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Choline: Exploring the Growing Science on Its Benefits for Moms and Babies

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Choline: Exploring the Growing Science on Its Benefits for Moms and Babies nutrients Communication Choline: Exploring the Growing Science on Its Benefits for Moms and Babies Hunter W. Korsmo 1,2 , Xinyin Jiang 1,2,* and Marie A. Caudill 3,* 1 Program in Biochemistry, Graduate Center of the City University of New York, New York, NY 10016, USA 2 Department of Health and Nutrition Sciences, Brooklyn College of the City University of New York, Brooklyn, NY 11210, USA 3 Division of Nutritional Sciences, Cornell University, Ithaca, NY 14853, USA * Correspondence: [email protected] (X.J.); [email protected] (M.A.C.) Received: 2 July 2019; Accepted: 5 August 2019; Published: 7 August 2019 Abstract: The importance of ensuring adequate choline intakes during pregnancy is increasingly recognized. Choline is critical for a number of physiological processes during the prenatal period with roles in membrane biosynthesis and tissue expansion, neurotransmission and brain development, and methyl group donation and gene expression. Studies in animals and humans have shown that supplementing the maternal diet with additional choline improves several pregnancy outcomes and protects against certain neural and metabolic insults. Most pregnant women in the U.S. are not achieving choline intake recommendations of 450 mg/day and would likely benefit from boosting their choline intakes through dietary and/or supplemental approaches. Keywords: choline; placenta; epigenetic programming; pregnancy outcomes; cognitive development 1. Introduction The importance of ensuring adequate choline intakes during pregnancy is increasingly recognized. The American Medical Association (AMA) in 2017 published new advice stating that prenatal vitamin supplements should contain ‘evidence-based’ amounts of choline [1]. Similarly, in 2018, the American Academy of Pediatrics recognized choline as a ‘brain-building’ nutrient and called upon pediatricians to ensure pregnant women and young children have adequate intakes of choline [2]. Choline, like vitamin D and docosahexaenoic acid (DHA), can be synthesized in the body but not in amounts sufficient to meet metabolic demands. In 1998, choline was recognized as an essential nutrient by the Institute of Medicine (now National Academy of Medicine) when it established dietary recommendations in the form of adequate intakes [3]. The choline adequate intake (AI) level is 425 mg choline/day for women of reproductive age with upward adjustments to 450 mg choline/day during pregnancy and 550 mg choline/day during lactation [3]. Although widely distributed in the diet, choline is absent from most prenatal vitamins currently on the market, and less than ten percent of pregnant women achieve target intake levels [4]. 2. Food Sources of Choline Choline is found in both animal and plant source foods; however, animal source foods typically contain more choline per gram of food product. Beef, eggs, chicken, fish, and pork are concentrated sources of choline providing more than 60 mg per 100 g [5]. Among plant source foods, nuts, legumes, and cruciferous vegetables (e.g., broccoli) are relatively good sources providing at least 25 mg per 100 g [5]. Although not a concentrated source, cow’s milk is a main contributor to dietary choline intake in the U.S. [6]. Nutrients 2019, 11, 1823; doi:10.3390/nu11081823 www.mdpi.com/journal/nutrients Nutrients 2019, 11, x FOR PEER REVIEW 2 of 16 100 g [5]. Although not a concentrated source, cow’s milk is a main contributor to dietary choline Nutrientsintake in2019 the, 11 U.S., 1823 [6]. 2 of 15 Various forms of choline are found in food. The most prominent dietary form of choline is usuallyVarious phosphatidylcholine forms of choline are (PC) found with in food. smaller The most amounts prominent of dietaryfree choline, form of cholinephosphocholine, is usually phosphatidylcholinesphingomyelin, glycerophosphocho (PC) with smallerline, amountsand lysophosphatidylcholine of free choline, phosphocholine, (LPC) [5]. All sphingomyelin,of these choline glycerophosphocholine,forms are interchangeable and within lysophosphatidylcholine the body and contribute (LPC) to an [5 ].individual’s All of these “total” choline choline forms intake. are Although betaine is a choline derivative, it is not considered a dietary source of choline because there interchangeable within the body and contribute to an individual’s “total” choline intake. Although is no direct route for converting betaine to choline. However, dietary betaine may have a choline- betaine is a choline derivative, it is not considered a dietary source of choline because there is no direct sparing effect since it participates in the remethylation of homocysteine, thus reducing the need for route for converting