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This review updates and complements the review of energy balance and body composition in the Proceedings of the 2003 IOC Consensus Conference on Sports Nutrition. It argues that the concept of energy availability is more useful than the concept of energy balance for managing the diets of athletes. It then summarizes recent reports of the existence, aetiologies, and clinical consequences of low energy availability in athletes. This is followed by a review of recent research on the failure of appetite to increase ad libitum energy intake in compensation for exercise energy expenditure. The review closes by summarizing the implications of this research for managing the diets of athletes.
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Energy availability in athletes
Anne B. Loucks a , Bente Kiens b & Hattie H. Wright c
a Department of Biological Sciences, Ohio University, Athens, Ohio, USA
b The Molecular Physiology Group, Department of Exercise and Sport Sciences, University of
Copenhagen, Copenhagen, Denmark
c Center of Excellence for Nutrition, Faculty of Health Sciences, North-West University,
Potchefstroom, South Africa
Available online: 28 Jul 2011
To cite this article: Anne B. Loucks, Bente Kiens & Hattie H. Wright (2011): Energy availability in athletes, Journal of Sports
Sciences, 29:sup1, S7-S15
To link to this article: http://dx.doi.org/10.1080/02640414.2011.588958
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Energy availability in athletes
ANNE B. LOUCKS
1
, BENTE KIENS
2
, & HATTIE H. WRIGHT
3
1
Department of Biological Sciences, Ohio University, Athens, Ohio, USA,
2
The Molecular Physiology Group, Department of
Exercise and Sport Sciences, University of Copenhagen, Copenhagen, Denmark, and
3
Center of Excellence for Nutrition,
Faculty of Health Sciences, North-West University, Potchefstroom, South Africa
(Accepted 13 May 2011)
Abstract
This review updates and complements the review of energy balance and body composition in the Proceedings of the 2003
IOC Consensus Conference on Sports Nutrition. It argues that the concept of energy availability is more useful than the
concept of energy balance for managing the diets of athletes. It then summarizes recent reports of the existence, aetiologies,
and clinical consequences of low energy availability in athletes. This is followed by a review of recent research on the failure
of appetite to increase ad libitum energy intake in compensation for exercise energy expenditure. The review closes by
summarizing the implications of this research for managing the diets of athletes.
Keywords: Energy availability, energy balance, diet, exercise, appetite
Introduction
In the 2003 IOC Consensus Conference on Sports
Nutrition, evidence was presented that many ath-
letes, most often female athletes, were deficient in
energy, and especially energy in the form of
carbohydrates, resulting in impaired health and
performance (Loucks, 2004). It was emphasized,
however, that energy balance is not the objective of
athletic training whenever athletes seek to modify
their body size and composition to achieve perfor-
mance objectives. They then need to carefully
manage their diet and exercise regimens to avoid
compromising their health.
Distinctions between energy availability and
energy balance
In the field of bioenergetics, the concept of energy
availability recognizes that dietary energy is expended
in several fundamental physiological processes, in-
cluding cellular maintenance, thermoregulation,
growth, reproduction, immunity, and locomotion
(Wade & Jones, 2004). Energy expended in one of
these processes is not available for others. Therefore,
bioenergeticists investigate the effects of a particular
metabolic demand on physiological systems in terms
of energy availability. They define energy availability
as dietary energy intake minus the energy expended
in the particular metabolic demand of interest. In
experiments investigating effects of cold exposure, for
example, energy availability would be defined,
quantified, and controlled as dietary energy intake
minus the energy cost of thermogenesis.
Exercise training increases, and in endurance
sports may double or even quadruple, the amount
of energy expended in locomotion. In exercise
physiology, therefore, energy availability is defined
as dietary energy intake minus the energy expended
in exercise (EA ¼EI – EEE). As the amount of dietary
energy remaining after exercise training for all other
metabolic processes, energy availability is an input to
the body’s physiological systems.
In the field of dietetics, the concept of energy
balance has been the usual basis of research and
practice. Defined as dietary energy intake minus total
energy expenditure (EB ¼EI – TEE), energy balance
is the amount of dietary energy added to or lost from
the body’s energy stores after the body’s physiological
systems have done all their work for the day. Thus
energy balance is an output from those systems. For
healthy young adults, EB ¼0 kcal day
71
when
EA ¼45 kcal kg FFM
71
day
71
(where FFM ¼
fat-free mass).
Correspondence: A. B. Loucks, Department of Biological Sciences, Ohio University, Athens, OH 45701, USA. E-mail: loucks@ohio.edu
Journal of Sports Sciences, 2011; 29(S1): S7–S15
ISSN 0264-0414 print/ISSN 1466-447X online Ó2011 Taylor & Francis
http://dx.doi.org/10.1080/02640414.2011.588958
Downloaded by [ ] at 22:56 17 January 2012
The contrast between energy availability and
energy balance is illustrated in Figure 1, which shows
data collected while eight lean, untrained men lived in
a room calorimeter for a week (Stubbs et al., 2004).
