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Usual Choline Intakes Are Associated with Egg and Protein Food Consumption in the United States

MDPI
Nutrients
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Choline is an essential nutrient with critical roles in several biological processes including neuronal development, cell signaling, nerve impulse transmission, and lipid transport and metabolism. The National Cancer Institute method was used to assess usual intakes of choline from foods according to data for participants enrolled in the National Health and Nutrition Examination Survey 2009–2014 datasets and pregnant women in the 2005–2014 datasets. Suboptimal intakes of choline are present across many gender and life-stage subpopulations, as well as pregnant women in the U.S. Only 8.03 ± 0.56% of adults and 8.51 ± 2.89% pregnant women meet the AI for choline. Children 2–3 years were the most likely to meet their gender and life-stage specific AI, followed by children 4–8 years. Adults 19+ years who consume eggs were more likely to meet their gender and life-stage AI as compared to non-consumers (57.3 ± 1.45% and 2.43 ± 0.28%). Consumers of eggs had almost double the usual intake of choline as compared to non-consumers (525 ± 5.17 mg/d and 294 ± 1.98; p < 0.0001). Protein food (meat, poultry and seafood) consumption also increased usual choline intakes compared to non-consumers (345 ± 2.21 mg/day and 235 ± 8.81; p < 0.0001) to a lesser degree, but did not result in substantial increases in the percent of individuals meeting the AI. No subpopulation exceeded the UL for choline. This research illustrates that it is extremely difficult to achieve the AI for choline without consuming eggs or taking a dietary supplement.
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nutrients
Article
Usual Choline Intakes Are Associated with Egg and
Protein Food Consumption in the United States
Taylor C. Wallace 1,2,* and Victor L. Fulgoni III 3
1Department of Nutrition and Food Studies, George Mason University, 10340 Democracy Lane, Suite 306,
Fairfax, VA 22030, USA
2Think Healthy Group, Inc., 127 U Street NW, Washington, DC 20001, USA
3Nutrition Impact, LLC, 9725 D Drive North, Battle Greek, MI 49014, USA; vic3rd@aol.com
*Correspondence: taylor.wallace@me.com; Tel.: +1-270-839-1776
Received: 3 July 2017; Accepted: 2 August 2017; Published: 5 August 2017
Abstract:
Choline is an essential nutrient with critical roles in several biological processes
including neuronal development, cell signaling, nerve impulse transmission, and lipid transport and
metabolism. The National Cancer Institute method was used to assess usual intakes of choline from
foods according to data for participants enrolled in the National Health and Nutrition Examination
Survey 2009–2014 datasets and pregnant women in the 2005–2014 datasets. Suboptimal intakes of
choline are present across many gender and life-stage subpopulations, as well as pregnant women
in the U.S. Only 8.03
±
0.56% of adults and 8.51
±
2.89% pregnant women meet the AI for choline.
Children 2–3 years were the most likely to meet their gender and life-stage specific AI, followed by
children 4–8 years. Adults 19+ years who consume eggs were more likely to meet their gender and
life-stage AI as compared to non-consumers (57.3
±
1.45% and 2.43
±
0.28%). Consumers of eggs
had almost double the usual intake of choline as compared to non-consumers (525
±
5.17 mg/d and
294
±
1.98; p< 0.0001). Protein food (meat, poultry and seafood) consumption also increased usual
choline intakes compared to non-consumers (345
±
2.21 mg/day and 235
±
8.81; p< 0.0001) to a
lesser degree, but did not result in substantial increases in the percent of individuals meeting the AI.
No subpopulation exceeded the UL for choline. This research illustrates that it is extremely difficult
to achieve the AI for choline without consuming eggs or taking a dietary supplement.
Keywords:
choline; NHANES; usual intake; adequate intake; tolerable upper intake level; dietary
reference intake
1. Introduction
Choline is an essential micronutrient with critical roles in several biological processes [
1
].
As a source of methyl groups, choline supports cellular methylation reactions, including genomic
methylation, which impacts gene expression, the cell membrane that signal the stability of DNA and
lipid transport and metabolism. It also serves as the substrate for the formation of acetylcholine,
a neurotransmitter and non-neuronal cell-signaling molecule that is important for memory, mood,
muscle control, and other brain and nervous system functions. The metabolic fate of choline is the
biosynthesis of phosphatidylcholine and sphingomyelin, which are major phospholipids within cell
membranes that are critical for structural integrity [
1
3
]. Humans can produce small amounts of
choline endogenously in the liver, primarily in the form of phosphatidylcholine; however, the amount
is not sufficient to meet human requirements for the micronutrient [
4
]. Therefore, humans must obtain
choline from the diet. The requirement for choline may be different among subpopulations and rises
when the diet is deficient in folate, since it becomes the primary methyl donor [
2
]. Choline is vital
for early brain development [
1
,
2
], which might be why estrogen in premenopausal women induces
the gene that catalyzes natural biosynthesis of choline [
4
]. Choline deficiency results in non-alcoholic
Nutrients 2017,9, 839; doi:10.3390/nu9080839 www.mdpi.com/journal/nutrients
Nutrients 2017,9, 839 2 of 10
fatty liver disease, because it is required to form the phosphatidylcholine present in very low-density
lipoprotein (VLDL) particles [
1
]. Deficiency can also lead to neural tube defects during pregnancy and
suboptimal brain development among the fetus and in infants [5].
The most common sources of choline in foods are fat-soluble phosphatidylcholine and
sphingomyelin as well as water-soluble phosphocholine, glycerolphosphocholine, and free choline [
2
].
Pancreatic and mucosal enzymes liberate free choline from about half of the fat-soluble forms and
some water-soluble forms [
6
]. Foods naturally containing choline include chicken liver (3 oz.; 247 mg),
salmon (3 oz.; 187 mg), eggs (1 large egg with yolk; 125 mg), shitake mushrooms (1/2 c.; 58 mg),
chicken broilers or fryers (3 oz.; 56 mg), beef grass-fed strip steak (3 oz.; 55 mg), wheat germ (1 oz.
toasted; 51 mg), milk (8 oz.; 38 mg), brussels sprouts (1/2 c.; 32 mg), and almonds (1 oz.; 15 mg). Eggs
represent the major source of choline in the US diet [
7
]. In 1998, the US National Academies of Medicine
(NAM) Food and Nutrition Board (FNB) established an adequate intake (AI) and a tolerable upper
intake level (UL) for choline. At the time, the FNB felt that the existing peer-reviewed literature was
insufficient to determine an estimated average requirement (EAR) or recommended dietary allowance
(RDA) for choline, so an AI was set based on the prevention of non-alcoholic fatty liver disease in two
studies of adult men [
1
]. The AI for infants reflects the observed mean intake from human breast milk.
The UL was derived from the lowest observed adverse effect level shown to cause hypotension in
adults (i.e., 3.50 g/day) [1]. Dietary reference intakes for choline are illustrated in Table 1.
Table 1. Dietary reference intakes for choline.
Life-Stage Group AI (mg/day) UL (mg/day)
Infant
0–6 Months 125 Not established
6–12 Months 150 Not established
Children
1–3 Years 200 1000
4–8 Years 250 1000
9–13 Years 375 2000
Males
14–18 Years 550 3000
19 Years 550 3500
Females
14–18 Years 400 3000
19 Years 425 3500
Pregnancy
All ages 450 Age-appropriate UL
Lactation
All ages 550 Age-appropriate UL
AI = adequate intake; UL = tolerable upper intake level.
When the AI for choline was established in 1998, it was not known whether there were
significant numbers of individuals who were choline deficient, and until recently, little data from food
composition databases have been available on the choline content of foods [
1
]. Our previous work
found large portions (approximately 90%) of the US population age
2 years to have suboptimal
intakes of choline [
8
]. Thus, this manuscript seeks to explore choline intakes among consumers vs.
non-consumers of eggs, protein foods (meat, poultry and seafood), and dietary supplements.
2. Materials and Methods
2.1. Study Population
The National Center for Health Statistics (NCHS) of the U.S. Centers for Disease Control and
Prevention administers and collects the National Health and Nutrition Examination Survey (NHANES),
a nationally representative, cross-sectional survey of noninstitutionalized, civilian U.S. residents [
9
]. The
NHANES survey protocol was approved by the Research Ethics Review Board of the NCHS. Written
Nutrients 2017,9, 839 3 of 10
informed consent was obtained for all survey participants. Data from NHANES 2009–2010, 2011–2012,
and 2013–2014 were combined for these analyses, except for pregnant women, which combined data
from NHANES 2005–2006, 2007–2008, 2009–2010, 2011–2012, and 2013–2014. The combined sample
included 24,774 participants and 593 pregnant women who had completed and provided 24-hour
dietary intake data. In addition to dietary intake data, participants were asked to provide other
information inclusive of, but not limited to, their gender, age, race, weight, household income level, and
vegetarian status. Subjects who were aged <2 years were excluded from these analyses.
