Brooke Beerman

Download as pdf or txt
Download as pdf or txt
You are on page 1of 10

Journal of the American College of Nutrition

ISSN: 0731-5724 (Print) 1541-1087 (Online) Journal homepage: https://www.tandfonline.com/loi/uacn20

Nutritional Intake and Energy Availability of


Collegiate Distance Runners

Brooke L. Beermann, Deborah G. Lee, Hawley C. Almstedt & William P.


McCormack

To cite this article: Brooke L. Beermann, Deborah G. Lee, Hawley C. Almstedt & William P.
McCormack (2020): Nutritional Intake and Energy Availability of Collegiate Distance Runners,
Journal of the American College of Nutrition, DOI: 10.1080/07315724.2020.1735570

To link to this article: https://doi.org/10.1080/07315724.2020.1735570

Published online: 19 Mar 2020.

Submit your article to this journal

Article views: 3

View related articles

View Crossmark data

Full Terms & Conditions of access and use can be found at


https://www.tandfonline.com/action/journalInformation?journalCode=uacn20
JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION
https://doi.org/10.1080/07315724.2020.1735570

Nutritional Intake and Energy Availability of Collegiate Distance Runners


Brooke L. Beermann, Deborah G. Lee, Hawley C. Almstedt and William P. McCormack
Department of Health and Human Sciences, Loyola Marymount University, Los Angeles, California, USA

ABSTRACT ARTICLE HISTORY


Objective: Research investigating the dietary habits of distance runners has presented varying Received 25 September 2019
results. Proper dietary intake appears to enhance distance running performance and low dietary Accepted 24 February 2020
intake may impact health. The purpose of this investigation was to perform a comprehensive
KEYWORDS
evaluation of nutrient intake of collegiate distance runners with comparison to recommendations
Carbohydrate intake; bone-
for athletes. free lean mass; fat free
Methods: Twenty-one men (Age: 19.6 ± 1.2 years; height: 177.1 ± 5.7 cm; body mass: 65.7 ± 4.6 kg; mass; protein intake;
body fat: 15.5 ± 2.2%) and 20 women (Age: 20.2 ± 1.7 years; height: 162.9 ± 6.6 cm; body mass: macronutrients;
53.7 ± 6.5 kg; body fat: 23.3 ± 3.6%) volunteered to participate in the investigation. Energy intake micronutrients
was derived from the Block Food Frequency Questionnaire. Energy availability was calculated by
subtracting exercising energy expenditure from daily energy intake, divided by bone free lean
mass and fat-free mass. Macronutrient and micronutrient consumption were compared with the
appropriate dietary reference intake values, U.S. Dietary Guidelines, or standards recommended for
endurance athletes.
Results: Dietary intake for the men was 2,741.0 ± 815.2kilocalories and for the women was
1,927.7 ± 638.2kilocalories. A majority of the runners (73%) consumed less than recommended lev-
els of carbohydrates. All men and 75% of women met or exceeded the recommended daily pro-
tein intake. Fifty percent of women and 24% of men did not meet the recommended daily
allowance for calcium. Ninety-five percent of the runners did not meet the RDA for vitamin D. All
the men and 75% of the women met the RDA for iron intake, with 24 of the runners taking an
iron supplement. Eight men and 10 women did not meet the recommended intake for potassium.
Conclusion: The dietary intake in this group of distance runners is below that necessary for the
level of energy expended in their training. Carbohydrate intake is below the recommended
amount for endurance athletes, and the calcium and vitamin D intake may not be favorable for
bone health in this group of distance runners.

Abbreviations: AMDR: acceptable macronutrient distribution range; BFLM: bone-free lean mass;
BMI: body mass index; BW: body weight; CHO: carbohydrate; DRI: dietary reference intake; DXA:
dual-energy x-ray absorptiometry; EA: energy availability; EEE: exercising energy expenditure; EI:
energy intake; FFQ: food frequency questionnaire; FFM: fat-free mass; Kcals: kilocalories; LBM: lean
body mass; MET: metabolic equivalent; PRO: protein; REDS: relative energy deficiency in sport;
RMR: resting metabolic rate; SD: standard deviation; Vit: vitamin

Introduction metabolic pathways that require micronutrients, and exercise


may result in muscular changes that escalate needs for some
Collegiate-level student-athletes often have a difficult time
vitamins and minerals (3). Proper nutrition can help to
meeting nutritional requirements due to frequent travel,
counteract the damaging effects of high-intensity training
demanding schedules, limited food availability, and changing
environments. In sports that favor a lean build, such as dis- including suppression of the immune system, increased
tance running, there is pressure for the athlete to eat a inflammation, and increased risk for infection. In particular,
nutrient dense diet in order to enhance performance, yet previous research has identified iron, zinc, vitamin A and D
many athletes may restrict dietary intake in order to main- as important micronutrients for immune health in athletes
tain or achieve a lean body composition in effort to enhance (4). Iron intake is particularly important for distance run-
performance. Nutrient requirements for athletes are higher, ners who often exhibit compromised iron status due to
as aerobic athletes need more carbohydrate than non-ath- hemolysis, alterations in hormones that regulate iron, insuf-
letes to fuel exercise and replace glycogen (1). In addition, ficient iron consumption, and menstrual blood losses for
protein needs for athletes are greater due to degradation and female athletes (5). These factors together can foster a diet
use of amino acids as an energy source during prolonged at risk for a number of nutritional deficiencies, specifically
endurance exercise (2). High-intensity training stresses in carbohydrates, vitamin D, iron, calcium, and zinc (6).

CONTACT William P. McCormack [email protected] Department of Health and Human Sciences, Loyola Marymount University, 1 LMU Dr. MS
8888, Los Angeles, CA 90045, USA.
ß 2020 American College of Nutrition
2 B. L. BEERMANN ET AL.

