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      Nutrition in Pregnancy: Optimising Maternal Diet and Fetal Adaptations to Altered Nutrient Supply

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          Abstract

          Maternal nutrition during pregnancy, and how this impacts placental and fetal growth and metabolism, is of considerable interest to women, their partners and their health care professionals. In developing countries, maternal undernutrition is a major factor contributing to adverse pregnancy outcomes. Conversely, with the increased prevalence of high calorie diets and resulting overweight and obesity issues in developed countries, the impact of this overnutrition situation upon pregnancy outcome is highlighted as a contributing factor for adverse metabolic outcomes in offspring later in life. Further, while low or excessive food intake per se is an important aspect of pregnancy development, the specific role that the placenta plays in nutrient metabolism and overall nutrient supply to the fetus in situations of undernutrion, overnutrition or poor diet composition is still poorly defined. Both epidemiology and animal studies now highlight that undernutrition, overnutrition, and diet composition negatively impact fetoplacental growth and metabolic patterns, having adverse later life metabolic effects for the offspring. This issue aims to highlight new research in a number of these abovementioned areas across the early life course. A great deal of data now highlights the periconceptional period as a critical period upon which insults may generate later life physiological and metabolic changes in the resulting offspring. In the review submitted by Padhee and colleagues [1], the procedures of ARTs are examined, specifically in terms of how common procedures associated with the handling and preparation of gametes and embryos may impact later life metabolism, particularly impacting offspring cardiometabolic health. These later life defective metabolic effects are also understood to be established during pregnancy. In surveying preconceptional women, pregnant and lactating women and women of reproductive age, Cuervo et al. report that these groups are not appropriately consuming foods for their physiological status, based upon the Spanish dietary guidelines and highlight a real need for improved education and community outreach programs to these groups of women to ensure adequate maternal and thus fetal nutrition [2]. Poor maternal nutritional intake after the periconceptional period during pregnancy can also negatively impact fetal genetic growth trajectory and can result in fetal growth restriction. Vonnahme et al. [3], describe the effects of maternal undernutrition on vascularity of nutrient transferring tissue during different stages of pregnancy. In addition to maternal nutrient supply, the effectiveness of the placenta in transporting nutrients and oxygen to the fetus is important in determining fetal growth. A range of adaptations to placental development occur when the fetus is growth restricted and these are described by Zhang et al. [4]. Regardless of the cause of low birth weight, Zheng et al. show a relationship between the placental microbiome and fetal growth [5]. Zohdi et al. describe the effects of maternal protein restriction during pregnancy on fetal development that increase the risk of cardiovascular disease later in life [6]. Davis et al. illustrate the importance of the adrenal gland in the fetal adaptation for placental insufficiency, highlighting the important role of norepinephrine in regulating fetal growth but not pancreatic mass in the growth restricted fetus [7]. Wood-Bradley and team provide a review of the literature surrounding the potential mechanisms by which maternal nutrition (focusing on malnutrition due to protein restriction, micronutrient restriction and excessive fat intake) influences offspring kidney development and thereby function in later life [8]. In the same light, Blumfield et al. detail evidence that a maternal diet during pregnancy that is low in protein is related to higher systolic blood pressure in childhood [9]. Furthermore, Colon-Ramos and colleagues investigated the potential association between maternal dietary patterns during pregnancy and birth outcomes in a diverse population with a historically high burden of low birth weight and other adverse birth outcomes [10]. Experiences in the perinatal period also play a key role in defining how offspring respond to stress(es) in postnatal life. To this point, Tsuduki and colleagues report upon the impact a high fat diet during mouse lactation, where it appears to increase the susceptibility of later life obesity induced through postnatal social stress [11]. This paper highlights the importance of understanding how an early life environment predisposes offspring to potential detrimental responses to postnatal adverse situations. In a review by Dunlop et al., the impact of fetal growth restriction on postnatal metabolism in skeletal muscle, but also the effect of a “second hit”, such as a Western diet in postnatal life, is presented [12]. While meeting dietary guidelines is important, overall maternal health status also plays a pivotal role in determining fetal nutrient supply. In situations of maternal disease, such as infection with human immunodeficiency virus (HIV), the ability of the mother to consume sufficient substrates to maintain herself and meet fetal demands is often compromised. In situations of HIV, resting energy expenditure is increased and the disease may limit dietary intake and reduce nutrient absorption, in addition to