During that week, their energy intake (2770 kcal
day
71
), exercise energy expenditure (840 kcal
day
71
), and energy availability (2770 840 ¼1930
kcal day
71
30 kcal kg FFM
71
day
71
)were
constant. Meanwhile, the magnitude of their negative
energy balance (2770 – 4500 ¼–1730 kcal day
71
on
Day 1) decreased towards zero at a rate of *90
kcal day
71
as various physiological processes slo-
wed down. At this rate, they would have recovered
EB ¼0 kcal day
71
(a pathological state of energy
balance achieved by suppressing physiological sys-
tems) in 3 weeks, while remaining in severely low
energy availability.
Undergraduate nutrition textbooks assert that
energy requirements can be determined by measur-
ing energy expenditure, but measures of energy
expenditure contain no information about whether
physiological systems are functioning in a healthy
manner. Because physiological processes are sup-
pressed by severely low energy availability, measure-
ments of total or resting energy expenditure will
underestimate a chronically undernourished athlete’s
energy requirements.
Therefore, because energy balance is an output
from, rather than an input to, physiological systems,
because it does not contain reliable information
about energy requirements, and because it is not
even the objective of athletic training, energy balance
is not a useful concept for managing an athlete’s
diet.
Figure 1. Negative energy balance rising at a rate of 90
kcal day
71
as metabolic processes were suppressed while the
energy intake (2770 kcal day
71
), exercise energy expenditure
(840 kcal day
71
), and energy availability (2770 840 ¼1930
kcal day
71
) of eight lean, untrained men remained constant. EI
(þ)¼energy intake, TEE (¤)¼total energy expenditure, EEE
()¼exercise energy expenditure, EA (.)¼energy availability, EB
(&)¼energy balance. Original figure based on data in Stubbs
et al. (2004).
Energy deficiency in athletes: Existence,
aetiologies, and consequences
At the 2003 IOC Consensus Conference, the
existence of widespread energy deficiency in athletes
was still questioned. Since then, the IOC Medical
Commission has published two position stands
(Sangenis et al., 2005, 2006) and the American
College of Sports Medicine (ACSM) has published a
revised position stand (Nattiv, Loucks, Manore,
Sundgot-Borgen, & Warren, 2007) on the ‘‘female
athlete triad’’. In addition, a coaches’ handbook on
Managing the Female Athlete Triad developed by
the co-chairs of the athlete interest group of the
Academy of Eating Disorders has been published by
the US National Collegiate Athletics Association
(NCAA) (Sherman & Thompson, 2005). All four
publications attribute the functional hypothalamic
menstrual disorders and low bone mineral density
found in many female athletes to energy deficiency,
but the ACSM position stand differs from the other
three in that it excludes disordered eating and eating
disorders as necessary components of the triad. The
ACSM emphasizes that athletes who expend large
amounts of energy in prolonged exercise training can
become energy deficient without eating disorders,
disordered eating or even dietary restriction.
The ACSM identified three distinct origins of
energy deficiency in athletes. The first is obsessive
eating disorders with their attendant clinical mental
illnesses. The second is intentional and rational but
mismanaged efforts to reduce body size and fatness
to qualify for and succeed in athletic competitions.
This mismanagement may or may not include
disordered eating behaviours such as fasting, diet
pills, laxatives, diuretics, enemas, and vomiting that
are entrenched parts of the culture and lore of some
sports. The third is the inadvertent failure to increase
energy intake to compensate for the energy expended
in exercise. The percentages of cases of the female
athlete triad originating from these three sources are
unknown, but ACSM emphasized that any epide-
miological study requiring the presence of an eating
disorder or disordered eating for diagnosing cases of
the triad (e.g. Schtscherbyna, Soares, de Oliveira, &
Ribeiro, 2009) will underestimate its prevalence.
Sports vary greatly in the relative importance of
various factors for competitive success. As they strive
to achieve sport-specific mixes of these factors,
athletes engage in different diet and exercise beha-
viours that impact energy availability. In endurance
sports, prolonged exercise training greatly reduces
energy availability, unless energy intake is increased
to replace the energy expended in exercise. In sports
where less energy is expended in training, dietary
restriction may be a prominent part of the strategy
for reducing energy availability to modify body size
and composition.
S8 A. B. Loucks et al.
Downloaded by [ ] at 22:56 17 January 2012
Female athletes may also under-eat for reasons
unrelated to sport. Around the world about twice as
many young women as men at every decile of body
mass index perceive themselves to be overweight
(Wardle, Haase, & Steptoe, 2006). The dispropor-
tionate numbers actively trying to lose weight are
even higher, and this disproportion increases as body
mass index declines, so that almost nine times as
many lean women as lean men are actively trying to
lose weight! Indeed, more young female athletes
report improvement of appearance than improve-
ment of performance as a reason for dieting
(Martinsen, Bratland-Sanda, Eriksson, & Sundgot-
Borgen, 2010). Thus issues unrelated to sport may
need to be addressed to persuade female athletes to
eat appropriately.