Diets lacking in macronutrients and micronutrients may athletes (26, 27). In a review, Loucks (2007) reported that
negatively affect performance and increase the risk for injury female athletes may consume approximately 30% less energy,
and illness (5). especially carbohydrates, than their male counterparts (28).
Previous research examining nutrient intake among non- Across many studies, there is a trend of low EA among
collegiate distance runners or endurance athletes in general is female athletes (24, 29, 30). Most of the research on EA has
equivocal. It appears that multisport and endurance athletes examined endurance sports (31–33) although Woodruff and
may not be meeting recommendations for energy and Meloche (2013) reported EA in collegiate volleyball players
carbohydrate intake (7–9), however, Japanese endurance (34). Several investigations have examined EA in male athletes,
athletes (10) and one study of distance runners (11) reported including older endurance athletes (35), recreationally active
achievement of carbohydrate and protein needs. Examination men (36), however more research is needed among collegiate
of elite distance runners from Kenya, reported 75% of energy distance runners, especially males. EA is difficult to assess
intake from carbohydrates with an average consumption accurately as there are many variables involved and measuring
of more than 10 g of carbohydrate relative to kg of body energy intake relies on self-reported data from athletes (37, 38).
weight (12). A number of studies have reported dietary intake Some research indicates EA should be reported relative to fat-
of distance runners or endurance athletes ranging in age free mass (FFM) (3, 24, 28), while others use the term lean
from 18 to 40 years with the purpose of assessing the influ- body mass (LBM) (39, 40), and still further literature uses the
ence of nutrition on risk for stress fractures (13–15), report- terms interchangeably (37). If researchers use dual-energy x-ray
ing that nutrients such as calcium, vitamin D, and protein absorptiometry (DXA) to measure body composition, as is rec-
may influence risk for stress fracture among runners (14, 15). ommended (37) due to its high precision (3), then reports are
When narrowing the research to focus on collegiate able to be more specific about whether bone mass is included
athletes in particular, including distance runners, previous in the denominator of the EA equation. Unlike other methods
investigations show energy, carbohydrate, protein, and of body composition assessment, like underwater weighing and
calcium intake to be under recommendations while some skinfold measurement, DXA uses a three-component model,
male athletes overconsumed fat (16–19). Only a few studies reporting fat mass, bone mass, and other fat-free soft tissue
have examined the nutritional habits specifically of collegiate which sum to total body mass (41).
distance runners (20–22). The results of these studies show In effort to provide clarity in calculations, we aimed to
that male collegiate runners, but not females, tend to meet analyze EA using only lean mass in comparison to lean
total energy needs while calcium and vitamin D intake mass with bone mass. With a limited number of studies on
are lower than recommendations. In general, the research the dietary intake and EA of male and female collegiate dis-
literature among collegiate distance runners is incomplete, tance runners, the purpose of this investigation was to per-
lacking examination of macro and micronutrients (21), form a comprehensive evaluation of nutrient intake of
inclusion of both male and female athletes (20), and com- collegiate distance runners with comparison to recommen-
parisons to standards or recommendation for athletes (22). dations for athletes.
With high training loads and increased nutritional needs,
suboptimal eating habits among athletes can lead to low
energy availability (EA) and subsequent health consequences Materials and methods
(23). Rather than evaluating energy balance, EA associates Participants
energy intake with ideal health and physical performance
(3). EA, defined as total energy intake minus energy Twenty-one men and 20 women from a National Collegiate
expenditure due to exercise, relative to fat free mass, is Athletic Association Division I cross-country team volun-
an important foundation for health and success of sport teered to participate in this study. Data collection occurred
nutrition strategies (23, 24). Low EA may be caused by during the competitive season for collegiate cross-country
disordered eating, restrictive eating, poor nutritional runners. At the time of dietary assessment, the runners were
knowledge, sudden increases in training intensity or volume training in excess of 100 km weekly, including two high-
without diet alterations, or simply unintentional failure to intensity workouts per week (interval, hill repeats, or race
consume sufficient calories. EA is an underlying feature day) and one long run of 20–25 km. In addition, the runners
of the female athlete triad, a syndrome of clinical issues performed four weekly cross-training sessions; two 1-hour
including disordered eating, menstrual dysfunction, and resistance training sessions, and two 1-hour aerobic training
poor skeletal health (24). Recently researchers have proposed sessions either “running” with a floated vest in the pool or
Relative Energy Deficiency in Sport (REDS) as a cluster of riding a cycle ergometer. The investigation was approved by
physiological complications observed in athletes of both the Loyola Marymount University Institutional Review
sexes when EA is below needs (23, 25). REDS affects endo- Board for Human Subjects. All participants provided written
crine, hematological, metabolic, cardiovascular, and immune informed consent prior to initiating the study.
systems while also impairing performance and increasing
risk for injury (5).
Nutrient intake
EA has been investigated in a number of sports, mainly
in female endurance athletes, although there is a growing Participants completed the Block 2014 Food Frequency
interest investigating this issue among male endurance Questionnaire (FFQ) via online survey, at their leisure. The
JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION 3

Table 1. Demographic and body composition variables for male and female regular exercise over the previous three months.
collegiate distance runners.
Training records were scored using metabolic equivalents
Males (n ¼ 21) Females (n ¼ 20)
Variable
(MET-hoursweek1) from the compendium of physical
Age (yrs) 19.6 ± 1.2 20.2 ± 1.7
Height (cm) 177.1 ± 5.7 162.9 ± 6.6
activity (52) to integrate energy expenditure at a variety of
Weight (kg) 65.7 ± 4.6 53.7 ± 6.5 intensities and for the reported lengths of time. To avoid
BMI (kg  m2) 21.0 ± 1.3 20.2 ± 1.6 overestimating energy expended during exercise, we
% body fat 15.5 ± 2.2 23.3 ± 3.6
BFLM (kg) 53.3 ± 4.2 39.4 ± 4.5
incorporated activities with an intensity greater than 4.0
FFM (kg) 55.7 ± 4.3 41.3 ± 4.7 METs (33, 53). EEE was the total of all exercise (>4.0
Note. Data are presented as means ± SD. BFLM ¼ bone-free lean mass METs) multiplied by the hours of activity and BFLM or
determined by dual energy x-ray absorptiometry; FFM ¼ sum of soft-tissue FFM. Additional modifications to EEE eliminated the
lean mass and bone mass determined by dual energy x-ray absorptiometry.