2.2. Dietary Choline
NHANES participants were asked to complete two dietary recall interviews, with the first
collected in person by trained interviewers. Proxy respondents provided dietary information for
young children and proxy-assisted interviews were used for children aged 6–11 years. The second
dietary recall interview was completed by telephone 3–10 days after the health examination. The U.S.
Department of Agriculture’s (USDA) Automated Multiple-Pass Method was utilized for both dietary
recall interviews [
10
,
11
]. Questionnaires, data sets, and related documentation from each NHANES
analysis can be found on the NCHS NHANES website [
12
]. Various USDA food composition databases
were utilized to determine the micronutrient contribution of specific foods consumed by NHANES
participants. The USDA estimated the choline content of foods in recipes by linking the ingredients in
survey food recipes to food composition data provided by the USDA National Nutrient Database for
Standard Reference [13].
2.3. Supplemental Choline
Information on the use of dietary supplements (including vitamins, minerals, herbs, and so forth)
over the previous 30 days prior to the dietary recall interview was collected as part of the dietary
supplement questionnaire. Detailed information was obtained for each reported dietary supplement,
including the frequency of consumption (i.e., the number of days the product was taken in the past
30 days), duration of use (i.e., how many days, weeks, months, or years the product was taken), and
the amount normally taken per day on days it was taken over the 30-day period. The interviewer also
examined each dietary supplement container and recorded complete product information so that each
dietary supplement could be matched or entered into a database. The average daily intake of choline
obtained from dietary supplements was calculated by using the number of days use was reported, the
reported amount taken daily, and the serving size unit from the Supplement Facts Panel.
2.4. Definitions
Gender was defined as male or female. DRI age groups (2–3, 4–8, 9–13, 14–18, 19–30, 31–50, 51–70,
and
71 years) were used to compare estimates of choline intakes. Children and adults were defined
as those individuals who were aged between 2 and 18 years and
19 years, unless otherwise specified.
2.5. Comparison to DRI Values
The DRIs are a family of nutrient reference values, defined by the NAM Food and Nutrition Board,
intended to serve as a guide for good nutrition and to provide the basis for the development of nutrient
guidelines in both the United States and Canada. In 1998, the NAM updated and established an AI, and UL
for choline [
1
]. These intake recommendations are specific to the role of choline in preventing non-alcoholic
fatty liver disease. The values differ for individuals based on age and gender. Choline was reported as
usual intake, as well as the percentage of the population with usual intakes above the AI and UL.
2.6. Statistical Analysis
The National Cancer Institute (NCI) method as previously described [
14
] was used to determine
estimates of usual choline intakes from the diet. The covariates used in the NCI model were as
Nutrients 2017,9, 839 4 of 10
follows: (1) sequence of 24-hour recall, (2) day of the week the 24-hour recall was collected, and (3)
dietary supplement use. All statistical analyses were performed with SAS software (version 9.2; SAS
Institute Inc., Cary, NC, USA). SAS macros necessary to fit this model and to perform the estimation of
usual intake distributions as well as additional details and resources regarding the NCI method are
available on the NCI website [
15
]. Sample weights were used to account for differential response and
non-coverage and to adjust for planned over-lapping of some groups. Survey weights were also used
to generate a nationally representative sample. Mean dietary intakes of choline between users and
nonusers of eggs and/or protein foods (meat, poultry and seafood) and the portion that met the AI and
exceeded the UL were compared by computing a z statistic. Significance was set at pvalue of <0.01.
3. Results
This manuscript expands our previous work (8) with more current population data, as well as
data in pregnant women, toddlers, and consumers vs. non-consumers of choline-rich eggs and protein
foods (meat, poultry and seafood). Only 11.3
±
0.47% of the U.S. population
2 years met the AI for
choline. Among the general adult population age 19+ y in the U.S., only 8.03
±
0.56% meet the AI for
choline (Table 2). Adult males were more likely than adult females to meet their age and gender specific
AI (12.7
±
0.95% and 3.61
±
0.58%; p
0.0001). Adults 19+ y had a usual intake of 338
±
1.86 mg/d
(males: 405
±
3.30 mg/d; females: 273
±
2.13 mg/d). Usual intakes of choline increased with age
until age 51–70 years. Pregnant women had a usual intake of 319
±
9.89 mg/d and only 8.51
±
2.89%
of pregnant women 13–44 years met the AI for choline. Children 2–3 years were the most likely to
meet their gender and life-stage specific AI, followed by children 4–8 years. Older children 9 + years
and adults had a low prevalence of meeting the AI for choline. Teenagers 14–18 years were the most
likely subpopulation to not meet the AI for choline. Children age 2-18 years had a usual intake of
252 ±2.21 mg/d (males: 276 ±2.96; females: 228 ±2.51).
Egg consumption was associated with higher usual intakes of choline across all subpopulations
(p< 0.0001). Adults 19+ years who consume eggs were more likely to meet their gender and life-stage AI
as compared to non-consumers (57.3
±
1.45% and 2.43
±
0.28%) (Table 3). Adults that consumed eggs on
day one of NHANES obtained almost double the usual intake of choline as compared to non-consumers
(525
±
5.17 mg/d and 294
±
1.98; p
0.0001). The relationship between egg consumption Healthy Eating
Index 2010 (HEI-2010) scores was small and varied across subpopulations. Adults who consumed eggs
were more likely to have a slightly higher HEI-2010 score as compared to non-consumers (51.7
±
0.40
vs. 50.3
±
0.27; p= 0.0037), however these differences were not statistically significant among adults age
31–50 or 51–70 years (data not shown). We did not identify any significant differences in the percent
of egg consumers vs. non-consumers in regard to gender, ethnicity, weight status, smoking status, or
amount of physical activity that were consistent across age and life-stage subpopulations (data not
shown). The substitution of 2 eggs per day for red and/or processed meat resulted in a Healthy US-style
2000-kcal food pattern model that enables the AI for choline to be met (Table 4).
Protein food (meat, poultry and seafood) consumption was also associated with also significantly
associated with higher usual intakes of choline across all subpopulations. Usual choline intakes increased
in consumers vs. non-consumers (345
±
2.21 mg/d and 235
±
8.81; p
0.0001), but to a lesser degree as
compared to egg consumers vs. non-consumers (Table 5). A small but significant increase in the percent
of individuals who met the AI was noted in protein food consumers vs. non-consumers (8.62
±
0.64%
and 2.32
±
0.89%; p= 0.0000). The relationship between protein food consumption and Healthy Eating
Index 2010 (HEI-2010) scores was also small and varied across subpopulations. Adults who consumed
protein foods were more likely to have a slightly lower HEI-2010 score as compared to non-consumers
(59.2
±
1.24 vs. 50.6
±
0.26; p
0.0001), however these differences were not statistically significant
among adults age 71+ years, males 19–30, 51–70, and 71+ years, or females 31–50 or 71+ years (data
not shown). We did not identify any significant differences in the percent of protein food consumers
vs. non-consumers in regard to gender, ethnicity, weight status, smoking status, or amount of physical
activity that were consistent across age and life-stage subpopulations (data not shown).
Nutrients 2017,9, 839 5 of 10
Table 2.
Choline Intakes among individuals in the National Health and Nutrition Examination Survey
(NHANES) 2009-2014 Datasets by Gender and Age a.