The controversy about whether female athletes can
increase glycogen stores as much as male athletes is
instructive in this regard. An experiment in which
participants consumed diets containing high and low
percentages of carbohydrates found that women
could not do so (Tarnopolsky, Atkinson, Phillips,
& MacDougall, 1995). Subsequently, it was noted
that the total energy intake (per kilogram of body
weight) of the women in that study had been so low
that the amount of carbohydrate they consumed on
the high percent carbohydrate diet was no greater
than the amount consumed by the men on the low
percent carbohydrate diet. Later research showed
that women could, indeed, load glycogen like men
when they ate as much as men (per kilogram of body
weight) (James et al., 2001; Tarnopolsky et al.,
2001).
In the 2003 IOC Consensus Conference, the
disruption of reproductive function at energy avail-
abilities 530 kcal kg FFM
71
day
71
was dis-
cussed in some detail and the low bone mineral
density (BMD) found in amenorrhoeic athletes was
represented as being mediated by oestrogen defi-
ciency (Loucks, 2004). Since then, oestrogen-
independent mechanisms by which low energy
availability can reduce BMD have also been
identified (Ihle & Loucks, 2004). As energy avail-
ability declines, the rate of bone protein synthesis
declines along with insulin, which enhances amino
acid uptake, in a linear dose–response manner. By
contrast, the rate of bone mineralization declines
abruptly as energy availability declines below 30
kcal kg FFM
71
day
71
, as do concentrations of
insulin-like growth factor-1 and tri-iodothyronine.
These effects occurred within 5 days of the onset of
energy deficiency, and without a reduction in
oestrogen concentration.
In older adults, fracture risk doubles for each
reduction of one standard deviation below mean
peak young adult BMD. In adolescents, fracture risk
can rise even as BMD increases. Because BMD
normally doubles during the decade of adolescence,
a child entering adolescence with a high BMD
relative to others of the same age can accrue bone
mineral so slowly that adulthood is entered with a
relatively low BMD. Because low BMD is an
aetiological factor in stress fractures, anything that
impairs bone mineral accrual during adolescence is
undesirable. Unfortunately, this is exactly what was
found in a study of 183 interscholastic competitive
female athletes, of whom 93 were endurance runners
and 90 were non-runners (Barrack, Rauh, & Nichols,
2010). The BMD z-scores were similar in runners
and non-runners aged 13–15 years, but were
significantly lower in runners than non-runners at
16–18 years of age.
Also questioned at the 2003 IOC Consensus
Conference was whether energy deficiency and its
clinical consequences were a problem among elite
athletes. Since then a study of 50 British national or
higher standard middle- and long-distance runners
found BMD to be lower in amenorrhoeic runners
and higher in eumenorrhoeic runners compared with
European reference data (Gibson, Mitchell, Harries,
& Reeve, 2004). The duration of eumenorrhoea was
positively associated with spine BMD, and the rate of
bone mineralization was reduced in the amenor-
rhoeic runners. Alone, the Eating Attitudes Test
(EAT) is not clinically diagnostic for eating dis-
orders, but in this study scores on the EAT classified
one of 24 amenorrhoeic runners and none of nine
oligomenorrhoeic runners as having an eating
disorder, while eight amenorrhoeic runners and
three oligomenorrhoeic runners were classified as
practising disordered eating behaviours. This left
63% of the cases of amenorrhoea and 67% of the
cases of oligomenorrhoea unaccounted for by the
EAT test (Figure 2). Similarly, a low body mass
index (518.5 kg m
72
) failed to account for 67% of
the cases of amenorrhoea and 67% of the cases of
oligomenorrhoea (Figure 3). Another study diag-
nosed low BMD (z-score less than –1) in the lumbar
spine of 34% and osteoporosis (z-score less than –2)
in the radius of 33% of 44 elite British female
endurance runners (Pollock et al., 2010). Reductions
in BMD over time were associated with training
volume. These findings led the authors to recom-
mend that all female endurance athletes undergo
dual-energy X-ray absorptiometry screening.
Ovarian function depends critically upon the
frequency with which the pituitary gland secretes
luteinizing hormone (LH) into the bloodstream, and
LH pulsatility in exercising women depends on
energy availability, rather than energy intake or
energy expenditure separately (Loucks, Verdun, &
Heath, 1998). Furthermore, exercise has no suppres-
sive effect on LH pulsatility beyond the impact of its
energy cost on energy availability (Loucks et al.,
Energy availability in athletes S9
Downloaded by [ ] at 22:56 17 January 2012
1998). Reproductive function (Loucks & Thuma,
2003) and bone formation (Ihle & Loucks, 2004) are
impaired abruptly and promptly below a threshold of
energy availability (530 kcal kg FFM
71
day
71
),
which corresponds closely to resting metabolic rate.
Figure 4 shows sleeping metabolic rate (SMR)
measured by indirect calorimetry in young adult
men (n¼20) and women (n¼17) (Westerterp,
2003). Sleeping metabolic rate is slightly less than
resting metabolic rate by the small energy expendi-
ture associated with being awake. In Figure 4,
the solid regression line relating sleeping metabolic
rate to fat-free mass (SMR [MJ day
71
]¼2.27 þ
0.091 6FFM [kg]) has a significant y-intercept.
