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Micronutrient Intakes in 553 Dutch Elite and Sub-Elite Athletes: Prevalence of Low and High Intakes in Users and Non-Users of Nutritional Supplements

TLDR
For most micronutrients, use of nutritional supplements does not completely compensate for intakes below the estimated average requirement (AR), so athletes should consider making better food choices and the daily use of a low-dosed multivitamin supplement.
Abstract
This study investigated whether athletes meet micronutrient recommendations and whether the adequacy of their intake is related to the use of dietary supplements, sport nutrition products or a combination. Micronutrient intakes of 553 Dutch (sub-) elite athletes were assessed using web-based 24-h dietary recalls with accompanying nutritional supplement questionnaires. In the majority of both users and non-users of dietary supplements, vitamin D intake was below the estimated average requirement (AR) if supplements were not included in the analysis. Including dietary supplements improved vitamin D intake, but still a part of the athletes, both men and women, reported an intake below the AR. Non-users of dietary supplements were particularly at risk for low intakes of vitamins B1, B2, B3 and vitamins A, C and selenium. Mean iron intake was reported below the AR in a substantial group of women, both users and non-users. The use of sport nutrition products contributed only slightly to micronutrient intake. A small prevalence of athletes using dietary supplements showed intakes of some micronutrients above the Upper Level. In conclusion, both users and non-users of nutritional supplements reported inadequate intake of micronutrients. For most micronutrients, use of nutritional supplements does not completely compensate for intakes below AR. Athletes should consider making better food choices and the daily use of a low-dosed multivitamin supplement.

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Article
Micronutrient Intakes in 553 Dutch Elite and
Sub-Elite Athletes: Prevalence of Low and High
Intakes in Users and Non-Users of
Nutritional Supplements
Floris Wardenaar
1,
*, Naomi Brinkmans
1
, Ingrid Ceelen
1
, Bo Van Rooij
1
, Marco Mensink
2
,
Renger Witkamp
2
and Jeanne De Vries
2
1
HAN University of Applied Sciences, Sports and Exercise Studies, 6525 AJ Nijmegen, The Netherlands;
Naomi.brinkmans@han.nl (N.B.); Ingrid.ceelen@han.nl (I.C.); Bo.v.rooij@gmail.com (B.V.R.)
2
Division of Human Nutrition, Wageningen University, 6700 EV Wageningen, The Netherlands;
Marco.mensink@wur.nl (M.M.); Renger.witkamp@wur.nl (R.W.); Jeanne.devries@wur.nl (J.D.V.)
* Correspondence: Floris.wardenaar@han.nl; Tel.: +31-062-274-7294
Received: 4 December 2016; Accepted: 9 February 2017; Published: 15 February 2017
Abstract:
This study investigated whether athletes meet micronutrient recommendations and whether
the adequacy of their intake is related to the use of dietary supplements, sport nutrition products or a
combination. Micronutrient intakes of 553 Dutch (sub-) elite athletes were assessed using web-based
24-h dietary recalls with accompanying nutritional supplement questionnaires. In the majority of
both users and non-users of dietary supplements, vitamin D intake was below the estimated average
requirement (AR) if supplements were not included in the analysis. Including dietary supplements
improved vitamin D intake, but still a part of the athletes, both men and women, reported an
intake below the AR. Non-users of dietary supplements were particularly at risk for low intakes
of vitamins B1, B2, B3 and vitamins A, C and selenium. Mean iron intake was reported below
the AR in a substantial group of women, both users and non-users. The use of sport nutrition
products contributed only slightly to micronutrient intake. A small prevalence of athletes using
dietary supplements showed intakes of some micronutrients above the Upper Level. In conclusion,
both users and non-users of nutritional supplements reported inadequate intake of micronutrients.
For most micronutrients, use of nutritional supplements does not completely compensate for intakes
below AR. Athletes should consider making better food choices and the daily use of a low-dosed
multivitamin supplement.
Keywords:
dietary supplement; sport nutrition product; dietary intake; estimated average
requirement; guidelines
1. Introduction
Low micronutrient intake in athletes can result in deficiencies affecting health and performance,
in particular when this occurs for longer periods of time [
1
]. Some studies report that many athletes
do not meet micronutrient recommendations [
2
5
], whereas others conclude the opposite [
1
,
6
]. Shifts
and variations in food patterns over time [
7
,
8
], increased availability of nutritional supplements [
9
],
and changing viewpoints regarding requirements [
10
,
11
] merit regular monitoring of dietary intake by
athletes. At the same time, rapid developments in assessment tools, such as web-based approaches,
make it easier to gain insight in the intake of large groups of athletes [12,13].
No consensus exists on whether micronutrient requirements are different in athletes as compared
to the general population [
14
,
15
]. In practice, athletes are nowadays often advised to meet the general
recommended dietary reference intakes (DRI) for all micronutrients by consuming a diverse diet
Nutrients 2017, 9, 142; doi:10.3390/nu9020142 www.mdpi.com/journal/nutrients