Gender/Age NUsual
Intake a
Percentile
5a25 a50 a75 a95 a% > AI % > UL
All
2–3 years
1316
224 ±3.60 129 ±3.95 176 ±3.31 217 ±3.58 264 ±4.82 344 ±8.41 60.7 ±2.09 0.00 ±0.00
4–8 years
2774
243 ±2.45 141±4.02 192 ±2.79 235 ±2.53 285 ±3.49 369 ±6.79 41.5 ±1.50 0.00 ±0.00
9–13 years
2559
257 ±3.63 151 ±4.88 205 ±3.67 249 ±3.66 301 ±4.45 389 ±7.78 6.63 ±0.96 0.00 ±0.00
14–18 years
2354
269 ±4.96 159 ±5.86 214 ±5.08 262 ±4.95 315 ±5.47 405 ±8.08 1.12 ±0.29 0.00 ±0.00
19–30 years
3288
330 ±3.56 169 ±3.76 240 ±3.29 308 ±3.75 399 ±5.21 561 ±9.75 6.59 ±0.66 0.00 ±0.00
31–50 years
5267
350 ±2.97 184 ±3.53 257 ±3.05 327 ±3.05 422 ±4.58 591 ±9.53 9.69 ±0.77 0.00 ±0.00
51–70 years
4975
342 ±3.36 183 ±3.72 254 ±3.25 321 ±3.60 409 ±4.66 572 ±8.91 8.42 ±0.68 0.00 ±0.00
71+ years
2244
307 ±3.16 167 ±3.61 232 ±3.10 289 ±3.45 364 ±4.48 506 ±7.77 4.39 ±0.48 0.00 ±0.00
Male
2–3 years 658 246 ±4.63 150 ±4.11 199 ±3.93 240 ±4.48 287 ±6.04 364 ±9.39 74.3 ±2.24 0.00 ±0.00
4–8 years
1452
265 ±3.11 162 ±3.95 215 ±2.98 258 ±3.22 307 ±4.35 390 ±7.35 54.5 ±1.85 0.00 ±0.00
9–13 years
1279
283 ±4.38 175 ±4.94 230 ±4.21 275 ±4.33 328 ±5.41 415 ±8.45 11.2 ±1.43 0.00 ±0.00
14–18 years
1207
295 ±5.18 184 ±5.57 241 ±5.16 288 ±5.01 341 ±5.96 431 ±9.53 0.32 ±0.13 0.00 ±0.00
19–30 years
1702
392 ±5.39 216 ±4.92 305 ±4.45 380 ±5.16 466 ±7.02 613 ±12.18 10.5 ±1.13 0.00 ±0.00
31–50 years
2563
421 ±4.99 236 ±5.07 330 ±4.13 408 ±4.74 498 ±6.63 652 ±11.57 15.3 ±1.25 0.00 ±0.00
51–70 years
2455
408 ±5.15 227 ±5.33 319 ±4.70 396 ±4.98 483 ±6.58 633 ±11.07 13.0 ±1.11 0.00 ±0.00
71+ years
1099
363 ±4.80 197 ±5.87 280 ±4.86 351 ±4.97 432 ±5.93 571 ±9.55 6.59 ±0.74 0.00 ±0.00
Female
2–3 years 658 201 ±3.64 118 ±4.37 160 ±3.47 195 ±3.53 235 ±4.75 303 ±7.74 46.7 ±2.56 0.00 ±0.00
4–8 years
1322
218 ±2.72 130 ±4.28 174 ±3.50 211 ±2.84 255 ±3.43 329 ±6.99 27.4 ±1.67 0.00 ±0.00
9–13 years
1280
233 ±3.75 140 ±4.74 187 ±4.22 226 ±3.88 272 ±4.31 347 ±6.87 2.46 ±0.51 0.00 ±0.00
14–18 years
1147
244 ±4.80 147 ±5.79 197 ±4.94 237 ±4.74 283 ±5.27 361 ±7.93 1.90 ±0.49 0.00 ±0.00
19–30 years
1586
257 ±4.14 152 ±4.38 206 ±3.92 250 ±4.09 301 ±5.16 386 ±8.13 2.08 ±0.49 0.00 ±0.00
31–50 years
2704
279 ±3.32 168 ±4.27 224 ±3.51 271 ±3.33 325 ±4.23 415 ±7.39 4.06 ±0.68 0.00 ±0.00
51–70 years
2520
280 ±3.88 169 ±4.17 226 ±3.60 273 ±3.77 327 ±4.98 416 ±8.29 4.16 ±0.79 0.00 ±0.00
71+ years
1145
266 ±4.02 158 ±4.35 213 ±4.05 259 ±4.03 311 ±4.83 397 ±8.04 2.76 ±0.58 0.00 ±0.00
Pregnant b
13–44 years 593 319 ±9.89 187 ±13.33 254 ±10.63 309 ±9.75 373 ±13.22 490 ±27.85 8.51 ±2.89 0.00 ±0.00
AI = Adequate intake; UL = Tolerable upper intake level;
a
Data are presented as mg/day
±
standard error;
bPregnant women were enrolled in the NHANES 2005–2014 datasets.
Table 3. Choline intakes among consumers vs. non-consumers of eggs a,b,c.
Gender/Age Day dNon-Consumers Consumers p-Value e
NUsual Intake a% > AI NUsual Intake a% > AI
All
19–30 years 1 2653 286 ±3.54 1.75 ±0.33 635 534 ±9.27 58.1 ±2.78 <0.0001
2 2291 279 ±3.63 1.22 ±0.26 997 454 ±6.69 24.2 ±3.51 <0.0001
31–50 years 1 4160 305 ±2.85 3.18 ±0.40 1107 545 ±8.61 64.1 ±2.66 <0.0001
2 3504 301 ±3.08 2.49 ±0.36 1763 453 ±6.24 23.0 ±2.90 <0.0001
51–70 years 1 3762 297 ±3.39 2.54 ±0.37 1213 520 ±8.48 57.4 ±2.91 <0.0001
2 2069 290 ±3.96 1.86 ±0.36 1906 429 ±5.44 13.7 ±2.45 <0.0001
71+ years 1 1723 266 ±3.19 1.01 ±0.20 521 463 ±8.54 37.3 ±2.71 <0.0001
2 1410 265 ±3.43 0.79 ±0.20 834 375 ±6.19 3.19 ±1.50 <0.0001
Male
19–30 years 1 1347 339 ±5.47 3.08 ±0.61 355 610 ±15.9 65.3 ±3.87 <0.0001
2 1163 327 ±5.16 1.99 ±0.43 539 539 ±11.4 42.4 ±6.20 <0.0001
31–50 years 1 1988 366 ±4.98 5.53 ±0.74 575 637 ±14.0 72.1 ±3.36 <0.0001
2 1677 360 ±5.41 4.38 ±0.69 886 543 ±10.7 44.5 ±5.48 <0.0001
51–70 years 1 1812 354 ±5.43 4.40 ±0.62 643 599 ±13.7 62.0 ±4.29 <0.0001
2 1477 346 ±6.17 3.28 ±0.67 978 509 ±9.84 28.1 ±5.04 <0.0001
71+ years 1 801 312 ±4.66 1.64 ±0.31 298 522 ±10.3 38.0 ±3.44 <0.0001
2 668 309 ±4.46 1.64 ±0.31 431 447 ±8.00 7.44 ±3.36 <0.0001
Female
19–30 years 1 1306 225 ±3.77 0.36 ±0.14 280 427 ±11.4 48.5 ±5.44 <0.0001
2 1128 224 ±4.14 0.31 ±0.13 458 341 ±7.62 0.00 ±0.03 <0.0001
31–50 years 1 2172 246 ±2.85 0.85 ±0.26 532 438 ±8.63 54.1 ±4.18 <0.0001
2 1827 243 ±3.46 0.68 ±0.29 877 358 ±6.19 0.00 ±0.31 <0.0001
51–70 years 1 1950 246 ±3.03 0.83 ±0.27 570 435 ±8.66 52.6 ±4.16 <0.0001
2 1592 239 ±3.38 0.64 ±0.25 928 352 ±6.35 0.00 ±0.10 <0.0001
71+ years 1 922 234 ±4.01 0.56 ±0.19 223 403 ±8.04 37.0 ±3.79 <0.0001
2 742 234 ±4.62 0.53 ±0.23 403 316 ±7.63 0.00 ±0.00 <0.0001
AI = Adequate intake; UL = Tolerable upper intake level;
a
Data are presented as mg/d
±
standard error;
b
No
incidence of any population exceeding the UL for choline;
c
Non-consumers are those who did not report consuming
whole eggs (i.e., they could have consumed products containing eggs);
d
Day 1 denotes consumer on day one. Day 2
denotes consumer on either NHANES intake day;
e
Comparison of usual intake of non-consumers vs. consumers.
Nutrients 2017,9, 839 6 of 10
Table 4. Food pattern modeling incorporating eggs as a substitute for red and/or processed meat.
Nutrient
Healthy US-Style
2000 Kcal Pattern
(%DV)
Eggs
(1 oz eq.) 1 Egg/Day 2 Eggs/Day
Energy (kcal) 2003 78 2019 2048
Protein (g) 91 (18%) 16.30 90.5 89.7
Total CHO (g) 256 (51%) 10.60 256 256
Fiber (g) 31 (111%) 0.00 31.0 31.0
Total fat (g) 72 (32%) 15.30 73.9 77.2
Sat fat (g) 18.7 (8%) 11.63 19.2 20.1
MUFA (g) 26.2 (12%) 12.04 26.9 28.0
PUFA (g) 22.5 (10%) 10.71 22.8 23.4
Cholesterol (mg) 215 (72%) 187 310 477
Calcium (mg) 1274 (98%) 25.0 1287 1310
Iron (mg) 17 (94%) 0.60 17.1 17.2
Magnesium (mg) 352 (84%) 5.00 351 350
Phosphorus (mg) 1717 (137%) 86.0 1729 1750
Potassium (mg) 3348 (71%) 63.0 3331 3301
Sodium (mg) 1787 (78%) 62.0 1750 1685
Zinc (mg) 14 (127%) 0.50 13.6 12.9
Copper (mg) 1.4 (156%) 0.00 1.40 1.40
Manganese (mg) 4 (174%) 0.01 4.00 4.00
Selenium (mg) 110 (200%) 15.4 114 121
Vitamin A (RAE) 898 (100%) 74.5 934 997
Vitamin E (mg AT) 10.2 (68%) 0.52 10.5 10.9
Vitamin D (IU) 274 (69%) 43.5 296 336
Vitamin C (mg) 117 (130%) 0.00 117 117
Thiamin (mg) 1.7 (142%) 0.03 1.70 1.70
Riboflavin (mg) 2.1 (162%) 0.26 2.20 2.40
Niacin (mg) 24 (150%) 0.03 23.1 21.4
Vitamin B6 (mg) 2.3 (135%) 0.06 2.30 2.20
Vitamin B12 (mcg) 6.8 (283%) 0.56 6.80 6.70
Choline (mg) 349 (63%) 147 418 539
Vitamin K (mcg) 139 (116%) 0.00 139 139
Table 5.