The dashed line through the data and the origin
has a slope of 30 kcal kg FFM
71
day
71
.As
Figure 4 shows, energy availabilities 530 kcal kg
FFM
71
day
71
provide less energy than is required
for physiological systems in young adults to function
at rest.
Observational and experimental data indicate that
low energy availability also suppresses Type 1
immunity. The immune system mounts different
defences against two types of pathogens. Type 1
defences are mounted against intracellular pathogens
like viruses, while Type 2 defences are mounted
against extracellular pathogens like bacteria. Endur-
ance athletes frequently suffer upper respiratory tract
infections (URTI) caused by viruses. A survey of all
members of Swedish teams participating in the
Olympic Games of 2002 and 2004 found that those
participating in disciplines emphasizing leanness
made more frequent attempts to lose weight, trained
longer, and reported almost twice as many illnesses,
primarily URTI, during the preceding 3 months
(Hagmar, Hirschberg, Berglund, & Berglund, 2008).
The results of a recent experiment challenge the
hypothesis that Type 1 immunity in athletes might be
suppressed by exercise itself (Lancaster et al., 2005).
Participants expended 2200 kcal of energy by
exercising for 2½ h at 65% of maximal oxygen
uptake ( _
VO
2max
). Replacing just 23% of this energy
with carbohydrate reduced the suppression of Type 1
defences by an average of 65%. Thus, ingesting
sufficient energy and nutrients is vital for supporting
Figure 3. Logistic relationship between the order of menstrual
dysfunction (right ordinate scale: 0 (þ)¼eumenorrhoea; 1
(6)¼oligomenorrhoea; 2 (.)¼amenorrhoea) and body mass
index (BMI) (P50.001 for model). Left ordinate scale is a scale
of probability. The right ordinate scale shows the proportions of
participants in each category. BMI 518.5 ¼underweight. Figure
modified from Gibson et al. (2004).
Figure 4. Sleeping metabolic rate plotted as a function of fat-free
mass (FFM). .¼females; (¼males. The solid regression line
has a significant non-zero intercept. The dashed line is 30 kcal kg
FFM
71
day
71
. Figure modified from Westerterp (2003).
Figure 2. Logistic relationship between the order of menstrual
dysfunction (right ordinate scale: 0 (þ)¼eumenorrhoea; 1
(6)¼oligomenorrhoea; 2 (.)¼amenorrhoea) and total EAT
score (P¼0.014 for model). Left ordinate scale is a scale of
probability. The right ordinate scale shows the proportions of
participants in each category. DE ¼classified as disordered eating.
ED ¼classified as eating disorder. Figure modified from Gibson
et al. (2004).
S10 A. B. Loucks et al.
Downloaded by [ ] at 22:56 17 January 2012
immune function, and even more so for immune-
compromised individuals, such as those infected
with HIV (Fenton & Silverman, 2008), whose resting
energy expenditure is elevated (Mangili, Murman,
Zampini, & Wanke, 2006). Therefore, HIV-infected
athletes should take special care to reach their energy
and nutrient needs.
Seventeen years have now passed since the first
IOC Consensus Conference on Nutrition. Yet
studies of energy intake and total energy expenditure
continue to report that elite American figure skaters
(Ziegler, Nelson, Barratt-Fornell, Fiveash, & Drew-
nowski, 2001), elite Kenyan runners (Fudge et al.,
2006), and high-performance Canadian athletes in
several sports (Lun, Erdman, & Reimer, 2009) train
in substantial negative energy balance. Depending on
the level of energy availability, such negative energy
balance may either impair or benefit health and
performance. In the current review period, two
studies of elite athletes reported energy intake and
exercise energy expenditure so that their average
energy availability could be estimated. In the week
before a race, the high percent carbohydrate diet of
male Kenyan runners provided an energy availability
of 34 kcal kg FFM
71
day
71
(Onywera, Kiplamai,
Boit, & Pitsiladis, 2004). This energy availability may
or may not have been appropriate depending on their
athletic objectives at the time. If their performance in
that particular race was less important than losing
weight to improve performance in a later race, it was
fine. However, no athletic objective would appear to
justify professional male cyclists training for the Tour
de France 6 months later at an energy availability of
only 8 kcal kg FFM
71
day
71
(Vogt et al., 2005).
Such observations indicate that the diet and exercise
regimens of elite athletes range widely and are
sometimes dangerously energy deficient.
Effects of prolonged exercise on hunger and
energy intake
Eating disorders may be intractable, and weight and
fat loss programmes may be challenging to manage
effectively and safely, but these two origins of low
energy availability in athletes are at least familiar to
sports dietitians. The third origin, the suppression
of appetite by prolonged exercise, appears to be
less familiar. Neglect of appetite as an important
factor in sports nutrition is indicated by the
appearance of the word ‘‘appetite’’ only once
(and then only in a discussion of fluid losses at
high altitude) in the recently revised position stand
on nutrition and athletic performance jointly
adopted by the American Dietetic Association,
the Dietitians of Canada, and the American
College of Sports Medicine (Rodriguez, DiMarco,
& Langley, 2009).