Males and Females were significantly different, p < 0.001. number of kilocalories contributed by resting metabolic rate
(RMR) during the hours of exercise (33, 38). Estimation of
questionnaire includes 127 beverage and food items, RMR was calculated using the Cunningham equation (54).
with additional questions to modify for consumption of In summary, adjusted EEE was the raw EEE minus RMR
carbohydrates, fats, protein, simple sugars and foods made per hour, multiplied by the number of hours of exercise at
from whole grains. The survey incorporates questions 4.0 METs or greater. The adjusted EEE was then subtracted
to assess supplemental, fortified, and enriched food sources from EI and divided by BFLM or FFM to calculate EA.
of nutrients. The food list of the FFQ is based on the For this investigation, EA has been categorized as optimal
United States Department of Agriculture Food and Nutrient for weight maintenance when it was 45 kcalkg1, sub-
Database, which was derived from data collection of the optimal when it is between 30–44 kcalkg1, and clinically
National Health and Nutrition Examination Survey. FFQ low when it was <30 kcalkg1 (24, 55). The number of
runners with EA in each of these categories was determined.
prompts inquire about portion sizes and frequency of con-
For comparison purposes, calculations were performed using
sumption on a monthly, weekly, and daily basis. Visuals assist
BFLM and FFM (including bone mass) as the denominator
in estimating the accurate portion sizes. The Block FFQ is
to analyze this influence on average EA of runners and
recognized as a valid (42) and reliable (43) measure of nutri-
categorization of EA as optimal, suboptimal, or clinically low.
tional intake over the preceding 12 months (44). Results for
micronutrients are reported as dietary intake from food and
beverages and total intake, which includes supplemental sour- Statistical analysis
ces. This analysis focused on micronutrients of particular
importance to athletes and those that are often problematic Descriptive statistics are presented with means, standard
for Americans (5, 45). The mean intake for macronutrients deviations, and range from low to high. Values were
and micronutrients were calculated for men and women and compared to current Dietary Reference Intakes (46–51), U.S.
compared to recommended values for athletes (3) and the Dietary Guidelines (45), or standards established as appro-
Dietary Reference Intakes (46–51). priate for endurance athletes (3). Analysis of variance was
used to compare mean values of macro and micronutrients
between the sexes. All analyses were performed using SPSS
Body composition Version 22 (IBM Corp.; Armonk, NY) and a significance
level of less than 0.05 was applied throughout.
Dual-energy x-ray absorptiometry (DXA; Hologic Discovery
A, Waltham, MA) of the whole body was used to measure
bone-free lean mass (BFLM), fat-free mass (FFM), and per- Results
cent body fat. For the purpose of this research, BFLM is the
Participants
total mass of the body derived by DXA without bone mass or
fat mass. The term FFM used in this paper refers to the total Participant characteristics are presented in Table 1. Volunteers
mass of the body derived by whole body DXA scan, exclud- had a reported mean running history of 7.3 ± 2.2 years and
ing fat mass, and therefore includes soft-tissue lean mass and identified themselves as White (64%), Hispanic (29%),
bone mass. Whole body scans were performed and analyzed and Asian (7%). Male and female athletes were similar in age
by one technician after daily calibration. Body mass index and BMI, however men were significantly taller, heavier, and
(BMI) was calculated from the height and weight measure- had a lower percent body fat than female athletes.
ments taken without shoes while wearing light clothing.
Macronutrients
Energy availability
Mean daily consumption macronutrients and recommended
EA was determined by subtracting exercising energy expend- intakes are presented in Table 2. In comparison to female
iture (EEE) from daily energy intake (EI) and dividing by athletes, male athletes consumed significantly more energy,
BFLM or FFM, derived from DXA. The Block FFQ provided grams of protein relative to body weight (BW), percent
EI as total daily kilocalorie consumption. Training logs were of kcals from protein, and grams of dietary fat (p < 0.05).
used to collect information about intensity and duration of A majority (73%) of the athletes consumed less than the
4 B. L. BEERMANN ET AL.

Table 2. Macronutrient intake among male and female collegiate distance athletes.
Males Females
Mean ± SD Not meeting recommendations Mean ± SD Not meeting recommendations Recommended
(n ¼ 21) N, % (n ¼ 20) N, % Intakea,b,c
Total energy intake (kcals) 2,741.8 ± 815.2 NA 1,927.7 ± 638.2 NA NA
(1,404–4,314) (1,076–3,589)
Dietary CHO (gkgBW1) 5.3 ± 1.7 13, 62% 4.7 ± 1.9 17 (85%) 6–10a
(2.66–8.70) (2.32–10.4)
% kcals from CHO 50.7 ± 5.9 4, 19% 51.0 ± 6.2 5, 25% 45–65%b
(35.8–61.3) (41.6–66.7)
Dietary PRO (gkgBW1) 1.8 ± .5 6, 29% 1.4 ± 0.6 7, 35% 1.2–2.0a
(1.07–2.79) (0.72–3.1)
% kcals from PRO 17.1 ± 2.0 0 15.2 ± 1.8 0 10–35%b
(13.3–22.3) (11.4–18.3)
Dietary fat (g) 104.1 ± 38.8 NA 75.8 ± 28.5 NA NA
(47.3–191.2) (34.5–147.8)
% kcals from fat 33.7 ± 5.0 9, 43% 35.2 ± 4.7 11, 55% 20–35%b
(24.1–45.6) (23.1–41.8)
% kcals from SFA 10.9 ± 2.3 13, 62% 11.1 ± 2.1 13, 65% <10%c
(6.3–15.9) (8.7–16.8)
Range presented in parentheses; the number (N) and percent of participants not meeting recommended values are displayed; kcals ¼ kilocalories; BW ¼ body
weight; CHO ¼ carbohydrates; PRO ¼ protein; SFA ¼ saturated fatty acids.
a
Thomas et al., 2016.
b
Acceptable Macronutrient Distribution Range.
c

Dietary Guidelines for Americans, 2015–2020.
Signifies the mean values between men and women are significantly different (p < 0.05).

Table 3. Energy availability in male and female collegiate distance runners. whether calculated using BFLM or FFM. Paired t-tests
Energy availability Males (n ¼ 20) Females (n ¼ 17) showed that calculating EA using FFM, which included
kcals  BFLM1 (M ± SD) 35.2 ± 15.1 35.2 ± 17.1 2 kg of bone mass measured via DXA, results in signifi-
(8.8–65.8) (12.2–69.0) cantly lower values than EA calculated using BFLM
45 kcals  BFLM1 5, 25% 4, 24%
30–44 kcals  BFLM1 6, 30% 6, 35% (p < 0.001). When categorizing the EA of athletes according
<30 kcals  BFLM1 9, 45% 7, 41% to thresholds established in the literature, 43% had clinically
kcals  FFM1 (M ± SD) 33.1 ± 15.0 32.8 ± 16.1
(7.5–61.5) (11.0–64.7)
low EA, while 32% or 38% had subclinical low EA when
45 kcals  FFM1 4, 20% 3, 18% using BFLM and FFM, respectively. Relatively few, 19–24%,
30–44 kcals  FFM1 7, 35% 7, 41% met EA needs for weight maintenance, optimal endocrine
<30 kcals  FFM1 9, 45% 7, 41%
function, and healthy bone metabolism.
Note. Data are reported as mean (M) ± standard deviation (SD) with the
range in parentheses; the number (N) and percent of participants below the
recommended 45 kcals  BFLM1 or FFM1 are displayed; BFLM ¼ bone-free
lean mass determined by dual energy x-ray absorptiometry; FFM ¼ soft-tissue Micronutrients