Choline intakes among consumers vs. non-consumers of protein foods (meat, poultry
and seafood).
Gender/Age Day cNon-Consumers bConsumers b
P-value d
N Usual Intake a% > AI N Usual Intake a% > AI
All
19–30 years 1 196 232 ±19.0 2.35 ±1.53 3092 336 ±3.89 6.76 ±0.81 <0.0001
2 84 227 ±23.7 3.15 ±2.13 3204 332 ±3.64 6.27 ±0.72 <0.0001
31–50 years 1 332 230 ±12.4 1.76 ±0.92 4935 359 ±3.36 10.6 ±0.89 <0.0001
2 149 251 ±20.0 5.08 ±2.12 5118 353 ±3.01 9.66 ±0.75 <0.0001
51–70 years 1 317 248 ±11.4 2.92 ±1.12 4658 349 ±3.04 8.79 ±0.71 <0.0001
2 118 235 ±20.5 3.67 ±1.71 4857 344 ±3.12 8.31 ±0.64 <0.0001
71+ years 1 174 221 ±10.2 1.58 ±0.75 2070 314 ±3.53 4.58 ±0.58 <0.0001
2 64 247 ±23.9 5.74 ±2.62 2180 309 ±3.37 4.13 ±0.49 <0.0001
Male
19–30 years 1 88 285 ±34.9 4.69 ±3.42 1614 398 ±6.42 10.5 ±1.33 <0.0001
2 39 255 ±39.3 5.86 ±3.67 1663 394 ±5.63 10.1 ±1.19 <0.0001
31–50 years 1 135 284 ±21.1 4.49 ±2.24 2428 429 ±5.42 16.1 ±1.42 <0.0001
2 67 289 ±27.0 8.77 ±3.37 2496 425 ±5.26 15.4 ±1.33 <0.0001
51–70 years 1 136 319 ±28.0 7.92 ±3.24 2319 413 ±4.99 13.1 ±1.23 <0.0001
2 52 270 ±48.8 6.86 ±4.03 2403 410 ±4.62 12.6 ±1.14 <0.0001
71+ years 1 62 284 ±23.2 4.46 ±2.34 1037 367 ±5.10 6.33 ±0.87 <0.0001
2 28 347 ±52.1 14.1 ±6.99 1071 363 ±4.97 5.96 ±0.81 0.0004
Female
19–30 years 1 108 180 ±12.6 0.07 ±0.21 1478 264 ±4.48 2.58 ±0.58 <0.0001
2 45 202 ±24.7 0.95 ±1.66 1541 258 ±4.16 1.99 ±0.49 <0.0001
Nutrients 2017,9, 839 7 of 10
Table 5. Cont.
Gender/Age Day cNon-Consumers bConsumers b
P-value d
N Usual Intake a% > AI N Usual Intake a% > AI
31–50 years 1 197 198 ±11.4 0.31 ±0.38 2507 287 ±3.52 4.84 ±0.82 <0.0001
2 82 215 ±20.8 1.90 ±1.58 2622 281 ±3.32 3.99 ±0.65 <0.0001
51–70 years 1 181 209 ±12.6 0.36 ±0.65 2339 287 ±3.65 4.98 ±0.80 <0.0001
2 66 214 ±15.6 1.92 ±1.36 2454 282 ±3.82 4.25 ±0.75 <0.0001
71+ years 1 112 193 ±9.15 0.23 ±0.27 1033 272 ±3.74 3.23 ±0.63 <0.0001
2 36 190 ±16.4 0.73 ±0.70 1109 267 ±3.77 2.66 ±0.52 <0.0001
AI = Adequate intake; UL = Tolerable upper intake level;
a
Data are presented as mg/d
±
standard error;
b
No
incidence of any population exceeding the UL for choline;
c
Day 1 denotes consumer on day one. Day 2 denotes
consumer on either NHANES intake day; dComparison of usual intake of non-consumed.
Usual choline intakes from dietary supplements are consistent with the amounts reported in our
previous work on multivitamins [
8
]. Multivitamins and other dietary multi-nutrient supplements
contain only minimal amounts of choline, since choline salts are bulky and vastly increase the
size of supplement product. Only minuscule portions of the U.S. population, including pregnant
women, consume choline as a single-nutrient supplement, making it impossible to assess their impact
on usual choline intakes from a population level. Dietary supplements provided approximately
13.83
±
0.97 mg/day of choline to the diets of children 2–18 years and 25.2
±
2.72 mg/day to that of
adults 19+ years. Consistent use of dietary supplements did slightly but significantly increase usual
choline intakes across all subpopulations (p< 0.0001) (Table 6).
Table 6. Contribution of dietary supplements by frequency to total usual choline intakes.
Gender/Age Consumers b1–10 d/mo b11–20 d/mo b21–30 d/mo b
NUsual Intake aNUsual Intake aNUsual Intake aNUsual Intake
All
2–3 years 268 12.6 ±1.22 34 4.00 ±1.23 75 8.97 ±1.45 159 16.4 ±1.73
4–8 years 555 13.9 ±1.39 82 3.45 ±0.80 134 12.7 ±1.79 339 16.7 ±1.73
9–13 years 333 15.1 ±1.46 69 2.81 ±0.84 68 10.9 ±1.40 196 20.4 ±1.89
14–18 years 130 12.2 ±2.03 22 1.38 ±0.63 36 12.1 ±2.78 72 16.3 ±3.16
19–30 years 169 21.2 ±4.67 42 4.07 ±0.63 35 8.31 ±2.45 92 31.3 ±8.32
31–50 years 310 14.1 ±2.01 67 4.54 ±1.17 77 10.3 ±1.88 166 19.0 ±3.54
51–70 years 200 39.3 ±6.10 22 2.53 ±0.57 22 6.96 ±2.03 156 47.4 ±7.55
71+ years 76 42.2 ±12.33 7 1.94 ±1.04 5 45.3 ±25.46 64 47.5 ±14.66
Male
2–3 years 139 12.1 ±1.52 22 4.25 ±1.86 43 8.74 ±1.45 74 17.6 ±2.78
4–8 years 296 14.1 ±1.70 43 3.78 ±0.96 66 13.1 ±2.02 187 16.6 ±2.20
9–13 years 171 14.3 ±2.08 35 3.35 ±1.47 36 6.92 ±2.24 100 20.3 ±2.56
14–18 years 70 12.5 ±2.83 11 1.46 ±0.80 21 13.2 ±4.23 38 15.2 ±4.05
19–30 years 87 29.1 ±8.73 21 4.25 ±1.00 16 9.62 ±4.24 50 42.3 ±14.1
31–50 years 131 14.0 ±2.31 33 4.41 ±1.17 26 12.6 ±4.05 72 18.9 ±4.51
51–70 years 73 44.0 ±8.80 7 1.84 ±0.35 13 8.33 ±2.89 53 57.9 ±13.2
71+ years 35 47.0 ±15.19 4 1.37 ±0.86 1 100 ±0.00 30 54.1 ±19.4
Female
2–3 years 129 13.0 ±1.71 12 3.56 ±0.81 32 9.34 ±2.55 85 15.7 ±2.32
4–8 years 259 13.7 ±1.95 39 2.94 ±1.03 68 12.2 ±2.41 152 16.9 ±2.50
9–13 years 162 16.1 ±1.59 34 2.19 ±0.69 32 14.9 ±1.83 96 20.5 ±2.25
14–18 years 60 11.8 ±2.98 11 1.30 ±0.89 15 10.8 ±3.34 34 18.5 ±4.46
19–30 years 82 12.9 ±2.59 21 3.83 ±0.63 19 7.62 ±3.06 42 18.3 ±4.51
31–50 years 179 14.2 ±2.61 34 4.74 ±2.42 51 8.87 ±2.00 94 19.1 ±4.27
51–70 years 127 36.8 ±7.66 15 3.11 ±1.03 9 5.48 ±2.56 103 42.5 ±8.59
71+ years 41 38.6 ±14.25 3 2.97 ±2.15 4 8.48 ±4.65 34 43.0 ±16.2
Pregnant
13–44 years 30 14.4 ±3.18 1 9.17 ±0.00 6 7.44 ±8.15 23 15.4 ±3.62
aData are presented as mg/d ±standard error; bNo incidence of any population exceeding the UL for choline.