Nutrients 2017, 9, 142 2 of 16
to ensure nutrient adequacy [
16
], paying special attention to optimal intake of iron, vitamin D and
calcium, and of antioxidants [
17
]. There seems to be less attention on the intake of B-vitamins [
17
].
Theoretically, exercise could increase the need for this group of micronutrients [
14
]. However, if energy
expenditure increases, food intake increases as well, which potentially could result in a higher vitamin
B intake. Unfortunately this is not necessarily the case, in particular when athletes make poor dietary
choices, resulting in a lower micronutrient intake than expected [
14
] because of a low micronutrient
density of the diet [5,6,18].
Nutritional supplements are frequently used by athletes [
19
], although use can be irregular
and varying over time [
20
]. Dietary supplements mainly comprise micronutrient supplements such
as vitamins and minerals. These supplements may promote athletes’ general health through the
prevention and treatment of nutrient deficiencies. On the other hand, sport nutrition products mainly
contain macronutrients, such as carbohydrates and protein, but can also contain micronutrients. These
sport nutrition products include, but are not limited to, sports drinks, recovery drinks, and sports bars.
Finally, the category of ergogenic supplements, such as creatine and caffeine, may contain additional
micronutrients although these products are also available as single bioactive substance products [21].
Therefore, nutritional supplements can be an important source of micronutrient intake.
Even though many athletes use multiple nutritional supplements at a time, this does not
necessarily guarantee adequate habitual dietary intake of micronutrients at an individual level [
7
].
In addition, case reports have shown that some athletes consume very high doses of certain
micronutrients exceeding the upper level (UL) also defined as tolerable upper intake level [
11
], possibly
resulting in reduced health and performance in the long term [
22
]. Examples of frequently reported
highly dosed micronutrient supplements used by individual athletes are antioxidants (i.e., vitamin C
and E) [
23
], vitamin D, iron and magnesium [
21
]. Further, practical experience and anecdotal reports
suggest a substantial use of high doses of vitamin B6 among athletes.
In the present study we aimed to evaluate the adequacy of micronutrient intake of Dutch
elite and sub-elite athletes, using a web-based 24-h recall method with accompanying nutritional
supplement questionnaires. In addition, we aimed to assess the effect of nutritional supplements
use on micronutrient intake, by making a comparison between both users and non-users of dietary
supplements, sport nutrition products or a combination of both. Ultimately this should lead to better
identification of athlete groups at risk of inadequate micronutrient intake, either too low or too high.
2. Materials and Methods
2.1. Study Design
The study was performed between February 2012 and June 2015 as described by Wardenaar et al. [24]
and others [
25
,
26
]. A total of 1800 athletes were informed about the study. A total of 759 elite
and sub-elite athletes were interested in participating in this study and delivering three or four
unannounced web-based, 24-h dietary recalls and questionnaires, preferably during a conditioning
training phase. Written informed consent to participate was provided by all contacted, and for
participants under the age of eighteen these documents were signed by their parents or guardian. No
incentive was given for participation in the study. The survey was approved by the Medical Ethics
Committee of Wageningen University.
2.2. Twenty-Four-Hour Recalls and Questionnaires
Dietary intake was estimated by combining information from web-based 24-h recalls and
questionnaires as previously described for our validation study [
13
]. The 24-h recall method was based
on the United States Department of Agriculture (USDA) five-step multiple-pass method [
27
,
28
], and
was collected with “Compl-eat
”, a program built by the Division of Human Nutrition, Wageningen
University. The web-based questionnaire, which was linked to the 24-h recall of a specific day, was
collected with “Vitality portal”, a web-based questionnaire module built by the HAN University