lean mass and bone mass determined by dual energy x-ray absorptiometry.
Significantly lower than kcals  BFLM1, p < 0.001. Data for micronutrient intake is presented in Table 4. Male
athletes consumed significantly greater amounts of calcium,
recommended 6–10 g  kg1BW of carbohydrates for dietary iron, zinc, vitamin B12, dietary vitamin C, and vita-
high-intensity endurance sports such as collegiate distance min D than female athletes. Supplement use by female ath-
running. Only one female runner consumed more than the letes allowed total iron and vitamin C intake to be similar
recommended 10 g  kg1BW. Five female (25%) and 4 male among the sexes while dietary intake alone differed. Average
(19%) athletes fell under the acceptable macronutrient total calcium intake for men and women were both above
distribution range (AMDR) for CHO, while one female the RDA for adults ages 19 years and older, however, 50% of
athlete reported carbohydrate consumption above the AMDR the women and 24% of the men were below the recom-
at 67%. Mean protein intake for the men and women were mended calcium intake for their age. Mean iron intake was
both within the AMDR, however five women (25%) were well above the RDA, though individually five of the female
below recommended protein intake for athletes when control- athletes (25%) consumed below the recommended threshold.
ling for body weight. Eight of the athletes (6 men and 2 Twenty-four of the runners reported taking a dietary supple-
women) ate more than 2 g  kg1BW of protein. All athletes ment for iron, which was a contributing factor for the seven
consumed at least 20% of kcals from fat, however 49% males (33%) and eight females (40%) who consumed more
of the athletes consumed more than 35% of kcals from fat. than the upper limit for iron. While average potassium
When examining types of fatty acids consumed, over half of intake met the expected adequate intake levels, eight men
the athletes ate more than 10% of kcals from saturated fats. (38%) and 10 women (50%) fell short. All of the men and
65% of the women met the RDA for zinc, while one male
athlete consumed more than the upper limit. Three men
Energy availability
(14%) and seven women (35%) fell short of the RDA for
Results for EA calculations are presented in Table 3. Male vitamin A, while two females consumed more than the
and female distance runners had similar EA to each other upper limit. Vitamin B12 and vitamin C intake met the RDA
JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION 5

Table 4. Consumption of selected vitamins and minerals among male and female collegiate distance runners.
Males Females
Micronutrient Mean ± SD (n ¼ 21) Below DRI N, % Mean ± SD (n ¼ 20) Below DRI N, % Recommended intake
Dietary calcium (mg  day1) 1,357.5 ± 352.0 965.0 ± 398.8
Total calcium (mg  day1) 1,468.5 ± 397.2 5, 24% 1,154.7 ± 552.5 10, 50% 18 yrs: 1,300
19 yrs: 1,000
(888.5–2,569.3) (497.9–1,849.4)
Dietary iron (mg  day1) 23.3 ± 6.3 15.2 ± 4.9
Total iron (mg  day1) 43.6 ± 27.2 0 44.0 ± 25.6 5, 25% 18 yrs M: 11, F: 15
19 yrs M: 8, F: 18
(16.9–96.3) (6.5–80.5)
Total potassium (mg  day1) 3,614.4 ± 977.8 8, 38% 2,806.5 ± 1,120.1 10, 50% 18 yrs M: 3,000, F: 2,300a
19 yrs M: 3,400, F: 2,600a
(1,742.0–5,388.1) (1,259.5–5,685.0)
Total sodium (mg  day1) 4485.2 ± 1609.0 0 2912.0 ± 935.2 0 1500a
(2152.7–7999.0) (1656.0–5,410.3)
Dietary zinc (mg  day1) 18.8 ± 5.0 11.8 ± 3.9
Total zinc 23.1 ± 11.5 0 14.9 ± 7.3 4, 20% M:11
F 18 yrs: 9; F 19 yrs: 8
(11.0–65.1) (6.3–34.2)
Dietary Vit A (mg  day1) 1,123.8 ± 330.9 927.0 ± 502.0
Total Vit A (mg  day1) 1,309.3 ± 471.6 3, 14% 1,313.4 ± 934.5 7, 35% M: 900, F: 700
(615.4–2,727.1) (338.8–3,708.7)
Dietary Vit B12 (mg  day1) 9.3 ± 2.6 5.2 ± 2.3
Total Vit B12 (mg  day1) 10.8 ± 3.2 0 6.5 ± 3.2 0 2.4
(6.9–18.7) (2.5–12.0)
Dietary Vit C (mg  day1) 162.8 ± 63.1 123.2 ± 51.8
Total Vit C (mg  day1) 275.6 ± 263.9 0 185.9 ± 134.2 2, 10% 18 yrs M: 75, F: 65
19 yrs M: 90, F: 75
(84.4–1214.8) (39.8–639.5)
Dietary Vit D (IU  day1) 277.7 ± 109.8 122.3 ± 86.0
Total Vit D (IU  day1) 336.2 ± 179.0 20, 95% 213.8 ± 180.2 19, 95% 600
(63.6–892.9) (54.8–680.7)
Note. Range of data is presented in parentheses; the number (N) and percent of participants not meeting recommended values are displayed; Total intake
includes supplemental sources, while dietary intake is from food and beverages alone; DRI ¼ Dietary Reference Intake; Vit ¼ vitamin; M ¼ males; F ¼ females.
a

indicates reference standard is an Adequate Intake, all other micronutrient reference values are Recommended Dietary Allowances.
Males and females are significantly different, p < 0.05.

for most athletes, with two females (10%) consuming should consume 1.6–2.4 g/kg, and endurance-trained athletes
less than the recommendation for vitamin C. A majority who consume protein at the upper end of the 1.2–2.0 g/kg
of athletes (95%) did not consumed the RDA for vitamin D. (1.83 g/kg) recommendation may have metabolic and
All of the athletes who consumed more than the RDA performance advantages (5, 56). Protein intake may become
for any micronutrient were using dietary supplements. more important when CHO intake is limited or when EA is
low, as is the case for these collegiate distance runners (3).
We report an elevated proportion of energy derived from
Discussion
dietary fat in male and female collegiate distance runners.
The main finding of this investigation is the low Recommendations for athletes suggest dietary fat intake
energy intake and EA for both the men and women in this should meet public health guidelines (3). The findings
sample of collegiate distance runners. In particular, athletes reported here are similar to Hinton et al. who also found
consumed too little carbohydrate in comparison to recom- elevated fat and SFA intake, especially among male athletes
mendations for high-intensity, endurance athletes (3). Low (17). On a positive note, none of the athletes in this study
carbohydrate intake may impair performance and recovery showed a chronic intake of lipids below 20% of total energy,
(5) while also lowering immune function (4). Previous which is important to ensure sufficient fat-soluble vitamins,
research among collegiate athletes (17, 19), endurance essential fatty acids, and omega-3 fatty acids (3).
athletes (7, 8) and specifically collegiate distance runners Suboptimal EA was found in 75–80% of the athletes,
(20, 21) also report poor carbohydrate intake. while over 40% of both male and female cross-country
Unlike data reported in this paper, Masson & Lamarche runners met criteria for clinically low EA. Similar to reports
(2016) found no difference in relative protein intake in published research (27, 57), EA was not significantly
between male and female athletes (8). As a group, the men different between male and female distance runners.
in this study were eating significantly more protein while Previous research among female endurance/track athletes
some of the female athletes were not consuming enough. report as low as 20% (31) but as high as 52% (58) of athletes
Athletes need more protein than the RDA, which is set to have clinically low EA. Of the few studies exploring EA
for the general adult population, however research suggests in male athletes, prevalence of clinically low EA for endurance
several different targets for protein intake among athletes. sports ranges from 42 to 58% (27, 57). Much of the research
Protein needs for weight maintenance among track and field on the triad and REDS has focused on female athletes thus far,
athletes is 1.3–1.7 g/kg, athletes working to lose weight however these findings suggest male distance runners exhibit
6 B. L. BEERMANN ET AL.