We did not identify any population where intakes of choline exceeded (or came close to exceeding)
the UL, even when supplements were included. At the 95th percentile males 31–50 years had the
Nutrients 2017,9, 839 8 of 10
highest usual intakes of choline (652
±
11.6 mg/day) which is well under the 3500 mg/day UL for
this subpopulation.
4. Discussion
There is a clear need to increase awareness among health professionals, policy makers, and
consumers regarding the large portion of individuals and subpopulations who do not currently achieve
the AI for choline in the United States. It is necessary for the National Academy of Medicine, Food and
Nutrition Board to update Dietary Reference Intakes (DRIs) for choline so that we may more accurately
assess the magnitude of concern about potential population inadequacies for any nutrient with an
assigned AI. Lack of an Estimated Average Requirement (EAR) severely limits the interpretation of the
population intake data because it is difficult to assess whether intake below the AI results in suboptimal
health status (e.g., impaired liver function, cognition, etc.). Furthermore, the USDA food composition
databases are somewhat limited in their estimations of the choline content of foods. The databases
do not currently accurately account for many branded food products. Despite these limitations, our
data and that previously published online by our group [
8
], the USDA [
16
], and other international
populations in Europe [
17
], Taiwan [
18
], New Zealand [
19
], and Canada [
20
] consistently illustrate
that intakes of choline fall well below the AI for many subpopulations (particularly pregnant and/or
lactating women), and that may pose a significant public health concern. We did not identify any
significant differences in the percent of protein food consumers vs. non-consumers in regard to gender,
ethnicity, weight status, smoking status, or amount of physical activity.
The 2015–2020 Dietary Guidelines for Americans Advisory Committee (DGAC) determined that
of the nutrients with an AI (vitamin K, choline, dietary fiber, and potassium), that a low proportion of
the population had fiber and potassium intakes above the AI, and therefore considered them to be
under-consumed [
21
]. These data strongly suggest that choline is also under-consumed by the U.S.
population, to a similar extent. The 2015–2020 DGAC also found that adequacy goals were not met in
almost all food patterns for potassium, vitamin D, vitamin E and choline [
17
]. This is surprising given
that the recent DGAC eliminated the long-standing recommendations around total cholesterol, which
enables eggs to be included in food pattern models to a greater extent. Our food pattern models show
that substituting red and/or processed meat with two eggs per day enables consumers to meet the AI
for choline without compromising other nutrient intakes. When young healthy adults consumed 1, 2,
or 3 eggs/day for 4-week serum trimethylamine-N-oxide (TMAO), a byproduct of choline which has
been thought to increase the risk of heart disease, levels did not increase [
22
]. Egg consumption in
this study did increase HDL-cholesterol but not LDL-cholesterol [
22
], thus reaffirming their utility to
safely increase choline intakes. It is important to note that most choline in eggs is bound and not in
free form, which changes how the nutrient is absorbed and digested. Miller et al., found that only 14%
of choline from eggs is converted to TMAO, which is efficiently excreted and does not accumulate in
the bloodstream [23].
Dietary supplements contributed minimal amounts of choline to the diet, since only small portions
of the population consume choline-containing supplements. The House of Delegates of the American
Medical Association (AMA) adopted Resolution 517 on June 13, 2017 in support evidence-based
amounts of choline in all prenatal supplements for the purpose of ensuring that the baby’s 4brain
and spinal cord develop properly [
24
]. Several forms of choline are available on the market, the most
popular being choline chloride and choline bitartrate.
Educating individuals on foods that are rich in choline may assist in the public health effort.
Particular public health emphasis should be given to pregnant and/or lactating women, since a
large majority do not meet the AI and since choline is vital to the development of the fetus. Serum
concentrations of choline in women are much less than that of breast milk [
25
]. Recommending
supplementation and/or higher egg consumption (or a mixture of both for those concerned with
dietary cholesterol intakes) in this subpopulation (and others) may be appropriate given that most
adult women have lower than usual intakes of choline. Fortification of staple commodities and
Nutrients 2017,9, 839 9 of 10
products may serve as an additional strategy to increase choline intakes across the population. These
recommended strategies are not likely to increase choline intakes anywhere near the UL.
5. Conclusions
Many gender and life-stage subpopulations, as well as pregnant women in the U.S. do not
currently meet the AI for choline. Only 8.03
±
0.56% of adults and 8.51
±
2.89 pregnant women meet
the AI for choline. Children 2–3 years were the most likely to meet their gender and life-stage specific
AI, followed by children 4–8 years. Adults 19+ years who consume eggs were more likely to meet their
gender and life-stage AI as compared to non-consumers. Protein food (meat, poultry and seafood)
consumption also increased usual choline intakes compared to non-consumers to a lesser degree, but
did not result in substantial increases in the percent of individuals meeting the AI. No subpopulation
exceeded the UL for choline. This research illustrates that it is extremely difficult to achieve the AI for
choline without consuming eggs or taking a dietary supplement. Educating individuals on foods that
are rich in choline, the fortification of staple food items, and/or encouragement of supplementation in
certain subpopulations such as pregnant and/or lactating women may assist in public health efforts.
Revision of the DRIs for choline to reflect the current peer-reviewed literature is critical.
Author Contributions:
V.L.F. III and T.C.W. conceived and designed and analyzed the data and wrote the paper.
Conflicts of Interest:
T.C.W. has accepted academic consulting and writing fees from Balchem Corp. T.C.W. is
currently an academic consultant for the Egg Nutrition Center. T.C.W. has obtained competitive research grants
within the past year from the National Cattleman’s Beef Association. V.L.F as Vice President of Nutrition Impact,
LLC conducts analyses of NHANES for numerous members of the food and beverage industry.
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2017 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/).
... Eight studies have reported choline intake in adults [17,18,24,27,28,54,66], one study measured choline intake in children [31], and four studies have recorded choline intake in pregnant women [13,[33][34][35]. Among the twenty-one studies measuring choline intake in non-European countries, the majority (52%) were conducted in the USA [19,20,25,32,[55][56][57][62][63][64][65], while the others were carried out in Palestine [58], South Africa [59], Australia [36,60], Mexico [23], Taiwan [16], Iran [22,29], Canada [21,61]. ...
... Thirteen studies identified the main sources of choline as being mainly products of animal origin, such as eggs, meat, dairy, dairy derivatives, and fish, as well as grain and bakery products [12,13,17,18,20,23,25,27,28,31,34,35,60,66], although not every study provided detailed data (Table 1). ...
... Contrary to those results, a study conducted in Poland did not show differences in choline intake between normal weight and overweight/obese people. The study conducted by Wallace et al. [20] in the United States showed that eggs and protein food (meat, seafood) are the major sources of choline in the diet. Interestingly, adults who consume eggs were more likely to meet the AI requirements than nonconsumers of eggs (57.3% ± 1.45% vs. 2.43% ± 0.28% respectively). ...
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Full-text available
Background Choline is a nutrient necessary for the proper functioning of the body with a multidimensional impact on human health. However, comprehensive studies evaluating the dietary intake of choline are limited. The aim of this narrative review is to analyze current trends in choline intake in European and non-European populations. The secondary aim was to discuss possible future choline trends. Methods The search strategy involved a systematic approach to identifying relevant literature that met specific inclusion criteria. Observational studies and randomized clinical trials were searched for in PubMed and Scopus databases from January 2016 to April 2024. This review includes the characteristics of study groups, sample sizes, methods used to assess choline intake and time period, databases used to determine intake, choline intakes, and the main sources of choline in the diet. The review considered all population groups for which information on choline intake was collected. Results In most studies performed in Europe after 2015 choline intake did not exceed 80% of the AI standard value. The mean choline intake for adults in different European countries were 310 mg/day, while the highest value was reported for Polish men at 519 mg/day. In non-European countries, mean choline intakes were 293 mg/day and above. The main reported sources of choline in the diet are products of animal origin, mainly eggs and meat. The available data describing the potential intake of these products in the EU in the future predict an increase in egg intake by another 8% compared to 2008–2019 and a decrease in meat intake by about 2 kg per capita from 2018 to 2030. Conclusions In the last decade, choline intake among adults has been insufficient, both in Europe and outside it. In each population group, including pregnant women, choline intake has been lower than recommended. Future choline intake may depend on trends in meat and egg consumption, but also on the rapidly growing market of plant-based products. However, the possible changes in the intake of the main sources of choline may lead to either no change or a slight increase in overall choline intake.
... During periods of rapid growth and development such as the first two years of life, demand for choline is particularly high,~125-200 mg/day [5,6] [7,8]. However, in the United States National Health and Nutrition Examination Survey 2009-2014 [9], toddlers 2-3 years were more likely than all other age groups to be above the AI. ...
... Although no published studies have evaluated choline intakes in infants, our toddler intake data are comparable with those reported in Canada and Europe [7,8] and are slightly lower than those of the United States (US) [9]. In a randomized controlled trial with Canadian toddlers aged 1-2 years supplemented with long-chain polyunsaturated fatty acids (n = 110), Weideman et al. reported mean choline intakes of 174 ± 56 and 205 ± 67.5 mg/day at one year and two years of age, respectively [8]. ...
