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      Earlier Menarche Is Associated with Lower Insulin Sensitivity and Increased Adiposity in Young Adult Women

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          Abstract

          Objective

          We aimed to assess whether age at menarche was associated with insulin sensitivity in young adult women.

          Methods

          We studied 54 healthy young women aged 20–30 years. Participants were grouped according to age at menarche: Early (≤11.0 years; n=13), Average (>12.0 and ≤13.0 years; n=28), and Late (≥14.0 years, n=13). Primary outcome was insulin sensitivity measured using intravenous glucose tolerance tests and Bergman’s minimal model. Body composition was assessed using whole-body dual-energy X-ray absorptiometry.

          Results

          Earlier menarche was associated with lower insulin sensitivity (p=0.015). There was also a continuous increase in adiposity with younger age at menarche, which was associated with increased weight (p=0.001), BMI (p=0.002), total body fat (p=0.049), and truncal fat (p=0.020). Stratified analyses showed that insulin sensitivity in Early women (5.5 x10 -4·min -1(mU/l)) was lower than in Average (8.0 x10 -4·min -1(mU/l), p=0.021) and Late (8.6 x10 -4·min -1(mU/l), p=0.033) groups. Early women (weight=66.1 kg; BMI=24.1 kg/m 2) were considerably heavier and fatter than Average (59.0 kg, p=0.004; 21.4 kg/m 2, p=0.002) and Late (57.0 kg, p=0.001; 20.8 kg/m 2, p=0.0009) women.

          Conclusions

          Early menarche is associated with lower insulin sensitivity and increased adiposity in young adulthood, potentially increasing the risk of type 2 diabetes and the metabolic syndrome later in life.

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          Most cited references 45

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          The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration.

          During the past decade, possible advancement in timing of puberty has been reported in the United States. In addition, early pubertal development and an increased incidence of sexual precocity have been noticed in children, primarily girls, migrating for foreign adoption in several Western European countries. These observations are raising the issues of current differences and secular trends in timing of puberty in relation to ethnic, geographical, and socioeconomic background. None of these factors provide an unequivocal explanation for the earlier onset of puberty seen in the United States. In the formerly deprived migrating children, refeeding and catch-up growth may prime maturation. However, precocious puberty is seen also in some nondeprived migrating children. Attention has been paid to the changing milieu after migration, and recently, the possible role of endocrine- disrupting chemicals from the environment has been considered. These observations urge further study of the onset of puberty as a possible sensitive and early marker of the interactions between environmental conditions and genetic susceptibility that can influence physiological and pathological processes.
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            Role of brain insulin receptor in control of body weight and reproduction.

            Insulin receptors (IRs) and insulin signaling proteins are widely distributed throughout the central nervous system (CNS). To study the physiological role of insulin signaling in the brain, we created mice with a neuron-specific disruption of the IR gene (NIRKO mice). Inactivation of the IR had no impact on brain development or neuronal survival. However, female NIRKO mice showed increased food intake, and both male and female mice developed diet-sensitive obesity with increases in body fat and plasma leptin levels, mild insulin resistance, elevated plasma insulin levels, and hypertriglyceridemia. NIRKO mice also exhibited impaired spermatogenesis and ovarian follicle maturation because of hypothalamic dysregulation of luteinizing hormone. Thus, IR signaling in the CNS plays an important role in regulation of energy disposal, fuel metabolism, and reproduction.
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              Insulin resistance during puberty: results from clamp studies in 357 children.

              Insulin resistance may be an important cause of a constellation of cardiovascular risk factors in adults, and onset of this syndrome may occur in childhood. However, children normally experience transient insulin resistance at puberty. There were 357 normal children (159 girls, 198 boys) age 10-14 years who underwent euglycemic clamp studies to assess the effects of Tanner stage (T), sex, ethnicity, and BMI on insulin resistance. Insulin resistance increased immediately at the onset of puberty (T2), but returned to near prepubertal levels by the end of puberty (T5). Its peak occurred at T3 in both sexes, and girls were more insulin resistant than boys at all T stages. White boys appeared to be more insulin resistant than black boys; no difference was seen between white and black girls. Insulin resistance was strongly related to BMI, triceps skinfold thickness, and waist circumference, and this relationship was independent of Tanner stage or sex. Differences in BMI and adiposity did not, however, entirely explain the insulin resistance of puberty. These results demonstrate that 1) significant differences in insulin resistance are present between boys and girls; 2) insulin resistance increases significantly at T2, T3, and T4, but decreases to near prepubertal levels at T5; and 3) while insulin resistance is related to BMI and anthropometric measures of fatness, these factors do not completely explain the insulin resistance that occurs during the Tanner stages of puberty.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                10 June 2015
                2015
                : 10
                : 6
                Affiliations
                [1 ]Liggins Institute, University of Auckland, Auckland, New Zealand
                [2 ]School of Nursing, Faculty of Medical and Health Sciences, Auckland, University of Auckland
                Faculty of Biology, SPAIN
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: DAW WSC PLH. Performed the experiments: DAW DLR. Analyzed the data: JGBD. Wrote the paper: JGBD WSC PLH DAW.

                Article
                PONE-D-14-53010
                10.1371/journal.pone.0128427
                4464528
                26061526

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                Counts
                Figures: 1, Tables: 1, Pages: 10
                Product
                Funding
                This work was funded by a Southern Trust Grant (DAW WSC). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of this manuscript.
                Categories
                Research Article
                Custom metadata
                The clinical data cannot be made available in a public repository due to strict conditions of the ethics approval of our study. Nonetheless, anonymized and unidentifiable data would be made available to other investigators upon request. For this purpose, anyone interested should contact the senior author Prof Wayne Cutfield ( w.cutfield@ 123456auckland.ac.nz ).

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