similar prevalence of suboptimal and clinically low EA 1,500 mg of calcium per day along with 2,000 IU of vitamin
as female distance runners (35, 59). Without alteration, D to optimize bone health (3).
chronically low EA will lead to injury, illness, and alterations All of the male runners and most (75%) of the female
in endocrine, reproductive, metabolic, and cardiovascular runners were consuming at or above the RDA for iron.
health (23, 38, 60, 61). Consumption of this trace mineral is particularly important
Some of the differences in EA reported in the literature for distance runners who are at greater risk of poor iron
may be due to the variety of measurement methods and status due to foot-strike hemolysis and typically low
challenges in accurately measuring the many components of consumption of heme containing foods (3). Female distance
EA (37, 38). One component of EA fraught with error is runners are especially prone to poor iron status because men-
assessment of energy intake, which often relies on self- strual blood loss, greater gastrointestinal losses of the mineral,
report. We measured calorie intake with a validated and and elevated hepcidin after exercise (68). Therefore, iron
reliable FFQ developed to assess routine consumption (42, needs for female athletes may be 70% more than estimated
43), however no measure of dietary intake is without error. average requirement for iron (69). The athletes in this study
Our measurement of EA is strengthened by use of DXA, the seemed to be well informed about the importance of iron
recommended method (37) of body composition assessment intake in running performance because more than half were
due to its low standard error of estimate, however some taking dietary supplements of this mineral. A recent review of
research reports DXA to be less reliable in accurately iron supplementation among marathon runners concluded
measuring fat mass of very lean athletes (41). We report that supplementation of the trace mineral should be used to
6.3–7.3% lower EA when using FFM in the calculation correct low ferritin concentrations in athletes, may be used
versus BFLM because when measured via DXA use of FFM to prevent iron deficiency, while also possibly improving
includes 2 kg of bone mass. Despite significant differences performance (68). Surprisingly, more than 37% of participants
in EA depending on use of FFM versus BFLM, the two in this study were consuming more than the upper limit
methods of calculation did not significantly alter classifica- for iron. Data collection did not inquire whether any of the
tion of athletes into categories of optimal, suboptimal, or athletes were working to treat or prevent iron deficiency. It is
clinically low EA. When considering all of the variables possible that some of these athletes were under guidance
involved with calculating EA, it is possible that differences from a health professional to take high doses of iron. Serum
in measurement of FFM versus the more precise BFLM assessment of iron status would improve this research. None
contribute a relatively small discrepancy to estimates of EA of the athletes in this study reported to be vegetarians.
compared with measurements of other components of the Most athletes were consuming adequate amounts of zinc,
EA calculation (37), however even this small change has the vitamin B12, and vitamin C. Even though male athletes were
ability to improve the accuracy of EA assessment. consuming more zinc, vitamin B12, and vitamin C than
One of most important ways for distance runners to female athletes, the average intake for both sexes was above
lower risk for bone injuries and stress fractures is to achieve the RDA. Potassium serves as an intracellular electrolyte
and maintain adequate EA, attain adequate vitamin D status, and is therefore an important nutrient for high-intensity
while also consuming sufficient levels of calcium (14, 62). endurance athletes, especially in a hot environment when
Similar to previous research (17, 22), the average calcium sweat loss of the mineral is substantial. Potassium consump-
intake for participants in this study met the RDA, however tion was below the recommended AI for 44% of the athletes
half of the female runners and 25% of male runners did not (38% of the men and 50% percent of the women). More
meet the recommended calcium intake. As reported else- information is needed on dietary potassium requirements.
where (16), male runners consumed significantly more cal- Vitamin A, an essential micronutrient for its antioxidant
cium than female counterparts. The vitamin D intake with properties and role in growth and repair, was below
this group was well below the RDA and the two athletes recommendations for 24% of athletes (3 men and 7 women).
who met the RDA or vitamin D were both taking dietary Strengths of this study include analysis of male and
supplements. One limitation of this study is that blood levels female athletes, with specific focus on a homogenous group
of vitamin D were not assessed. This group is training out- of collegiate athletes within a narrow age range. Further,
doors most of the year in Southern California where there is comparison to current dietary standards and needs
ample sunshine, which may foster in vivo synthesis of vita- established for athletes contributes valuable information to
min D. As reported elsewhere among female distance run- the literature in the field of sports nutrition. There was an
ners (63), it is possible that serum levels of vitamin D are attempt to increase accuracy of EA calculation by analyzing
adequate due to skin exposure to UVB light, even though results with BFLM and FFM. A major limitation of this
dietary intake of the micronutrient is low. Vitamin D is cru- research is the error associated with self-reported dietary
cial for optimal skeletal health, but is also particularly intake. Self-reported data may convey lower than actual
important for athletes due to its role in muscular function caloric intake, which would directly influence the macro-
(64), injury prevention (65), reduced inflammation, and a and micronutrient intake. Research in sports nutrition of
strong immune system (66). Previous research shows that collegiate distance runners could be improved by examining
low vitamin D status may affect strength and power in col- timing of nutrient intake throughout the day and in relation
lege athletes (67). It is also important to note that athletes to intensity of training and length of workouts. Further
with low EA and/or menstrual dysfunction may need up to improvements in this work, would assess whether athletes
JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION 7