Some of the then available evidence that appetite is
not a reliable indicator of energy needs in athletes
was reviewed at the 2003 IOC Consensus Con-
ference (Loucks, 2004). Shortly afterwards, the
suppressive effect of prolonged exercise on ad libitum
energy intake was clearly demonstrated by the
experiment in which eight lean, untrained men
expended *840 kcal day
71
by cycle ergometry as
they lived in a room calorimeter for 7 days (Stubbs
et al., 2004). During that week, their ad libitum
energy intake was similar to another week in the
room calorimeter when they did not exercise. This
inadvertent failure to increase energy intake in
compensation for exercise energy expenditure re-
duced their ad libitum energy availability by *10
kcal kg FFM
71
day
71
.
The participants in that experiment actually
performed the experiment four times, with and
without exercise while consuming equally palatable
62% and 37% carbohydrate diets in a 2 62 cross-
over design. Compared with weeks when the
participants ate the 37% carbohydrate diet, their ad
libitum energy intake declined by *1000 kcal -
day
71
on the 62% carbohydrate diet, reducing their
ad libitum energy availability by *16 kcal kg
FFM
71
day
71
. Moreover, the suppressive effects
of prolonged exercise and the high percent carbohy-
drate diet were additive. Ad libitum energy avail-
ability declined from *47 kcal kg FFM
71
day
71
when the participants were sedentary on the 37%
carbohydrate diet to *21 kcal kg FFM
71
day
71
when they exercised on the 62% carbohydrate diet
(Figure 5).
These findings in lean, untrained men exercising
in a laboratory confirmed a previous report of a high
Figure 5. The ad libitum energy intake, energy balance, and energy
availability of eight lean men living in a laboratory for 7 days
during an experiment contrasting two diets (50% fat, 32%
carbohydrate [CHO]; and 25% fat, 67% CHO) and two levels
of exercise (840 and 0 kcal day
71
) (data from Stubbs et al.,
2004). Energy availability was estimated assuming 16% body fat.
Appetite failed to match energy intake to activity-induced energy
expenditure on either diet. Appetite also failed to drive energy
intake on a low fat, high carbohydrate diet to match energy
expenditure at either activity level. These effects were additive.
Reproduced from Loucks (2007) with permission from Adis, a
Wolters Kluwer business (ÓAdis Data Information BV 2007. All
rights reserved).
Energy availability in athletes S11
Downloaded by [ ] at 22:56 17 January 2012
percent carbohydrate diet suppressing ad libitum
energy intake in 12 male and 13 female trained
runners living at home (Horvath, Eagen, Fisher,
Leddy, & Pendergast, 2000a; Horvath, Eagen, Ryer-
Calvin, & Pendergast, 2000b). These runners ran 42
miles a week, expending *600 kcal day
71
for 31
days. They repeated this regimen three times while
consuming equally palatable diets containing 42%,
55%, and 67% carbohydrate. As the percent
carbohydrate content of the diet decreased, ad
libitum energy availability increased from 27 to 34
and 39 kcal kg FFM
71
day
71
in the women and
similarly from 27 to 37 and 42 kcal kg
FFM
71
day
71
in the men. Endurance time at
80% _
VO
2max
on a treadmill improved by 18% as the
percent carbohydrate content of the diet was reduced
from 67% to 55%. Interestingly, this reduction in
percent carbohydrate content did not reduce the
amount of carbohydrate consumed, because of the
associated increase in ad libitum energy intake. The
differences in ad libitum energy intake on the three
diets had no effects on body weight or body fat
(Figure 6). The mechanism by which a high percent
carbohydrate diet suppresses appetite has yet to be
investigated, but plausible factors include the greater
bulk and fibre content (Mann et al., 2007) of
carbohydrate-rich foods.
Recently, an even longer experiment simulating
the microgravity in space confirmed the suppression
of ad libitum energy intake by prolonged exercise
(Bergouignan et al., 2010). In this experiment, eight
healthy, lean, untrained women exercised in the
prone position for 50 min at 40–80% _
VO
2max
on
alternate days during 60 days of bed rest while eight
others did not exercise. Ad libitum energy balance
was 0.7 MJ day
71
lower in the women who
exercised than in those who did not. Again, there
were no differences in body weight between the two
groups at any time during the 60-day study.
Evidence about the influence of gender on the
suppression of ad libitum energy intake by prolonged
exercise is conflicting. Some researchers have found
the suppression in women to be greater (Staten,
1991) and others smaller (Stubbs et al., 2002a,
2002b) than that in men.
Investigators of the mechanisms that mediate the
suppression of ad libitum energy intake by exercise
recognize that appetite is comprised of two drives.