... In contrast, Wallace et al. reported a higher mean intake (217 ± 3.58) and percentage of toddlers 2-3 years above the AI (61%) in the US NHANES 2009-2014 [9]. This difference may be attributable to the age of the children at the time of the survey and differences in food consumption patterns, particularly meat and dairy foods. ...
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(1) Background: Despite the important role choline plays in child development, there are no data on dietary choline intake in early childhood in Australia. (2) Aim: In this cross-sectional study, we estimated the usual total choline intake and the proportion exceeding the Adequate Intake (AI) and determined the main dietary sources of choline in infants 6–12 months (n = 286) and toddlers 12–24 months (n = 475) of age. (3) Methods: A single 24-h food record with repeats collected during the 2021 Australian Feeding Infants and Toddlers Study (OzFITS 2021) was used to estimate dietary choline intake. (4) Results: The mean choline intake was 142 ± 1.9 mg/day in infants and 181 ± 1.2 mg/day in toddlers. Only 35% of infants and 23% of toddlers exceeded the AI for choline based on Nutrient Reference Values (NRVs) for Australia and New Zealand. Breastmilk was the leading source of choline, contributing 42% and 14% of total choline intake in infants and toddlers, respectively; however, egg consumers had the highest adjusted choline intakes and probability of exceeding the AI. (5) Conclusions: Findings suggest that choline intake may be suboptimal in Australian infants and toddlers. Further research to examine the impact of low choline intake on child development is warranted.
... Nineteen studies reported the prevalence of adequate choline intake during pregnancy (Table 3). [13][14][15]25,[36][37][38][39][40][41][42][43][44][45][46][47][48][49][50] The distributions of mean (95%CI) and prevalence (95%CI) of pregnant women with adequate choline intake across countries and regions are reported in Figures S1, 13-15,25,36-50 S2, 15,36,37,39-50 and S3 13,36,38 in the Supporting Information online. Most studies were conducted in the Americas, with 5 in the United States, 15,[39][40][41][42] 3 in Canada, [43][44][45] 1 in Brazil, 46 and 1 in Jamaica. ...
... [13][14][15]25,[36][37][38][39][40][41][42][43][44][45][46][47][48][49][50] The distributions of mean (95%CI) and prevalence (95%CI) of pregnant women with adequate choline intake across countries and regions are reported in Figures S1, 13-15,25,36-50 S2, 15,36,37,39-50 and S3 13,36,38 in the Supporting Information online. Most studies were conducted in the Americas, with 5 in the United States, 15,[39][40][41][42] 3 in Canada, [43][44][45] 1 in Brazil, 46 and 1 in Jamaica. 47 There were 3 conducted in Europe, 13,36,37 3 in Asia, 14,25,48 2 in South Africa, 49,50 and 1 in Australia. ...
... In North America, the prevalence of pregnant women meeting adequate choline intake was low: 23% in Canada 43 and 16.5% in the United States. 42 High-risk populations in Africa had even lower rates, with some at 0%. 40 Pregnant women in the United States had a gradually increasing sufficient choline intake status over time, increasing from 4.7% in 2014 39 to 8.5% in 2017, 41 and further to 16.5% in 2019. 42 In the contrast, the prevalence in Canada exhibited a downward trend, decreasing from 23% in 2014 43 to 18% in 2019 45 ( Table 3). ...
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Context Choline is a critical nutrient. Inadequate choline intake during pregnancy increases the risk of adverse maternal and offspring health. Objective A systematic review and meta-analysis were conducted to examine the current recommendations for choline intake by pregnant women, estimate the overall prevalence of pregnant women with adequate choline intake, and explore associations between maternal choline level and adverse pregnancy outcomes (APOs). Methods Choline recommendations for pregnant women were assessed from eight nutrient guidelines of the United States, United Kingdom, Canada, Australia, Asia, International Federation of Gynecology and Obstetrics, and World Health Organization. Data on the prevalence of pregnant women with adequate choline intake and the association between maternal choline level and APOs were collected from 5 databases up to May 2023. Meta-analyses with random effects and subgroup analyses were performed for the pooled estimate of prevalence and association. Results Five recent nutrition guidelines from the United States (United States Department of Agriculture), United States (Food and Drug Administration), Canada, Australia, and the International Federation of Gynecology and Obstetrics have emphasized the importance of adequate choline intake for pregnant women. Of 27 publications, 19 articles explored the prevalence and 8 articles explored the association. Meta-analysis of 12 prevalence studies revealed a concerning 11.24% (95% confidence interval, 6.34–17.26) prevalence of pregnant women with adequate choline intake recommendations. A meta-analysis of 6 studies indicated a significant association between high maternal choline levels and a reduced risk of developing APOs, with an odds ratio of 0.51 (95% confidence interval, 0.40–0.65). Conclusion The existing guidelines highlight the importance of choline in supporting maternal health and fetal development during pregnancy. Furthermore, a high maternal choline level was likely to be associated with a lower risk of APOs. However, 88.76% of pregnant women do not achieve the optimal choline intake. Therefore, specific policies and actions may be necessary to improve choline intake in pregnant women’s care and support the well-being of pregnant women. Systematic Review Registration PROSPERO registration no. CDR42023410561.
... [10][11][12][13][14][15] In contrast, choline is absent or found in small or negligible concentrations in prenatal supplements with general under-consumption not achieving the Adequate Intake (AI) level for choline during pregnancy. [15][16][17][18] The impact of such intake patterns on offspring phenotypes has seldom been examined. ...
... 20,21,24 On the other hand, most people do not meet the AI level for choline. [15][16][17][18] Excessive folic acid and inadequate choline intake patterns have recently been raised as a concern in Canada. 34 In our present study, we sought to investigate the consequences from a maximal imbalance between folic acid and choline thus we retained the 10× supplemental level for folic acid with the removal of choline in the diet. ...
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Prenatal multivitamins, including folic acid, are commonly consumed in excess, whereas choline, an essential nutrient and an important source of labile methyl groups, is underconsumed. Here, we characterized profiles of one‐carbon metabolism and related pathways and patterns of DNA methylation in offspring exposed to excess or imbalanced micronutrients prenatally. Pregnant Wistar rats were fed either recommended 1× vitamins (RV), high 10× vitamins (HV), high 10× folic acid with recommended choline (HFolRC), or high 10× folic acid with no choline (HFolNC). Offspring were weaned to a high‐fat diet for 12 weeks. Circulating metabolites were analyzed with a focus on the hypothalamus, an area known to be under epigenetic regulation. HV, HFolRC, and HFolNC males had higher body weight (BW) and lower plasma choline and methionine consistent with lower hypothalamic S‐adenosylmethionine (SAM):S‐adenosylhomocysteine (SAH) and global DNA methylation compared with RV. HV and HFolNC females had higher BW and lower plasma 5‐methyltetrahydrofolate and methionine consistent with lower hypothalamic global DNA methylation compared with RV. Plasma dimethylglycine (DMG) and methionine were higher as with hypothalamic SAM:SAH and global DNA methylation in HFolRC females without changes in BW compared with RV. Plasma trimethylamine and trimethylamine‐N‐oxide were higher in males but lower in females from HFolRC compared with RV. Network modeling revealed a link between the folate‐dependent pathway and SAH, with most connections through DMG. Final BW was negatively correlated with choline, DMG, and global DNA methylation. In conclusion, prenatal intake of excess or imbalanced micronutrients induces distinct metabolic and epigenetic perturbations in offspring that reflect long‐term nutritional programming of health.
... Trace elements like selenium and iodine can be increased through dietary supplementation of hens. Selenium-enriched eggs, for example, provide up to 40 µg of selenium per egg, supporting antioxidant functions and reducing deficiency risks [51,52]. ...
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This study explores the nutritional benefits and health implications of omega-3- and omega-6-enriched eggs, positioning them within the context of functional foods aimed at improving public health outcomes. With rising consumer interest in nutritionally fortified foods, omega-enriched eggs have emerged as a viable source of essential fatty acids, offering potential benefits for cardiovascular health, inflammation reduction, and cognitive function. This research examines enrichment techniques, particularly dietary modifications for laying hens, such as the inclusion of flaxseed and algae, to enhance omega-3 content and balance the omega-6-to-omega-3 ratio in eggs. The findings indicate that enriched eggs provide significantly higher levels of essential fatty acids and bioactive compounds than conventional eggs, aligning with dietary needs in populations with limited access to traditional omega-3 sources like fish. This study further addresses consumer perception challenges, regulatory constraints, and environmental considerations related to sustainable production practices. The conclusions underscore the value of omega-enriched eggs as a functional food that aligns with health-conscious dietary trends and recommend ongoing research to refine enrichment methods and expand market accessibility.