were trying to, or needed to, make changes in dietary intake 6. Parnell JA, Wiens KP, Erdman KA. Dietary intakes and supple-
to alter body composition and thereby improve performance. ment use in pre-adolescent and adolescent canadian athletes.
Nutrients. 2016;8(9):526. doi:10.3390/nu8090526.
7. Heikura IA, Burke LM, Mero AA, Uusitalo ALT, Stellingwerff T.
Dietary microperiodization in elite female and male runners and
Conclusions
race walkers during a block of high intensity precompetition
In this group of collegiate distance runners, it appears that training. Int J Sport Nutr Exerc Metab. 2017;27(4):297–304. doi:
10.1123/ijsnem.2016-0317.
most athletes have low energy availability. Additionally,
8. Masson G, Lamarche B. Many non-elite multisport endurance
there is need for further education among athletes because athletes do not meet sports nutrition recommendations for car-
carbohydrate intake was insufficient for optimal perform- bohydrates. Appl Physiol Nutr Metab. 2016;41(7):728–734. doi:
ance. Measurement of EA decreases significantly when FFM 10.1139/apnm-2015-0599.
is used in the equation versus BFLM. To improve the accur- 9. Burkhart SJ, Pelly FE. Dietary intake of athletes seeking nutrition
advice at a major international competition. Nutrients. 2016;
acy of EA assessment, we propose for future research to use 8(10):638. doi:10.3390/nu8100638.
DXA to measure BFLM and express EA kcals available per 10. Sugiura K, Suzuki I, Kobayashi K. Nutritional intake of elite
kg of BFLM, as bone tissue is less metabolically active dur- Japanese track-and-field athletes. Int J Sport Nutr. 1999;9(2):
ing exercise than muscle tissue. In general, dietary intake 202–212. doi:10.1123/ijsn.9.2.202.
could be improved by reducing the proportion of energy 11. Ludbrook C, Clark D. Energy expenditure and nutrient intake in
long-distance runners. Nutr Res. 1992;12(6):689–699. doi:10.
derived from fat, especially working to lower consumption 1016/S0271-5317(05)80566-4.
of saturated fatty acids, while replacing these kcals with 12. Onywera VO, Kiplamai FK, Tuitoek PJ, Boit MK, Pitsiladis YP.
nutrient-dense complex carbohydrates. Increased consump- Food and macronutrient intake of elite Kenyan distance runners.
tion of calcium, vitamin D, and potassium are also needed, Int J Sport Nutr Exerc Metab. 2004;14(6):709–719. doi:10.1123/
however protein and iron intake were mostly adequate in ijsnem.14.6.709.
13. Guest NS, Barr SI. Cognitive dietary restraint is associated with
this population of collegiate distance runners. stress fractures in women runners. Int J Sport Nutr Exerc Metab.
2005;15(2):147–159. doi:10.1123/ijsnem.15.2.147.
14. Nieves JW, Melsop K, Curtis M, Kelsey JL, Bachrach LK,
Acknowledgements Greendale G, Sowers MF, Sainani KL. Nutritional factors that
We are grateful to Coaches Scott Guerrero, Jason Zarb-Cousin, and influence change in bone density and stress fracture risk among
Caitlin Jennings, and all of the research participants who volunteered young female cross-country runners. PM R. 2010;2(8):740–750.
for and supported this research investigation. Thank you to Makenzie doi:10.1016/j.pmrj.2010.04.020.
Cook, Lily Bramble, and Rowena Feng for their assistance with data 15. Wentz L, Liu PY, Ilich JZ, Haymes EM. Dietary and training
analysis and management. predictors of stress fractures in female runners. Int J Sport Nutr
Exerc Metab. 2012;22(5):374–382. doi:10.1123/ijsnem.22.5.374.
16. Leachman Slawson D, McClanahan BS, Clemens LH, Ward KD,
Klesges RC, Vukadinovich CM, Cantler ED. Food sources of cal-
Funding cium in a sample of African-American an Euro-American colle-
This research was supported by the Loyola Marymount University giate athletes. Int J Sport Nutr Exerc Metab. 2001;11(2):199–208.
Rains Research Assistant Program. doi:10.1123/ijsnem.11.2.199.
17. Hinton PS, Sanford TC, Davidson MM, Yakushko OF, Beck NC.
Nutrient intakes and dietary behaviors of male and female colle-
ORCID giate athletes. Int J Sport Nutr Exerc Metab. 2004;14(4):389–405.
doi:10.1123/ijsnem.14.4.389.
William P. McCormack http://orcid.org/0000-0002-8634-2305 18. Gropper SS, Blessing D, Dunham K, Barksdale JM. Iron status of
female collegiate athletes involved in different sports. Biol Trace
Elem Res. 2006;109(1):1–14. doi:10.1385/BTER:109:1:001.
References 19. Shriver LH, Betts NM, Wollenberg G. Dietary intakes and eating
habits of college athletes: Are female college athletes following
1. Costill DL, Sherman WM, Fink WJ, Maresh C, Witten M, Miller the current sports nutrition standards? J Am Coll Health. 2013;
JM. The role of dietary carbohydrates in muscle glycogen resyn- 61(1):10–16. doi:10.1080/07448481.2012.747526.
thesis after strenuous running. Am J Clin Nutr. 1981;34(9): 20. Niekamp RA, Baer JT. In-season dietary adequacy of trained
1831–1836. doi:10.1093/ajcn/34.9.1831. male cross-country runners. Int J Sport Nutr. 1995;5(1):45–55.
2. Lemon PW. Is increased dietary protein necessary or beneficial doi:10.1123/ijsn.5.1.45.
for individuals with a physically active lifestyle? Nutr Rev. 2009; 21. Tanaka JA, Tanaka H, Landis W. An assessment of carbohydrate
54(4):S169–S175. doi:10.1111/j.1753-4887.1996.tb03913.x. intake in collegiate distance runners. Int J Sport Nutr. 1995;5(3):
3. Thomas DT, Erdman KA, Burke LM. Position of the academy of 206–214. doi:10.1123/ijsn.5.3.206.
nutrition and dietetics, dietitians of canada, and the american col- 22. Giffin KL, Knight KB, Bass MA, Valliant MW. Predisposing
lege of sports medicine: Nutrition and athletic performance. J Acad risk factors and stress fractures in division I cross country
Nutr Diet. 2016;116(3):501–528. doi:10.1016/j.jand.2015.12.006. runners. J Strength Cond Res. 2017;117(9):31. doi:10.1519/JSC.
4. Castell LM, Nieman DC, Bermon S, Peeling P. Exercise-induced 0000000000002408.
illness and inflammation: Can immunonutrition and iron help? 23. Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini
Int J Sport Nutr Exerc Metab. 2019;29(2):181–188. doi:10.1123/ N, Lebrun C, Meyer N, Sherman R, Steffen K, Budgett R, et al.
ijsnem.2018-0288. The IOC consensus statement: Beyond the female athlete triad-
5. Burke LM, Castell LM, Casa DJ, Close GL, Costa RJS, Desbrow Relative Energy Deficiency in Sport (RED-S). Br J Sports Med.
B, Halson SL, Lis DM, Melin AK, Peeling P, et al. International 2014;48(7):491–497. doi:10.1136/bjsports-2014-093502.
association of athletics federations consensus statement 2019: 24. Nattiv A, American College of Sports MedicineAmerican college
Nutrition for athletics. Int J Sport Nutr Exerc Metab. 2019;29(2): of sports medicine position stand. The female athlete triad. Med
73–84. doi:10.1123/ijsnem.2019-0065. Sci Sports Exerc. 2007;39(10):1867–1882., Loucks AB, Manore
8 B. L. BEERMANN ET AL.