Hunger, which urges us to begin eating, is stimulated
by the orexigenic hormone ghrelin, whereas satiety,
which leads us to stop eating, is stimulated by several
anorexigenic hormones including peptide YY (PYY),
glucagon-like peptide 1 (GLP-1), and pancreatic
polypeptide (PP). Compared with placebo infusions,
peripheral infusions of ghrelin and PYY at physiolo-
gical concentrations alter food intake, with ghrelin
increasing food intake at a single meal and cumula-
tively over 24 h by 28% (Wren et al., 2001) while
PYY reduces it by 30% (Batterham et al., 2003).
A common experimental protocol for investigating
these mechanisms has been to administer a standard
dinner and breakfast followed by either a prolonged
exercise bout or rest and then an ad libitum buffet
lunch. One such study administered 60 min of
exercise at 66% of maximum heart rate (Martins,
Morgan, Bloom, & Robertson, 2007). The *300
kcal of exercise energy expenditure was followed by
an increase of only *150 kcal in ad libitum energy
intake. At lunchtime, hunger scores and concentra-
tions of ghrelin were no higher after exercise than
after rest, but PP was significantly increased after
exercise.
Similar results have been found in one-day
experiments on lean, untrained young men who
performed 30 min of exercise at 50% and 75% of
_
VO
2max
(Ueda, Yoshikawa, Katsura, Usui, & Fuji-
moto, 2009), 90 min of exercise at 68% of _
VO
2max
(King, Miyashita, Wasse, & Stensel, 2010), and a
450-kcal bout of resistance exercise (Ballard et al.,
2009), and on healthy post-menopausal women who
performed 2 h of exercise at 46% of _
VO
2max
(Borer,
Figure 6. The ad libitum energy intake (kcal kg
FFM
71
day,
71
), energy availability (kcalkg FFM
71
day
71
),
carbohydrate (CHO) intake (g kg body weight
7
1day
71
), 80%
maximal oxygen uptake endurance time, body weight and percent
body fat of 12 female (W) and 13 male (M) endurance-trained
runners living at home for 31 days during an experiment
contrasting three diets (17% fat, 67% CHO; 31% fat, 55%
CHO; and 44% fat, 43% CHO) (data from Horvath et al., 2000a,
2000b). Arrows indicate statistically significant differences. In-
creasing dietary fat from 17% to 31% (reducing dietary CHO from
67% to 55%) increased ad libitum energy intake enough to preserve
carbohydrate intake and increased endurance performance by 18%
without affecting body weight or body fat. Reproduced from
Loucks (2007) with permission from Adis, a Wolters Kluwer
business (ÓAdis Data Information BV 2007. All rights reserved).
S12 A. B. Loucks et al.
Downloaded by [ ] at 22:56 17 January 2012
2010), as well as on male and female endurance
trained runners who ran for 90 min at *60% of
_
VO
2max
before a 10-km time-trial as fast as possible
on a treadmill after 2 days of carbohydrate loading
and a standardized 70% carbohydrate breakfast
(Russel, Willis, Ravussin, & Larson-Meyer, 2009).
Other experiments have investigated individual
differences in the effects of exercise training on ad
libitum energy intake over a period of 12 weeks
(King, Hopkins, Caudwell, Stubbs, & Blundell,
2008; King et al., 2009). These experiments on
overweight and obese men and women confirmed
the exercise-induced suppression of ad libitum energy
intake mediated by suppressed hunger and increased
satiety that had been found in shorter term experi-
ments, but they also revealed a high degree of
individual variability in weight and fat loss. When
participants were retrospectively classified as com-
pensators or non-compensators based on actual
weight loss compared with the weight loss expected
from exercise energy expenditure, ad libitum energy
intake was found to have increased in the compen-
sators and decreased in the non-compensators (King
et al., 2008). Exercise induced a similar increase in
satiety in both groups, which was even greater after
12 weeks of training than before, but compensators
became progressively hungrier during the experi-
ment (King et al., 2009).
Thus, findings in both trained and untrained
male and female participants consistently demon-
strate that a single bout of diverse forms of exercise
acutely suppresses ad libitum energy intake and that
exercise training chronically maintains the resulting
energy deficiency for many weeks. This effect has
been interpreted to be at least partially responsible
for exercise-induced anorexia (Russel et al., 2009).
Whether some female athletes become hungrier
and increase ad libitum energy intake as their
training progresses, and thereby avoid developing
functional hypothalamic amenorrhoea (like over-
weight participants who do not lose weight on an
exercise training programme), has yet to be
investigated.
Implications for managing the diets of athletes
The studies of ad libitum energy intake cited above
demonstrate that appetite is an unreliable indicator
of energy requirements for athletes engaged in
prolonged exercise training, just as thirst is an
unreliable indicator of water requirements during a
marathon race. Marathon runners are advised not to
wait until they are thirsty before they begin drinking
during a race. Similarly, athletes who engage in
prolonged exercise training should be advised to eat
by discipline, that is, to eat specific amounts of
particular foods at planned times, instead of waiting
until they are hungry and then eating only until they
are satisfied.