... Since choline from shell eggs seems to be more bioavailable than from nutritional supplements (Lemos et al., 2018;Smolders et al., 2019;DiBella et al., 2020), the egg sector has recently increased its activities to raise the awareness within the health community and general population about choline and egg nutrition. While shell eggs are already one of the main dietary sources of choline in many countries, a greater consumption of eggs should further reduce the gap between adequate and mean intakes of choline and contribute further to human nutrition (Wallace & Fulgoni, 2017;Wallace et al., 2018;Wiedeman et al., 2018). ...
Chapter
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As one of the few foods produced and consumed with no geographical or religious restrictions, shell eggs have always played a key role in the human diet. The consistency in the composition of shell eggs along with their versatility have made them a food of choice for consumers of all ages. The high digestibility of egg proteins along with their content in indispensable amino acids are just one of the nutritional benefits of shell eggs. The eggs are also rich in a wide range of vitamins and minerals, choline, lutein and zeaxanthin, all playing an important role in human nutrition. With the dietary intake of cholesterol no longer seen as a health risk factor in the general population, shell eggs are now widely recommended by governments and health professionals as an essential component of a healthy diet. The ease of production of shell eggs enriched in various nutrients, also called functional eggs, further boost their potential to alleviate the growing incidence of nutrient deficiencies in human diets. There is however a need to further boost the production and consumption of shell eggs in various parts of the world, where they could contribute more to food security and human health.
... Lifelong deficiencies in brain function may occur if choline is not provided during the first 1000 days of life [45]. It has been demonstrated that low maternal choline intakes during pregnancy increase the incidence of neural tube abnormalities, a cleft palate and suboptimal brain development among the fetus and in infants [192,193]. ...
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Introduction: Nutrition is one of the critical factors that influence brain development, and has a significant impact on the brain’s developmental processes and functioning from foetal to adult age. Newborn human brains utilise 60% of the body’s total oxygen, which has an impact on calorie intake. For the anatomical and functional growth of the brain, all nutrients are essential, the ones that aid in energy, carbohydrate, protein, and fat metabolism are especially significant. Objectives: The aim of this review is to boost up memory through diet, to know about the Nutrients for the development of the brain and to ensure Foods that adversely affect normal brain function. Methodology: This literature review consulted multiple databases, focusing on brain health and development, cognitive function, and maternal diet. The review included research from previous decades and analysed around 1,000 articles, with nearly 185 selected. The review assessed the relevance of the content to search terms, evaluating resources based on material quality, topicality, and publication year. The review discussed macronutrients and micronutrients, healthy and unhealthy foods, and maternal diets for foetal brain development. Conclusion: Factors such as maternal diet and macro and micronutrient consumption significantly impact brain development and cognitive function. Nutrition is crucial for optimal brain health and preventing cognitive decline. Deficiencies and excesses of certain nutrients affect cognitive function differently. Vitamin A, LC-PUFAs, ketones, protein, zinc, neurotrophins, neuropeptides, choline deficiency, vitamin B, copper, lutein, and zeaxanthin are essential for brain health. Consuming foods like walnuts, dairy, fish, caffeine, and low glycemic index foods can be beneficial for brain health, while junk foods, refined sugar, and saturated fats can be harmful.
Article
Objective Dietary choline is associated with lower risk of dementia in older adults, yet this association during mid-life remains unknown. Given that menopause reflects a nutrition-sensitive time point where prevention strategies may mitigate cognitive deficits, we examined the relationship of choline, betaine, and egg intakes (ie, dietary exposures) with cognitive performance in the Study of Women's Health Across the Nation (SWAN) cohort ( N = 1,006). Methods SWAN is a longitudinal study of women across the menopause transition. Diet was assessed via modified Block food frequency questionnaire, and cognitive function was examined using the Symbol Digit Modalities Test, Digits Backward Test, and East Boston Memory Test (EBMT). Annualized rate of cognitive scores and quartiles of diet were computed using linear mixed models overall (all diet exposures) and by baseline menopausal status (choline, betaine only). Results Among all women, higher choline ( P -for-trend = 0.006) and betaine ( P -for-trend = 0.005) intakes, independently and combined (ie, choline + betaine; P -for-trend = 0.001), were significantly associated with reduced rate of change on the EBMT–Delayed Recall (DR), but egg intake did not consistently impact cognitive function. By menopausal status, higher betaine, but not choline, was associated with a lower annualized rate of change in cognitive performance on the EBMT-DR (mean difference [95% confidence interval]; Q1: referent vs Q4: −0.071 [−0.17, 0.03]; P -for-trend = 0.006) for early perimenopausal women; nevertheless, choline and betaine were not associated with cognitive function among premenopausal women. Conclusions Higher dietary betaine intake among early perimenopausal women and higher dietary intakes of betaine and choline, independently and combined, among all women, were minimally associated with the trajectory of verbal episodic memory, yet no associations between diet and cognition were observed among premenopausal women. Future research should address the relationship between dietary intake and cognition during menopause in other research settings and cohorts.
Article
Objectives: To synthesize evidence from animal models of neurodevelopmental disorders (NDD) using maternal choline supplementation, to characterize current knowledge on the mechanisms of choline's protective effects against NDD, and to identify gaps in knowledge for future study. Methods: A literature review was conducted in PubMed to identify studies using prenatal choline supplementation interventions in rodent models of neurodevelopmental disorders. 24 studies were identified, and behavioral and biological findings were extracted from each. Studies examining both genetic and environmental risk factors were included. Results: Maternal choline supplementation during gestation is protective against both genetic and environmental NDD risk factors. Maternal choline supplementation improves both cognitive and affective outcomes throughout the lifespan in NDD models. Prenatal choline improved these outcomes through its participation in processes like neurogenesis, epigenetic regulation, and anti-inflammatory signaling. Discussion: Maternal choline supplementation improves behavioral and neurobiological outcomes in animal models of NDD, paralleling findings in humans. Animal models provide a unique opportunity to study the mechanisms by which gestational choline improves neurodevelopmental outcomes. This is especially important since nearly 90% of pregnant people in the United States are deficient in choline intake. However, much is still unknown about the mechanisms through which choline and its derivatives act. Further research into this topic, especially mechanistic studies in animal models, is critical to modernize maternal choline intake guidelines and to develop interventions to increase maternal choline intake in vulnerable populations.
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Eggs are a source of cholesterol and choline and may impact plasma lipids and trimethylamine-N-oxide (TMAO) concentrations, which are biomarkers for cardiovascular disease (CVD) risk. Therefore, the effects of increasing egg intake (0, 1, 2, and 3 eggs/day) on these and other CVD risk biomarkers were evaluated in a young, healthy population. Thirty-eight subjects [19 men/19 women, 24.1 ± 2.2 years, body mass index (BMI) 24.3 ± 2.5 kg/m²] participated in this 14-week crossover intervention. Participants underwent a 2-week washout with no egg consumption, followed by intake of 1, 2, and 3 eggs/day for 4 weeks each. Anthropometric data, blood pressure (BP), dietary records, and plasma biomarkers (lipids, glucose, choline, and TMAO) were measured during each intervention phase. BMI, waist circumference, systolic BP, plasma glucose, and plasma triacylglycerol did not change throughout the intervention. Diastolic BP decreased with egg intake (P < 0.05). Compared to 0 eggs/day, intake of 1 egg/day increased HDL cholesterol (HDL-c) (P < 0.05), and decreased LDL cholesterol (LDL-c) (P < 0.05) and the LDL-c/HDL-c ratio (P < 0.01). With intake of 2–3 eggs/day, these changes were maintained. Plasma choline increased dose-dependently with egg intake (P < 0.0001) while fasting plasma TMAO was unchanged. These results indicate that in a healthy population, consuming up to 3 eggs/day results in an overall beneficial effect on biomarkers associated with CVD risk, as documented by increased HDL-c, a reduced LDL-c/HDL-c ratio, and increased plasma choline in combination with no change in plasma LDL-c or TMAO concentrations.
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Choline is an essential nutrient important for normal function of all cells and for brain development and function (1,2). Choline availability during pregnancy is important for optimal fetal development (3). In the past, little data were available on the choline content of foods from which dietary intake levels could be calculated. Beginning with the 2005-2006 What We Eat in America, NHANES, choline intakes were estimated. Nationally representative data from What We Eat In America, NHANES 2007-2008 on dietary intakes from foods and beverages and food sources of choline are presented in this report. These estimates exclude choline intake from dietary supplements.