influencing the progression of HIV disease as reported by Ramlal and colleagues [13]. Their study described typical diets of HIV-infected, pregnant Malawian women and highlighted that poor quality maternal diets should be enhanced to meet demands of this particular group of pregnant women, vulnerable to both HIV and malnutrition. While deficiencies in nutrition during pregnancy can result in adverse offspring outcomes, once pregnant, maternal weight gain during and after pregnancy are critical issues for maternal and fetal health as well. In the pilot RCT report lead by Martin et al., a cohort of women were recruited with the aim of reducing postpartum weight retention and improving breastfeeding outcomes [14]. The findings indicate that the approach reported is feasible and acceptable to pregnant women and that the methodology, including the collection of blood for biomarker assessment, could be adapted based on qualitative feedback to a larger, adequately powered RCT. Assessing maternal body composition, as part of monitoring maternal well-being, prior to and during pregnancy is critical to estimate the requirements for dietary energy during gestation and when investigating relationships between maternal nutritional status and offspring development. Forsum and co-workers investigate the possibility of estimating body density and the use of a two-component model (2CM) to calculate total body fat concluding it may present a new clinically appropriate methodology [15]. Many nutritional studies in pregnancy have focussed on the impact of changes in total or macronutrient intake. This current issue features several studies that expand our knowledge regarding nutrient uptake during pregnancy, but have focused on changes in micronutrients during pregnancy. Grieger and Clifton, provide updated evidence from epidemiological and RCTs on the impact of dietary and supplemental intakes of omega-3 long-chain polyunsaturated fatty acids, zinc, folate, iron, calcium, and vitamin D, as well as dietary patterns, on infant birth weight [16]. Additionally, in studying maternal intakes of polyunsaturated fatty acids (PUFAs), Bascuñán et al. report a Chilean study that highlights the need for new strategies to improve n-3 PUFA intake throughout pregnancy and breastfeeding periods and the need to develop dietary interventions to improve the quality of consumed foods with particular emphasis on n-3 PUFA for adequate fetal development [17]. Fish intake during pregnancy is recognized as an important source of PUFAs. Starling and co-workers present a systematic review of fish intake during pregnancy and fetal neurodevelopment [18]. The review covers approximately a 14 year period of publications between January 2000 and March 2014 involving over 270 papers, of which only eight were selected for a qualitative comparison of study findings. Deficiencies in a range of micronutrients in low vs middle income countries that may act through epigenetic mechanisms to influence fetal development and risk of chronic disease in adult life are identified by Darnton-Hill et al. [19]. They also discuss supplementation programs. One particular micronutrient that is important for sulphonation of steroids and hormones is sulphate. Dawson et al. describe the requirements for sulphate during pregnancy, the consequences of reduced sulphonation capacity and the use of animal models to adequately understand the role of sulphate in human pregnancy [20]. Folic acid and Vitamin B12, are crucial factors for metabolic pathways, and have been extensively studied and demonstrated to play important roles in preventing the development of neural tube defects (NTDs). Wang et al. present data that in a local Chinese population consumption of non-staple foods such as milk, fresh fruits, and nuts were associated with decreasing NTDs risk in offspring [21]. Further independent roles for folate and Vitamin B12 deficiency amongst pregnant women are presented in this issue. The relationship between maternal Vitamin B12 neonatal HDL is presented by Adaikalakotwewari et al. [22], and folate deficiency resulting in birth defects is highlighted by Li et al., who present a mouse model to provide evidence that folate deficiency can impair decidual angiogenesis [23]. The importance of adequate Vitamin D in women of reproductive age and its role in fetal development is of great interest and importance. A review of calcitrol biosynthesis during pregnancy, particularly by the placenta is presented by Olmos-Ortiz et al. [24]. Additionally, Choi et al. describe the high prevalence of Vitamin D deficiency in Korean women during pregnancy [25], particularly in the winter, while Yu et al. report the cord blood Vitamin D in babies born in Shanghai [26]. Finally regarding Vitamin D, the impact of sun exposure and Vitamin D supplementation on achieving appropriate Vitamin D status in women whom are breastfeeding is explored by Dawodu and colleagues [27]. In this issue, several new studies highlighted the importance of diet intake and composition upon maternal and fetal well-being parameters in human population and animal studies. Many of these studies show that deficiencies in consumption/delivery of components (e.g., protein, vitamins, PUFAs) of a diet can lead to adverse fetal/offspring development and detail how consumption of certain foods may have beneficial effects on fetal/offspring growth and development. We hope that the articles contained within this issue, and the material they reference and describe, are of interest to women, their partners and their health care professionals in promoting continual and informed dialogue about nutrition in pregnancy.