The recommendation for athletes in endurance
sports to consume a diet containing a high percen-
tage of carbohydrates should also be reconsidered.
The original evidentiary basis for this recommenda-
tion was the finding that high carbohydrate intake for
a few days before a high-intensity endurance event
increased glycogen storage and improved perfor-
mance (Costill, 1988). It may be reasonable to
expect endurance athletes to override their appetites
to consume a high volume of a high percent
carbohydrate diet for glycogen loading for a day or
two as a pre-race tactic, but it may not be realistic to
expect them to override the appetite-suppressive
effects of both a high percent carbohydrate diet and
prolonged exercise as a lifestyle. Meanwhile, research
is needed to determine whether the suppression of ad
libitum energy intake by a high percent carbohydrate
diet can be ameliorated by increasing the proportion
of refined carbohydrate in the diet (Mann et al.,
2007).
The American Academy of Pediatrics (AAP,
2005), the IOC Medical Commission (Sangenis
et al., 2005), and ACSM (Nattiv et al., 2007) have
all recommended that national and international
governing bodies of sports and athletic organizations
put policies and procedures in place to eliminate
potentially harmful weight loss practices of female
athletes. Procedures and policies were not specified,
because best practices may be sport-specific. These
recommendations followed the establishment of such
policies and procedures by the governing bodies of
US men’s collegiate wrestling in the late 1990s
(Oppliger, Utter, Scott, Dick, & Klossner, 2006) and
men’s international ski jumping in 2004 (FIS, 2004).
The procedures specified by NCAA Wrestling Rule
3 are expensive, intrusive for the athlete, labour-
intensive for athletic trainers, and bureaucratic with
local and national databases, but they seem to have
been effective in reducing unhealthy weight loss
behaviours and promoting competitive equity (Op-
pliger et al., 2006). Based on this success, a call has
gone out for the International Judo Federation (IJF)
to implement regulations to improve weight manage-
ment behaviours among judo competitors, and for
these regulations to be adopted by all National and
Regional Federations (Artioli et al., 2010a).
By contrast, the International Ski Federation (FIS)
employed a very different strategy for preventing
excessive weight loss practices in ski jumpers (FIS,
2004). Instead of policing athlete behaviour, the FIS
removed the motivation for ski jumpers to pursue
excessive weight loss objectives. Ski jumpers have
their height and weight measured at the top of the hill
immediately before their jump, whereupon they are
simply issued skis that are shorter or longer in
Energy availability in athletes S13
Downloaded by [ ] at 22:56 17 January 2012
proportion to their body mass index. Shorter skis
reduce aerodynamic lift to compensate for the
advantage a lighter jumper would otherwise gain,
so that a jumper’s success depends on their skill
rather than their body weight. Adoption of this new
rule reduced the percentage of underweight ski
jumpers in the next World Cup competition from
23% to 8% (Muller, Groschl, Muller, & Sudi, 2006).
Replacing body mass index with mass index (MI ¼
body mass divided by the square of sitting height) has
been proposed to further improve the rule (Muller,
2009).
Periodization of training may require a period-
ization of energy availability to achieve training
objectives. Experimental evidence indicates that
athletes should follow diet and exercise regimens
that provide energy availabilities of 30–45 kcal kg
FFM
71
day
71
while training to reduce body size or
fatness. However, if athletes in other sports are like
judo competitors, personal counselling of athletes by
sports dietitians may not be the most effective way to
moderate athlete behaviour to prevent excessive
energy deficiency. Among seven different types of
advisors for weight management behaviour, judo
competitors ranked dietitians second to last, ahead
only of physicians (Artioli et al., 2010b). The most
influential advisor was the coach. In that context, a
more effective way to modify athlete behaviour may
be for sports dietitians and nutritionists to educate
coaches, using workshops and handbooks that are
specifically targeted at them, about the importance of
energy availability and practical techniques for
managing it.
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Energy availability in athletes S15
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... This simplification is pertinent when an energydeficient organism may reduce basal metabolism in an attempt to restore balance, albeit with a suppression of nonimmediately essential physiological functions (Stubbs et al., 2004). Taken together, the concept of EA may be a more useful model for longitudinal adaptation to training as it is closer to an "input" to the body's physiological systems (Loucks et al., 2011). In an athletic population, reduced EA (30-45 kcal·kg FFM −1 ·day −1 ) has been associated with increased risk of impaired physiological functions and physical performance (Loucks et al., 2011). ...
... Taken together, the concept of EA may be a more useful model for longitudinal adaptation to training as it is closer to an "input" to the body's physiological systems (Loucks et al., 2011). In an athletic population, reduced EA (30-45 kcal·kg FFM −1 ·day −1 ) has been associated with increased risk of impaired physiological functions and physical performance (Loucks et al., 2011). Reduced EA has been shown to increase risk of bone stress injuries in both men and women (Papageorgiou et al., 2017), increase risk of menstrual disorders and infertility in women (Loucks et al., 2011), and reduce testosterone levels in men (Burke, Close, et al., 2018;Hackney, 2020). ...
