [,,]. Obesity, which mostly caused by high caloric oodintake, may always combine with insulin resistance [].An unavorable programming o body composition could beone mechanism linking early childhood growth with laterincreased risk or type diabetes. In addition, a study per-ormed in French children aged yr hassuggested thatobese children have signicantly shorter leukocyte telomeresthan their nonobese counterparts []. Leukocyte telomerelength (LL), a marker o biological age, is associated withage-related conditions including cardiovascular disease and

type diabetes which highlights a potentially deleteriousimpact o early onset obesity on uture health.

4. Conclusion

Tere is increasing recognition that the risk o type diabetescan be inuenced by prenatal, neonatal, and childhood expo-sures. In the present studies, we have reviewed nutritional,environmental, and physiological actors rom prenatal topostnatal periods, which have been documented in studiesthat may correlate with insulin resistance or type diabetes inadult lie. Further investigations are still required. However,relative knowledge education might be successul in women

o child-bearing age and ultimate to reduce the disease risk intheir potential offspring.

Acknowledgments

Tis work is supported by the National Nature Science

Foundation o China: , , and ;Hebei Province Nature Science Foundation: Hand H; and the Scientic Foundation o theDepartment o Public Health o Hebei Province: and .

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