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      Liver Proteome Profile of Growth Restricted and Appropriately Grown Newborn Wistar Rats Associated With Maternal Undernutrition

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          Abstract

          Background

          Fetal growth restriction (FGR) has been associated with adverse perinatal outcomes and epigenetic modifications that impact gene expression leading to permanent changes of fetal metabolic pathways and thereby influence development of disease in childhood and adult life. In this study, we investigated the result of maternal food restriction on liver protein expression in Wistar male newborn pups.

          Materials & Methods

          Ten (n = 10) timed pregnant Wistar rats on their 14th day of gestation were randomly assigned to either control (n = 4) or food restricted group (n = 6). The control group had ad libitum access to food. In the food restricted group, maternal diet was limited in a moderate fashion (50%) from day 15 of pregnancy until delivery. All rats delivered spontaneously on day 21 and newborn pups were immediately weighed. Pups born to normally nourished mothers were considered as controls, while pups born to food restricted mothers were subdivided into two groups, based on their birth weight: growth restricted (FGR) and appropriately grown (non-FGR). Rats were euthanized immediately after birth and liver tissues of 11 randomly selected male offspring (FGR n = 4, non-FGR n = 4, control n = 3) were collected and analyzed using quantitative proteomics.

          Results

          In total 6,665 proteins were profiled. Of these, 451 and 751 were differentially expressed in FGR and non-FGR vs. control, respectively, whereas 229 proteins were commonly expressed. Bioinformatics analysis of the differentially expressed proteins (DEPs) in FGR vs. control revealed induction of the super-pathway of cholesterol biosynthesis and inhibition of thyroid hormone metabolism, fatty acid beta oxidation and apelin liver signaling pathway. Analysis of DEPs in non-FGR vs. control groups showed inhibition of thyroid hormone metabolism, fatty acid beta oxidation, and apelin liver signaling pathway.

          Conclusion

          This study demonstrates the impact of prenatal food restriction on the proteomic liver profile of FGR and non-FGR offspring underlying the importance of both prenatal adversities and birth weight on liver-dependent postnatal disease.

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          Most cited references51

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          Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth

          Two follow-up studies were carried out to determine whether lower birthweight is related to the occurrence of syndrome X-Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia. The first study included 407 men born in Hertfordshire, England between 1920 and 1930 whose weights at birth and at 1 year of age had been recorded by health visitors. The second study included 266 men and women born in Preston, UK, between 1935 and 1943 whose size at birth had been measured in detail. The prevalence of syndrome X fell progressively in both men and women, from those who had the lowest to those who had the highest birthweights. Of 64-year-old men whose birthweights were 2.95 kg (6.5 pounds) or less, 22% had syndrome X. Their risk of developing syndrome X was more than 10 times greater than that of men whose birthweights were more than 4.31 kg (9.5 pounds). The association between syndrome X and low birthweight was independent of duration of gestation and of possible confounding variables including cigarette smoking, alcohol consumption and social class currently or at birth. In addition to low birthweight, subjects with syndrome X had small head circumference and low ponderal index at birth, and low weight and below-average dental eruption at 1 year of age. It is concluded that Type 2 diabetes and hypertension have a common origin in sub-optimal development in utero, and that syndrome X should perhaps be re-named "the small-baby syndrome".
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            Maternal and fetal risk factors for stillbirth: population based study

            Objective To assess the main risk factors associated with stillbirth in a multiethnic English maternity population. Design Cohort study. Setting National Health Service region in England. Population 92 218 normally formed singletons including 389 stillbirths from 24 weeks of gestation, delivered during 2009-11. Main outcome measure Risk of stillbirth. Results Multivariable analysis identified a significant risk of stillbirth for parity (para 0 and para ≥3), ethnicity (African, African-Caribbean, Indian, and Pakistani), maternal obesity (body mass index ≥30), smoking, pre-existing diabetes, and history of mental health problems, antepartum haemorrhage, and fetal growth restriction (birth weight below 10th customised birthweight centile). As potentially modifiable risk factors, maternal obesity, smoking in pregnancy, and fetal growth restriction together accounted for 56.1% of the stillbirths. Presence of fetal growth restriction constituted the highest risk, and this applied to pregnancies where mothers did not smoke (adjusted relative risk 7.8, 95% confidence interval 6.6 to 10.9), did smoke (5.7, 3.6 to 10.9), and were exposed to passive smoke only (10.0, 6.6 to 15.8). Fetal growth restriction also had the largest population attributable risk for stillbirth and was fivefold greater if it was not detected antenatally than when it was (32.0% v 6.2%). In total, 195 of the 389 stillbirths in this cohort had fetal growth restriction, but in 160 (82%) it had not been detected antenatally. Antenatal recognition of fetal growth restriction resulted in delivery 10 days earlier than when it was not detected: median 270 (interquartile range 261-279) days v 280 (interquartile range 273-287) days. The overall stillbirth rate (per 1000 births) was 4.2, but only 2.4 in pregnancies without fetal growth restriction, increasing to 9.7 with antenatally detected fetal growth restriction and 19.8 when it was not detected. Conclusion Most normally formed singleton stillbirths are potentially avoidable. The single largest risk factor is unrecognised fetal growth restriction, and preventive strategies need to focus on improving antenatal detection.
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              The consequences of fetal growth restriction on brain structure and neurodevelopmental outcome.