MM, Sanborn CF, Sundgot-Borgen J, Warren MP. doi:10.1249/ behalf of the ad hoc research working group on body compos-
mss.0b013e318149f111. ition health and performance, under the auspices of the I.O.C.
25. Mountjoy M, Sundgot-Borgen J, Burke L, Ackerman KE, Medical commission. Sports Med. 2012;42(3):227–249. doi:10.
Blauwet C, Constantini N, Lebrun C, Lundy B, Melin A, Meyer 2165/11597140-000000000-00000.
N, et al. International olympic committee (IOC) consensus state- 42. Block G, Woods M, Potosky A, Clifford C. Validation of a self-
ment on Relative Energy Deficiency in Sport (RED-S): 2018 administered diet history questionnaire using multiple diet
update. Int J Sport Nutr Exerc Metab. 2018;28(4):316–331. doi: records. J Clin Epidemiol. 1990;43(12):1327–1335. doi:10.1016/
10.1123/ijsnem.2018-0136. 0895-4356(90)90099-B.
26. Tenforde AS, Nattiv A, Ackerman K, Barrack MT, Fredericson M. 43. Block G, Subar AF. Estimates of nutrient intake from a food fre-
Optimising bone health in the young male athlete. Br J Sports quency questionnaire: The 1987 national health interview survey.
Med. 2017;51(3):148–149. doi:10.1136/bjsports-2016-097000. J Am Diet Assoc. 1992;92(8):969–977.
27. McCormack WP, Shoepe TC, LaBrie J, Almstedt HC. Bone min- 44. Block G, Thompson FE, Hartman AM, Larkin FA, Guire KE.
eral density, energy availability, and dietary restraint in collegiate Comparison of two dietary questionnaires validated against mul-
cross-country runners and non-running controls. Eur J Appl tiple dietary records collected during a 1-year period. J Am Diet
Physiol. 2019;119(8):1–10. doi:10.1007/s00421-019-04164-z. Assoc. 1992;92(6):686–693.
28. Loucks AB. Low energy availability in the marathon and other 45. U.S. Department of Health, Human Services and U.S.
endurance sports. Sports Med. 2007;37(4):348–352. doi:10.2165/ Department of Agriculture. 2015–2020 dietary guidelines for
00007256-200737040-00019. Americans. In 2015–2020 dietary guidelines for Americans; 2015.
29. Sygo J, Coates AM, Sesbreno E, Mountjoy ML, Burr JF. 46. Institute of medicine, Food and Nutrition Board. Dietary refer-
Prevalence of indicators of low energy availability in elite female ence intakes: Energy, carbohydrate, fiber, fat, fatty acids, choles-
sprinters. Int J Sport Nutr Exerc Metab. 2018;28(5):490–496. doi: terol, protein and amino acids. In: Institute of medicine, food
10.1123/ijsnem.2017-0397. and nutrition board, dietary reference intakes: Energy, carbohy-
30. Loucks AB, Stachenfeld NS, DiPietro L. The female athlete triad: drate, fiber, fat, fatty acids, cholesterol, protein and amino acids.
Do female athletes need to take special care to avoid low energy Washington: The National Academy; 2005.
availability? Med Sci Sports Exerc. 2006;38(10):1694–1700. doi: 47. Institute of Medicine, Food and Nutrition Board. Dietary refer-
10.1249/01.mss.0000239397.01203.83. ence intakes for calcium, phosphorus, magnesium, vitamin D,
31. Melin A, Tornberg AB, Skouby S, Moller SS, Sundgot-Borgen J, and fluoride. In: Dietary reference intakes for calcium, phos-
Faber J, Sidelmann JJ, Aziz M, Sjodin A. Energy availability and phorus, magnesium, vitamin D, and fluoride. Washington D.C.:
the female athlete triad in elite endurance athletes. Scand J Med National Academy Press; 1997.
Sci Sports. 2015;25(5):610–622. doi:10.1111/sms.12261. 48. Institute of Medicine Standing Committee. Scientific evaluation of
32. Fahrenholtz IL, Sjodin A, Benardot D, Tornberg AB, Skouby S, dietary reference intakes. In Dietary reference intakes for thiamin,
Faber J, Sundgot-Borgen JK, Melin AK. Within-day energy deficiency riboflavin, niacin, vitamin B6, folate, vitamin B12, pantothenic
and reproductive function in female endurance athletes. Scand J Med acid, biotin, and choline. USA: National Academies Press; 1998.
Sci Sports. 2018;28(3):1139–1146. doi:10.1111/sms.13030. 49. Food, Nutrition Board Institute of Medicine. Dietary reference
33. Viner RT, Harris M, Berning JR, Meyer NL. Energy availability intakes for vitamin A, vitamin K, arsenic, boron, chromium, copper,
and dietary patterns of adult male and female competitive iodine, iron, manganese, molybdenum, nickel, silicon, vanadium,
cyclists with lower than expected bone mineral density. Int J and zinc. Washington D.C.: National Academy of Medicine; 2001.
Sport Nutr Exerc Metab. 2015;25(6):594–602. doi:10.1123/ijsnem. 50. Stallings VA, Harrison M, Oria M. Dietary reference intakes for
2015-0073. sodium and potassium. USA: National Academies Press; 2019.
34. Woodruff SJ, Meloche RD. Energy availability of female varsity 51. Monsen ER. Dietary reference intakes for the antioxidant
volleyball players. Int J Sport Nutr Exerc Metab. 2013;23(1): nutrients: Vitamin C, vitamin E, selenium, and carotenoids. J
24–30. doi:10.1123/ijsnem.23.1.24. Acad Nutr Diet. 2000;100(6):637.
35. Torstveit MK, Fahrenholtz I, Stenqvist TB, Sylta O, Melin A. 52. Ainsworth BE, Haskell WL, Herrmann SD, Meckes N, Bassett
Within-day energy deficiency and metabolic perturbation in DR, Jr., Tudor-Locke C, Greer JL, Vezina J, Whitt-Glover MC,
male endurance athletes. Int J Sport Nutr Exerc Metab. 2018; Leon AS. 2011 compendium of physical activities: A second
28(4):419–427. doi:10.1123/ijsnem.2017-0337. update of codes and met values. Med Sci Sports Exerc. 2011;
36. Koehler K, Hoerner NR, Gibbs JC, Zinner C, Braun H, De 43(8):1575–1581. doi:10.1249/MSS.0b013e31821ece12.
Souza MJ, Schaenzer W. Low energy availability in exercising 53. Guebels CP, Kam LC, Maddalozzo GF, Manore MM. Active
men is associated with reduced leptin and insulin but not with women before/after an intervention designed to restore men-
changes in other metabolic hormones. J Sports Sci. 2016;34(20): strual function: Resting metabolic rate and comparison of four
1921–1929. doi:10.1080/02640414.2016.1142109. methods to quantify energy expenditure and energy availability.
37. Burke LM, Lundy B, Fahrenholtz IL, Melin AK. Pitfalls of con- Int J Sport Nutr Exerc Metab. 2014;24(1):37–46. doi:10.1123/ijs-
ducting and interpreting estimates of energy availability in free- nem.2012-0165.
living athletes. Int J Sport Nutr Exerc Metab. 2018;28(4): 54. Cunningham JJ. Body composition as a determinant of energy
350–363. doi:10.1123/ijsnem.2018-0142. expenditure: A synthetic review and a proposed general predic-
38. Heikura IA, Uusitalo ALT, Stellingwerff T, Bergland D, Mero tion equation. Am J Clin Nutr. 1991;54(6):963–969. doi:10.1093/
AA, Burke LM. Low energy availability is difficult to assess but ajcn/54.6.963.
outcomes have large impact on bone injury rates in elite distance 55. De Souza MJ, Nattiv A, Joy E, Misra M, Williams NI, Mallinson RJ,
athletes. Int J Sport Nutr Exerc Metab. 2018;28(4):403–411. doi: Gibbs JC, Olmsted M, Goolsby M, Matheson G. 2014 female athlete
10.1123/ijsnem.2017-0313. triad coalition consensus statement on treatment and return to play
39. Ihle R, Loucks AB. Dose-response relationships between energy of the female athlete triad: 1st international conference held in San
availability and bone turnover in young exercising women. J Bone Francisco, California, may 2012 and 2nd international conference
Miner Res. 2004;19(8):1231–1240. doi:10.1359/JBMR.040410. held in Indianapolis, Indiana, may 2013. Br J Sports Med. 2014;
40. Loucks AB, Thuma JR. Luteinizing hormone pulsatility is dis- 48(4):289–289. doi:10.1097/JSM.0000000000000085.
rupted at a threshold of energy availability in regularly menstru- 56. Williamson E, Kato H, Volterman KA, Suzuki K, Moore DR.
ating women. J Clin Endocrinol Metab. 2003;88(1):297–311. doi: The dffect of dietary protein on protein metabolism and per-
10.1210/jc.2002-020369. formance in endurance-trained males. Med Sci Sports Exerc.
41. Ackland TR, Lohman TG, Sundgot-Borgen J, Maughan RJ, 2019;51(2):352–360. doi:10.1249/MSS.0000000000001791.
Meyer NL, Stewart AD, Muller W. Current status of body com- 57. Koehler K, Achtzehn S, Braun H, Mester J, Schaenzer W.
position assessment in sport: Review and position statement on Comparison of self-reported energy availability and metabolic
JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION 9