Nutrients 2017, 9, 142 3 of 16
of Applied Sciences. By this questionnaire, characteristics (i.e., weight (kg), height (cm) and age in
years), training load (total minutes of exercise per day) and nutritional supplement use were filled
out by the participants or by a trained sports dietician during a face to face or telephonic interview.
Nutritional supplements were defined as dietary supplements (i.e., micronutrients and essential
fatty acids),
sport nutrition
products (i.e., carbohydrate and protein based products) or ergogenic
supplements, for example creatine, b-alanine and other products with ergogenic claims [
21
]. For this
study all products containing micronutrients, classified as dietary supplements (including ergogenic
supplements) and sport nutrition products, were included in the analysis.
Two trained dieticians checked all web-based 24-h recalls and questionnaires for their
completeness and any unusual portion sizes (i.e., incorrect amounts), and processed all notes made by
the participants. If information on foods or nutritional supplements was missing, this was retrieved by
contacting subjects. Adjustments for missing data and errors and dealing with relevant notes were done
in a uniform way, using standard portion sizes and recipes according to a protocol [
29
]. Conversion
of reported food consumption into energy and micronutrient intake was done using the Dutch food
composition database of 2010 (Stichting NEVO, 2010), the Dutch database for dietary supplements
(NES), and individual product ingredient declarations. To be able to correct for within-person variation,
athletes had to deliver information for at least two complete days consisting of a complete 24-h recall
and questionnaire. Results of the 24-h recall and questionnaires were combined to calculate: median
(25–75 percentile) intake (g) of the most relevant basal nutrition food groups in relation to micronutrient
intake (16 out of 22 provided by the Dutch food composition database), and total energy (MJ) and
micronutrient intake (mg or µg) per gender and category.
2.3. Statistical Analyses
The statistical analysis included data of all athletes handing in at least two complete datasets
using the statistical software program SPSS (version 23, IBM, Armonk, NY, USA). Prevalence of
nutritional supplement use was reported as a percentage (%). Energy intake and micronutrient intake
was reported as mean
±
SD. Data was presented separately for men and women, for each of the four
subgroups: non-users of nutritional supplements (‘non-users’), users of dietary supplements (DS),
users of sport nutrition products (SNP) and users of a combination of both (DS + SNP).
Intake data was checked for normal distribution, by visual inspection of histograms and based
on skewness and kurtosis. The intake distribution was adjusted for day to day variation using the
following formula: SD
corrected
= SD
observed
×
r
ic
where r
ic
is the intra class correlation coefficient
(P =
δ
s
2
/
δ
s
2
+
δ
e
2
). Precision of the mean estimate (D
t
) of basal nutrition intake was acceptable around
10% for most micronutrients, and mostly below 20% [
30
]. The ratio of calculated energy intake/Basal
Metabolic Rate (BMR) using Schofield’s formula [
31
] may be referred to as the food intake level (FIL)
value, and was used to evaluate possible underreporting by comparison to a previously defined lower
limit Physical Activity Level (PAL) of 1.55 [13].
The software program PC-SIDE (version 1.0), developed by the Department of Statistics and
Center for Agricultural and Rural Development (CARD) at Iowa State University, was used to
estimate distribution of usual intake [
32
]. This distribution was compared with the estimated average
requirement (AR) based on Nordic Nutrition Recommendations [
11
] using the cut-off approach [
33
].
As for magnesium, only the Adequate Intake (AI) was available [
11
]; 75% of the AI was used as an
estimator of average requirement. The prevalence (%) of athletes with an actual micronutrient intake
exceeding the upper level (UL) [
11
] was calculated within each subgroup for all individuals using
nutritional supplements.
Differences within and between subgroups for each gender were analysed using
Wilcoxon-signed-rank-test, Kruskall-Wallis and Mann-Whitney-U-test using a Monte Carlo approach.
Statistical significance was set at p 0.05, no additional corrections were done for type II errors.