              Fetal growth restriction (FGR) is a significant complication of pregnancy describing a fetus that does not grow to full potential due to pathological compromise. FGR affects 3-9% of pregnancies in high-income countries, and is a leading cause of perinatal mortality and morbidity. Placental insufficiency is the principal cause of FGR, resulting in chronic fetal hypoxia. This hypoxia induces a fetal adaptive response of cardiac output redistribution to favour vital organs, including the brain, and is in consequence called brain sparing. Despite this, it is now apparent that brain sparing does not ensure normal brain development in growth-restricted fetuses. In this review we have brought together available evidence from human and experimental animal studies to describe the complex changes in brain structure and function that occur as a consequence of FGR. In both humans and animals, neurodevelopmental outcomes are influenced by the timing of the onset of FGR, the severity of FGR, and gestational age at delivery. FGR is broadly associated with reduced total brain volume and altered cortical volume and structure, decreased total number of cells and myelination deficits. Brain connectivity is also impaired, evidenced by neuronal migration deficits, reduced dendritic processes, and less efficient networks with decreased long-range connections. Subsequent to these structural alterations, short- and long-term functional consequences have been described in school children who had FGR, most commonly including problems in motor skills, cognition, memory and neuropsychological dysfunctions.
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                Author and article information

                Contributors
                Journal
                Front Endocrinol (Lausanne)
                Front Endocrinol (Lausanne)
                Front. Endocrinol.
                Frontiers in Endocrinology
                Frontiers Media S.A.
                1664-2392
                28 May 2021
                2021
                : 12
                : 684220
                Affiliations
                [1] 1 Second Department of Obstetrics and Gynaecology, Medical School, National and Kapodistrian University of Athens , Athens, Greece
                [2] 2 Beckman Research Institute, City of Hope National Medical Center , Duarte, CA, United States
                [3] 3 First Department of Paediatrics, Medical School, National and Kapodistrian University of Athens , Athens, Greece
                [4] 4 Institute for Life Sciences, University of Southampton , Southampton, United Kingdom
                Author notes

                Edited by: Kunal Sharan, Central Food Technological Research Institute (CSIR), India

                Reviewed by: Alexandre-Gouabau Marie-Cécile, Le nouvel Institut national de recherche sur l’agriculture, l’alimentation et l’environnement en France INRAE, France; Maria Elisabeth Street, Azienda Unita Sanitaria Locale di Reggio Emilia, Italy

                *Correspondence: Makarios Eleftheriades, makarios@ 123456hotmail.co.uk ; melefth@ 123456med.uoa.gr

                ‡These authors have contributed equally to this work and share first authorship

                †Present address: Spiros D. Garbis, Proteas Bioanalytics Inc., BioLabs at the Lundquist Institute, Torrance, CA, United States

                This article was submitted to Pediatric Endocrinology, a section of the journal Frontiers in Endocrinology

                Article
                10.3389/fendo.2021.684220
                8195994
                34aa2f4b-6ca9-4948-bdca-e7e833f8cfef
                Copyright © 2021 Sarli, Manousopoulou, Efthymiou, Zouridis, Potiris, Pervanidou, Panoulis, Vlahos, Deligeoroglou, Garbis and Eleftheriades

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 23 March 2021
                : 04 May 2021
                Page count
                Figures: 8, Tables: 2, Equations: 0, References: 51, Pages: 13, Words: 4458
                Funding
                Funded by: Procter and Gamble 10.13039/100004357
                Award ID: "George Papanikolaou 2018-2020"
                Categories
                Endocrinology
                Original Research

                Endocrinology & Diabetes
                fgr,fetal programming,food restriction,metabolic disorders,liver proteomics

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