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          Most cited references 27

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          Micronutrients in Pregnancy in Low- and Middle-Income Countries

          Pregnancy is one of the more important periods in life when increased micronutrients, and macronutrients are most needed by the body; both for the health and well-being of the mother and for the growing foetus and newborn child. This brief review aims to identify the micronutrients (vitamins and minerals) likely to be deficient in women of reproductive age in Low- and Middle-Income Countries (LMIC), especially during pregnancy, and the impact of such deficiencies. A global prevalence of some two billion people at risk of micronutrient deficiencies, and multiple micronutrient deficiencies of many pregnant women in LMIC underline the urgency to establishing the optimal recommendations, including for delivery. It has long been recognized that adequate iron is important for best reproductive outcomes, including gestational cognitive development. Similarly, iodine and calcium have been recognized for their roles in development of the foetus/neonate. Less clear effects of deficiencies of zinc, copper, magnesium and selenium have been reported. Folate sufficiency periconceptionally is recognized both by the practice of providing folic acid in antenatal iron/folic acid supplementation and by increasing numbers of countries fortifying flours with folic acid. Other vitamins likely to be important include vitamins B12, D and A with the water-soluble vitamins generally less likely to be a problem. Epigenetic influences and the likely influence of micronutrient deficiencies on foetal origins of adult chronic diseases are currently being clarified. Micronutrients may have other more subtle, unrecognized effects. The necessity for improved diets and health and sanitation are consistently recommended, although these are not always available to many of the world’s pregnant women. Consequently, supplementation programmes, fortification of staples and condiments, and nutrition and health support need to be scaled-up, supported by social and cultural measures. Because of the life-long influences on reproductive outcomes, including inter-generational ones, both clinical and public health measures need to ensure adequate micronutrient intakes during pregnancy, but also during adolescence, the first few years of life, and during lactation. Many antenatal programmes are not currently achieving this. We aim to address the need for micronutrients during pregnancy, the importance of micronutrient deficiencies during gestation and before, and propose the scaling-up of clinical and public health approaches that achieve healthier pregnancies and improved pregnancy outcomes.
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            Placental Adaptations in Growth Restriction

            The placenta is the primary interface between the fetus and mother and plays an important role in maintaining fetal development and growth by facilitating the transfer of substrates and participating in modulating the maternal immune response to prevent immunological rejection of the conceptus. The major substrates required for fetal growth include oxygen, glucose, amino acids and fatty acids, and their transport processes depend on morphological characteristics of the placenta, such as placental size, morphology, blood flow and vascularity. Other factors including insulin-like growth factors, apoptosis, autophagy and glucocorticoid exposure also affect placental growth and substrate transport capacity. Intrauterine growth restriction (IUGR) is often a consequence of insufficiency, and is associated with a high incidence of perinatal morbidity and mortality, as well as increased risk of cardiovascular and metabolic diseases in later life. Several different experimental methods have been used to induce placental insufficiency and IUGR in animal models and a range of factors that regulate placental growth and substrate transport capacity have been demonstrated. While no model system completely recapitulates human IUGR, these animal models allow us to carefully dissect cellular and molecular mechanisms to improve our understanding and facilitate development of therapeutic interventions.
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              The Placental Microbiome Varies in Association with Low Birth Weight in Full-Term Neonates

              Substantial evidence indicated that low birth weight was an independent risk factor for obesity, impaired glucose regulation, and diabetes later in life. However, investigations into the association between low birth weight and placental microbiome in full-term neonates are limited. Placentas were collected from low birth weight (LBW) and normal birth weight (NBW) full-term neonates (gestational age 37 w0d–41 w6d) consecutively born at Peking Union Medical College Hospital. The anthropometric measurements were measured and 16S ribosomal DNAamplicon high-throughput sequencing were utilized to define bacteria within placenta tissues. It showed that birth weight, ponderal index, head circumference, and placenta weight were significantly lower in LBW than NBW neonates (p < 0.05). The operational taxonomic units (OTUs) (p < 0.05) and the estimators of community richness (Chao) indexes (p < 0.05) showed a significantly lower diversity in LBW than NBW neonates. There were significant variations in the composition of placenta microbiota between the LBW and NBW neonates at the phylum and genus level. Furthermore, it indicated that Lactobacillus percentage was positively associated with birth weight (r = 0.541, p = 0.025). In conclusion, our present study for the first time detected the relationship between birth weight and placental microbiome profile in full-term neonates. It is novel in showing that the placental microbiome varies in association with low birth weight in full-term neonates.
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                Author and article information

                Affiliations
                [1 ]Early Origins of Adult Health Research Group, Sansom Institute for Health Research, University of South Australia, Adelaide 5001, Australia
                [2 ]The Susan Vitali-Lovell Laboratories for Studies in Fetal Programming of Human Health Risks, Department of Obstetrics and Gynaecology and Physiology and Pharmacology, Western University, London, ON N6A-5C1, Canada; tim.regnault@ 123456uwo.ca
                Author notes
                [* ]Correspondence: janna.morrison@ 123456unisa.edu.au ; Tel.: +618-8302-2166
                Journal
                Nutrients
                Nutrients
                nutrients
                Nutrients
                MDPI
                2072-6643
                04 June 2016
                June 2016
                : 8
                : 6
                nutrients-08-00342
                10.3390/nu8060342
                4924183
                27271666
                © 2016 by the authors; licensee MDPI, Basel, Switzerland.

                This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC-BY) license ( http://creativecommons.org/licenses/by/4.0/).

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