Nutrients 2017, 9, 142 4 of 16
3. Results
A substantial part of the 759 athletes (n = 206) provided incomplete dietary information, i.e., less
than 2 complete days. As a consequence, a total of 553 athletes, both men (59%) and women (41%), were
included in the final analysis of this study. All results described in this paragraph are reported in Table 1.
They recorded an average of 2.83 days by 24-h recalls and accompanying nutritional supplement intake
questionnaires per person. For men and women respectively, 157 and 83 participants were classified
as endurance athletes, 138 and 104 participants as team sports athletes, and 32 and 39 participants as
strength athletes as described in Wardenaar et al. [
24
]. Mean age of the men was 23.5
±
11.5 years and
of the women 22.0
±
7.6 years, and mean exercise time was 93.5
±
61.3 min per day. Reported energy
intake was on average 11.7
±
3.2 MJ for men and 9.1
±
2.5 MJ for women. Mean food intake level (FIL)
values, as an indicator of the quality of energy reporting, were slightly higher for men (mean
±
SD:
1.55
±
0.39) than for women (1.50
±
0.42) and differed between non-users and users of nutritional
supplements resulting in a somewhat lower FIL in those not using supplements. Non-users of DS
and SNP were mainly younger athletes in comparison to the other categories and particular users of
DS + SNP were the oldest and reported the highest exercise load.
Of the total group of athletes, 61.8% reported the use of one or more nutritional supplements; 65%
in men, and 56% in women. The use of DS alone was slightly lower in men (20%) than women (24%),
while the use of SNP alone was more frequently reported by men (24%) than women (17%), as was the
combined use of DS + SNP (men: 21%, women: 15%).
3.1. Basal Diet Intake
Food group intake is shown in Table 2 showing that median intake of athletes in all categories
shows a divers consumption pattern. The most consumed food groups contributing to micronutrient
intake were: milk products, meat, vegetables, cereals and grains and potatoes, fruit and bread.
The consumption of eggs, fish and vegetarian meat-replacement products was low. In most cases,
vegetable and fruit consumption was below the minimum recommendations of 150 grams and 2
servings respectively.
For men, micronutrient intake from the basal diet, i.e., excluding nutritional supplements, was
in most cases lower in non-users than in all subgroups of users (Table 3, p < 0.05). In women this
difference was less pronounced except for the users of DS + SNP, who reported higher mean intakes
than non-users, DS users and SNP users (p < 0.05).
3.2. Total Micronutrient Intake
When nutritional supplements were included, users of DS and DS + SNP reported a higher
total intake of all micronutrients as compared to the basal diet for both men and women (p
0.05).
For SNP users
(both men and women) the same trend was seen, except for vitamin A, vitamin D, iron,
copper, selenium and zinc, for which values did not differ with the basal diet after including SNP in
the calculation (p > 0.05).
Differences in mean intake existed between subgroups for almost all nutrients. Intake for most
micronutrients was higher in users of DS and DS + SNP than in non-users and users of SNP in both
men and women (p
0.05). In men, users of SNP also reported higher intake of most nutrients than
non-users (p
0.05), except for vitamin A and D. Women using SNP only reported higher intakes than
non-users for vitamin B2, B3, B6, folate equivalents and selenium (p 0.05).

Nutrients 2017, 9, 142 5 of 16
Table 1. Mean ± SD of characteristics, duration of exercise and energy intake per day, and food intake level (FIL) for the total group and subgroups of athletes.
Characteristics
Men (n = 327) Women (n = 226)
Non-Users Users DS Users SNP Users DS and SNP Non-Users Users DS Users SNP Users DS and SNP
A B C E F G H I
Number ( n) and % 115 (35%) 67 (20%) 77(24%) 68 (21%) 99 (44%) 53 (24%) 39 (17%) 35 (15%)
Endurance (n) 36 40 44 37 33 21 9 20
Team (n) 68 25 20 25 55 19 20 10
Strength (n) 11 2 13 6 11 13 10 5
Height (cm) 177 ± 12.4 180 ± 10.4 183 ± 7.5
a
184 ± 8.1
a,b
173 ± 6.7 172 ± 9.9 171 ± 9.7 174 ± 8.6
Weight (kg) 67.7 ± 15.3 70.7 ± 13.3
75.3 ± 9.9
a,b
78.4 ± 12.0
a,b
64.8 ± 7.3 63.1 ± 9.9 64.6 ± 9.9 66.3 ± 8.8
BMI (kg
1
·m
2
)
21.3 ± 2.9 21.6 ± 2.4
22.5 ± 2.0
a,b
23.0 ± 2.3
a,b
21.8 ± 1.9 21.3 ± 2.2 22.0 ± 2.2
g
22.0 ± 2.3
Age (year) 21.1 ± 11.9 22.3 ± 10.6
a
26.4 ± 12.4
a,b
25.3 ± 9.7
a,b
20.3 ± 5.7 22.5 ± 9.2 20.0 ± 4.4
28.1 ± 9.2
f,g,h
Exercise time (min
1
·day)
69 ± 59 75 ± 39
a
96 ± 56
a
96 ± 47
a,b
95 ± 63 117 ± 78
117 ± 69
f
131 ± 59
f
Energy intake (MJ) 10.5 ± 2.4 11.7 ± 3.6
a
12.5 ± 3.4
a
12.9 ± 3.2
a,b
8.7 ± 2.0 8.9 ± 3.1 9.4 ± 2.3
10.5 ± 2.6
f,g
Food intake level (FIL) 1.44 ± 0.3 1.54 ± 0.4
a
1.62 ± 0.4
a
1.64 ± 0.4
a
1.40 ± 0.3 1.47 ± 0.5 1.52 ± 0.4
1.73 ± 0.4
f,g,h
Capital letters (A–I) are used as a label for subgroups for gender. Lower case letters displayed below a specific value indicate that this value is significantly larger than the corresponding
column defined with a capital. Significance based on Mann-Whitney U test was set at p-value of 0.05, significant values of p 0.001 were displayed with a cursive lower case.

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