betaine to choline. However, dietary betaine may have a choline-sparing effect endogenous choline oxidation to betaine [7] and lowering the dietary requirement for choline. Upon since it participates in the remethylation of homocysteine, thus reducing the need for endogenous absorption of choline, water-soluble biomolecules (free choline, phosphocholine and choline oxidation to betaine [7] and lowering the dietary requirement for choline. Upon absorption glycerophosphocholine) enter portal blood, while lipid-soluble forms (PC, LPC and sphingomyelin) of choline, water-soluble biomolecules (free choline, phosphocholine and glycerophosphocholine) are incorporated into chylomicrons [8]. enter portal blood, while lipid-soluble forms (PC, LPC and sphingomyelin) are incorporated into chylomicrons [8]. 3. Choline Function 3. CholineWithin Function the body, choline is critical for a number of functions with wide-ranging roles in metabolicWithin and the physiologic body, choline processes. is critical forThe a choline number de ofrivative, functions PC, with iswide-ranging a major constituent roles in metabolicof all cell andmembranes physiologic and processes.is required The for choline the biosynthesis derivative, PC, of islipoproteins, a major constituent including of allvery cell membraneslow-density andlipoproteins is required (VLDLs), for the which biosynthesis facilitate of lipoproteins,the hepatic expo includingrt of lipid very (Figure low-density 1). Inadequate lipoproteins choline (VLDLs), intake whichdisturbs facilitate the integrity the hepatic of cellular export ofmembranes lipid (Figure resulting1). Inadequate in ‘leaky choline membranes’ intake disturbs [9] and theimpairs integrity the ofmobilization cellular membranes of fat resultingfrom liver in ‘leakyresulting membranes’ in fatty [9 ] andliver impairs [10]. theAcetylcholine mobilization functions of fat from as liver a resultingneurotransmitter in fatty liverin both [10 the]. Acetylcholine central nervous functions system as (CNS) a neurotransmitter and the peripheral in both nervous the central system nervous (PNS). systemIn the CNS, (CNS) cholinergic and the peripheral projections nervous from the system basal (PNS). forebrain In the to CNS,the cerebral cholinergic cortex projections and hippocampus from the basalsupport forebrain the cognitive to thecerebral functions cortex of those and target hippocampus areas [11]. support In the the PNS, cognitive acetylch functionsoline activates of those skeletal target areasmuscle [11 and]. In is the a major PNS, acetylcholineneurotransmitter activates in the skeletal autonomic muscle nervous and is system a major [12]. neurotransmitter Sphingomyelin in is the a autonomicconstituent nervous of the myelin system sheath [12]. Sphingomyelin [13], which covers is a constituent the axons of of the nerve myelin cells sheath and facilitates [13], which efficient covers thetransmission axons of nerveof nerve cells signals. and facilitates Finally, betaine efficient is a transmission source of methyl of nerve groups signals. for S-adenosylmethionine Finally, betaine is a source(SAM)-dependent of methyl groups methyltransferases for S-adenosylmethionine and for folate (SAM)-dependent mediated one-carbon methyltransferases metabolism following and for folate the mediateddemethylation one-carbon of dimethylglycine metabolism following (produced the when demethylation betaine is used of dimethylglycine as a methyl donor) (produced within when the betainemitochondria is used of as hepatocytes a methyl donor) [8]. within the mitochondria of hepatocytes [8]. Figure 1.1. A simplifiedsimplified diagram of the metabolic fate of maternal dietary choline and its delivery to the developing fetus. fetus. In In the the liver liver,, choline choline can can be be used used to tomake make phosphatidylcholine phosphatidylcholine (PC) (PC) through through the thecytidine cytidine diphosphate diphosphate (CDP)-choline (CDP)-choline pathway pathway (CDP-PC), (CDP-PC), or it can or be it canoxidized be oxidized to betaine to and betaine serve and as servea source as aof source methyl of methylgroups groupsfor PC for synthesi PC synthesiss via the via de the novo de novo phos phosphatidylethanolaminephatidylethanolamine N- Nmethyltransferase-methyltransferase (PEMT) (PEMT) pathway pathway (PEMT-PC). (PEMT-PC). Bo Bothth pathways pathways are are upregulated upregulated during during the thirdthird trimester ofof pregnancy,pregnancy, but but PEMT-derived PEMT-derived PC PC is preferentiallyis preferentially partitioned partitioned to the to developingthe developing fetus. fetus. CM, chylomicron;CM, chylomicron; MET, MET, methionine; methioni PE,ne; phosphatidylethanolamine; PE, phosphatidylethanolamine SAM,; S-adenosylmethionine;SAM, S-adenosylmethionine; VLDL, veryVLDL, low-density very low-density lipoprotein. lipoprotein. Nutrients
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