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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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