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Background: It is important to understand whether eating eggs, which are a major source of dietary choline, results in increased exposure to trimethylamine-N-oxide (TMAO), which is purported to be a risk factor for developing heart disease. Objective: We determined whether humans eating eggs generate TMAO and, if so, whether there is an associated increase in a marker for inflammation [ie, high-sensitivity C-reactive protein (hsCRP)] or increased oxidation of low-density lipoprotein (LDL). Design: In a longitudinal, double-blind, randomized dietary intervention, 6 volunteers were fed breakfast doses of 0, 1, 2, 4, or 6 egg yolks. Diets were otherwise controlled on the day before and day of each egg dose with a standardized low-choline menu. Plasma TMAO at timed intervals (immediately before and 1, 2, 4, 8, and 24 h after each dose), 24-h urine TMAO, predose and 24-h postdose serum hsCRP, and plasma oxidized LDL were measured. Volunteers received all 5 doses with each dose separated by >2-wk washout periods. Results: The consumption of eggs was associated with increased plasma and urine TMAO concentrations (P < 0.01), with ∼14% of the total choline in eggs having been converted to TMAO. There was considerable variation between individuals in the TMAO response. There was no difference in hsCRP or oxidized LDL concentrations after egg doses. Conclusions: The consumption of ≥2 eggs results in an increased formation of TMAO. Choline is an essential nutrient that is required for normal human liver and muscle functions and important for normal fetal development. Additional study is needed to both confirm the association between TMAO and atherosclerosis and identify factors, microbiota and genetic, that influence the generation of TMAO before policy and medical recommendations are made that suggest reduced dietary choline intake.
Book
Present Knowledge in Nutrition, 10th Edition provides comprehensive coverage of all aspects of human nutrition, including micronutrients, systems biology, immunity, public health, international nutrition, and diet and disease prevention. This definitive reference captures the current state of this vital and dynamic science from an international perspective, featuring nearly 140 expert authors from 14 countries around the world. Now condensed to a single volume, this 10th edition contains new chapters on topics such as epigenetics, metabolomics, and sports nutrition.The remaining chapters have been thoroughly updated to reflect recent developments. Suggested reading lists are now provided for readers wishing to delve further into specific subject areas. An accompanying website provides book owners with access to an image bank of tables and figures as well as any updates the authors may post to their chapters between editions. Now available in both print and electronic formats, the 10th edition will serve as a valuable reference for researchers, health professionals, and policy experts as well as educators and advanced nutrition students.
Article
Objective: Choline is an essential nutrient and plays a critical role in brain development, cell signaling, nerve impulse transmission, and lipid transport and metabolism. This analysis aimed to assess usual intakes of choline and compare them with the dietary reference intakes for U.S. residents aged ≥2 years. Methods: The National Cancer Institute method was used to assess usual intakes of choline from foods according to data for participants in the 2009-2012 National Health and Nutrition Examination Survey (NHANES; n = 16,809). Results: Suboptimal intakes of choline are prevalent across many life-stage subpopulations in the United States. Only 10.8 ± 0.6% of 2009-2012 NHANES participants aged ≥2 years (15.6 ± 0.8% of males and 6.1 ± 0.6% of females) achieved the adequate intake (AI) for choline. Children aged 2-3 years were the most likely to exceed the AI (62.9 ± 3.1%), followed by children aged 4-8 years (45.4 ± 1.6%) and children aged 9-13 years (9.0 ± 1.0%), compared to adolescents aged 14-18 years (1.8 ± 0.4%) and adults aged ≥19 years (6.6 ± 0.5%). When comparing by age and gender, males consumed significantly more choline than females for all age groups. Conclusions: These data indicate that there is a need to increase awareness among health professionals and consumers regarding potential suboptimal intakes of choline in the United States, as well as the critical role that choline plays in health maintenance throughout the lifespan. Food scientists and the food and dietary supplement industries should consider working collectively with government agencies to discuss strategies to help offset the percentage of the population that does not meet the AI. Revision of the dietary reference intakes for choline should include replacement of the AI with an estimated average requirement and a recommended dietary allowance, so that more accurate population estimates of inadequate intakes may be calculated.
Article
Choline is an important nutrient for humans. Choline intake of the European population was assessed considering the European Food Safety Authority European Comprehensive Food Consumption Database and the United States Department of Agriculture Nutrient Database. Average choline intake ranges were 151-210 mg/d among toddlers (1 to ≤3 years old), 177-304 mg/d among other children (3 to ≤10 years old), 244-373 mg/d among adolescents (10 to ≤18 years old), 291-468 mg/d among adults (18 to ≤65 years old), 284-450 mg/d among elderly people (65 to ≤75 years old) and 269-444 mg/d among very elderly people (≥75 years old). The intakes were higher among males compared with females, mainly due to larger quantities of food consumed per day. In most of the population groups considered, the average choline intake was below the adequate intake (AI) set by the Institute of Medicine in the USA. The main food groups contributing to choline intake were meat, milk, grain, egg and their derived products, composite dishes and fish. The main limitations of this study are related to the absence of choline composition data of foods consumed by the European population and the subsequent assumption made to assess their intake levels. Given the definition of AI, no conclusion on the adequacy of choline intake can be drawn for most European population groups. Such results improve the knowledge on choline intake in Europe that could be further refined by the collection of choline composition data for foods as consumed in Europe.
Article
Despite recommendations for higher choline intakes during pregnancy and lactation, there is limited research regarding maternal intake during these important periods. In the present study, we estimated dietary choline intake during pregnancy and lactation in a population of Albertan women and the contribution of egg and milk consumption to intake. Dietary intake data were collected from the first 600 women enrolled in a prospective cohort study carried out in Alberta, Canada. During the first and/or second trimester, the third trimester and 3 months postpartum, 24 h dietary intake recall data were collected. A database was constructed including foods consumed by the cohort and used to estimate dietary choline intake. The mean total choline intake value during pregnancy was 347 (sd 149) mg/d, with 23 % of the participants meeting the adequate intake (AI) recommendation. During lactation, the mean total choline intake value was 346 (sd 151) mg/d, with 10 % of the participants meeting the AI recommendation. Phosphatidylcholine was the form of choline consumed in the highest proportion and the main dietary sources of choline were dairy products, eggs and meat. Women who consumed at least one egg in a 24 h period had higher (P< 0·001) total choline intake and were eight times more likely (95 % CI 5·2, 12·6) to meet choline intake recommendations compared with those who did not consume eggs during pregnancy. Women who reported consuming ≥ 500 ml of milk in a 24 h period were 2·8 times more likely (95 % CI 1·7, 4·8) to meet daily choline intake recommendations compared with those consuming < 250 ml of milk/d during pregnancy. Choline intake is below the recommendation levels in this population and the promotion of both egg and milk consumption may assist in meeting the daily choline intake recommendations.
Article
Recently, choline has been associated with neurodevelopment, cognitive function and neural tube defect incidence. However, data on usual intakes are limited, and estimates of dietary intakes of choline and its metabolite betaine, are not available for New Zealanders. The objective of the present study was to determine usual intake and food sources of choline and betaine in a group of New Zealand reproductive age women. Dietary intake data were collected from a sample of 125 women, aged 18-40 years, by means of a 3-day weighed food record, and usual choline and betaine intake distributions were determined. The mean (SD) daily intakes of choline and betaine were 316 (66) mg and 178 (66) mg, respectively. The total choline intake relative to energy intake and body weight was 0.18 mg/kcal and 5.1 mg/kg, respectively. Only 16% of participants met or exceeded the Adeuate Intake (AI) for adult women of 425 mg of choline. The top five major food contributors of choline were eggs, red meat, milk, bread and chicken; and of betaine were bread, breakfast cereal, pasta, grains and root vegetables (carrots, parsnips, beetroot, swedes). Our findings contribute towards the recent emergence of published reports on the range of dietary choline and betaine intakes consumed by free-living populations. In our sample of New Zealand women, few participants were meeting or exceeding the AI level. Given recent epidemiological evidence suggesting health benefits of increased choline and betaine intakes, recommendations should be made to encourage the consumption of choline and betaine-rich foods.
Article
Choline and betaine are involved in several similar health-relevant metabolic pathways, but the foods sources are different. We have assessed their intakes (individual, sums and ratios) from a dominantly Chinese food cultural point of view. A representative free-living Taiwanese population aged 13-64 years was drawn from the Nutrition and Health Survey in Taiwan (NAHSIT) 1993-1996. Food intake was derived from interviews as 24-hour recalls. The USDA database, with adaptations for Taiwan, provided choline and betaine food compositions. Major food contributors of these nutrients were identified and compared with data from the US Framingham offspring study. Mean and variance reduced median nutrient intakes were calculated. Top ten major food contributors of choline in Taiwan were eggs, pork, chicken, fish, soybean and its products, dark leafy vegetables, dairy, fruit, wheat products and light leafy vegetables in sequence. For betaine, the top ten were dark leafy vegetables, wheat products, fish, pork, bread, chicken, cake/cookies, grain-based alcoholic beverages, rice and its products and sauces. The main contributors of choline in Taiwan and the USA were, respectively, eggs and red meat; and for betaine, greens were similarly best contributor. The rankings of the main food contributors of choline and betaine differed substantially between Taiwan and the USA. The total daily intakes (mean±SE, mg) in Taiwan for choline were 372±19 (median=348) in men and 265±9 (median 261) for women; for betaine, values were 101±3 (median 93) in men and 78±8 (median 76) for women. These allow for health outcome considerations.