hormones to assess adequacy of dietary energy intake in young 63. Wentz LM, Liu PY, Ilich JZ, Haymes EM. Female distance run-
elite athletes. Appl Physiol Nutr Metab. 2013;38(7):725–733. doi: ners training in southeastern United States have adequate vita-
10.1139/apnm-2012-0373. min d status. Int J Sport Nutr Exerc Metab. 2016;26(5):397–403.
58. Day J, Wengreen H, Heath E, Brown K. Prevalence of low doi:10.1123/ijsnem.2014-0177.
energy availability in collegiate female runners and implementa- 64. Cannell JJ, Hollis BW, Sorenson MB, Taft TN, Anderson JJ.
tion of nutrition education intervention. Sports Nutr Ther. 2015; Athletic performance and vitamin D. Med Sci Sports Exerc.
1(1):1–7. doi:10.4172/2473-6449.1000101. 2009;41(5):1102–1110. doi:10.1249/MSS.0b013e3181930c2b.
59. Burke LM, Close GL, Lundy B, Mooses M, Morton JP, Tenforde 65. Ruohola JP, Laaksi I, Ylikomi T, Haataja R, Mattila VM, Sahi T,
AS. Relative energy deficiency in sport in male athletes: A com- Tuohimaa P, Pihlajamaki H. Association between serum 25(oh)d
mentary on its presentation among selected groups of male ath- concentrations and bone stress fractures in Finnish young men. J
letes. Int J Sport Nutr Exerc Metab. 2018;28(4):364–374. doi:10. Bone Miner Res. 2006;21(9):1483–1488. doi:10.1359/jbmr.060607.
66. Halliday TM, Peterson NJ, Thomas JJ, Kleppinger K, Hollis BW,
1123/ijsnem.2018-0182.
Larson-Meyer DE. Vitamin D status relative to diet, lifestyle,
60. Ackerman KE, Holtzman B, Cooper KM, Flynn EF, Bruinvels G,
injury, and illness in college athletes. Med Sci Sports Exerc.
Tenforde AS, Popp KL, Simpkin AJ, Parziale AL. Low energy
2011;43(2):335–343. doi:10.1249/MSS.0b013e3181eb9d4d.
availability surrogates correlate with health and performance
67. Hildebrand RA, Miller B, Warren A, Hildebrand D, Smith BJ.
consequences of relative energy deficiency in sport. Br J Sports Compromised vitamin D status negatively affects muscular
Med. 2019;53(10):628–633. doi:10.1136/bjsports-2017-098958. strength and power of collegiate athletes. Int J Sport Nutr Exerc
61. Elliott-Sale KJ, Tenforde AS, Parziale AL, Holtzman B, Metab. 2016;26(6):558–564. doi:10.1123/ijsnem.2016-0052.
Ackerman KE. Endocrine effects of relative energy deficiency in 68. Zourdos MC, Sanchez-Gonzalez MA, Mahoney SE. A brief
sport. Int J Sport Nutr Exerc Metab. 2018;28(4):335–349. doi:10. review: The implications of iron supplementation for marathon
1123/ijsnem.2018-0127. runners on health and performance. J Strength Cond Res. 2015;
62. Close GL, Sale C, Baar K, Bermon S. Nutrition for the preven- 29(2):559–565. doi:10.1519/JSC.0000000000000636.
tion and treatment of injuries in track and field athletes. Int J 69. DellaValle DM. Iron supplementation for female athletes: Effects
Sport Nutr Exerc Metab. 2019;29(2):189–197. doi:10.1123/ijsnem. on iron status and performance outcomes. Curr Sports Med Rep.
2018-0290. 2013;12(4):234–239. doi:10.1249/JSR.0b013e31829a6f6b.

You might also like