... In an athletic population, reduced EA (30-45 kcal·kg FFM −1 ·day −1 ) has been associated with increased risk of impaired physiological functions and physical performance (Loucks et al., 2011). Reduced EA has been shown to increase risk of bone stress injuries in both men and women (Papageorgiou et al., 2017), increase risk of menstrual disorders and infertility in women (Loucks et al., 2011), and reduce testosterone levels in men (Burke, Close, et al., 2018;Hackney, 2020). Low EA (LEA; ≤30 kcal·kg FFM −1 ·day −1 ) limits the amount of energy used for thermoregulation, growth, cellular maintenance, and reproduction in favor of the more crucial physiological mechanisms that are necessary for survival, with implications for health and performance (Mountjoy et al., 2018). ...
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Military training is characterized by high daily energy expenditures which are difficult to match with energy intake, potentially resulting in negative energy balance (EB) and low energy availability (EA). The aim of this study was to quantify EB and EA during British Army Officer Cadet training. Thirteen (seven women) Officer Cadets (mean ± SD: age 24 ± 3 years) volunteered to participate. EB and EA were estimated from energy intake (weighing of food and food diaries) and energy expenditure (doubly labeled water) measured in three periods of training: 9 days on-camp (CAMP), a 5-day field exercise (FEX), and a 9-day mixture of both CAMP and field-based training (MIX). Variables were compared by condition and gender with a repeated-measures analysis of variance. Negative EB was greatest during FEX (−2,197 ± 455 kcal/day) compared with CAMP (−692 ± 506 kcal/day; p < .001) and MIX (−1,280 ± 309 kcal/day; p < .001). EA was greatest in CAMP (23 ± 10 kcal·kg free-fat mass [FFM] ⁻¹ ·day ⁻¹ ) compared with FEX (1 ± 16 kcal·kg FFM ⁻¹ ·day ⁻¹ ; p = .002) and MIX (10 ± 7 kcal·kg FFM ⁻¹ ·day ⁻¹ ; p = .003), with no apparent difference between FEX and MIX ( p = .071). Irrespective of condition, there were no apparent differences between gender in EB ( p = .375) or EA ( p = .385). These data can be used to inform evidenced-based strategies to manage EA and EB during military training, and enhance the health and performance of military personnel.
... The EA is obtained by subtracting exercise energy expenditure from energy intake, adjusted by FFM (Loucks, 2004;Loucks et al., 2011). Each component of the equation relies on accurate measurement tools and a clear definition of what should be measured (Loucks, 2004). ...
... concurrently with the period of growth and development, and may lead to irreparable impairment (Loucks, 2004;Loucks et al., 2011). ...
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Energy availability (EA) is calculated by subtracting exercise energy expenditure from energy intake, adjusted for fat-free mass (FFM) obtained using accurate methods, such as dual-energy X-ray absorptiometry (DXA). Unlike DXA, the bioelectrical impedance analysis (BIA) is low in cost, simple and easy to carry out. This study aimed to test the concordance between the calculation of EA using FFM values from four BIA predictive equations and FFM obtained using DXA in female adolescent athletes ( n = 94), recruited via social media. Paired Student’s t test, Wilcoxon test, Lin’s concordance correlation coefficient, root mean square error, limits of agreement, and mean absolute percentage error were used to evaluate agreement between the FFM values obtained by the four SF-BIA predictive equations and DXA. Regression linear analysis was used to determine the relation between FFM values obtained using DXA and the BIA predictive equations. Standardized residuals of the FFM and EA were calculated considering DXA values as reference. The most appropriate model for the FFM (limits of agreement = 4.0/−2.6 kg, root mean square error = 1.9 kg, mean absolute percentage error = 4.34%, Lin’s concordance correlation coefficient = .926) and EA (limits of agreement = 2.51/4.4 kcal·kg FFM ⁻¹ ·day ⁻¹ , root mean square error = 1.8 kcal·kg FFM ⁻¹ ·day ⁻¹ , mean absolute percentage error 4.24%, Lin’s concordance correlation coefficient = .992) was the equation with sexual maturity as a variable, while the equation with the greatest age variability was the one with the lowest agreement. FFM-BIA predictive equations can be used to calculate EA of female adolescent athletes. However, the equation should be chosen considering sex, age, and maturation status. In the case of athletes, researchers should use equations developed for this group.
... In a similar manner, the proportion of players in the poor EA range (<30 kcal/kgFFM/day) was highest on the heavy training load days. This phenomenon where an increase in EEE is not accompanied by an increase in EI has been commonly recorded in female athletes (more so than their male counterparts) [27,28]. In the varsity athlete population specifically, it is difficult to determine whether this discrepancy stems from a lack of knowledge, a lack of preparation, or the inability to prepare for ever-changing schedules as a student-athlete. ...
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This study estimated the daily energy intake (EI) and energy expenditure (TDEE) in female varsity rugby union players during a weekly training/game cycle. Fifteen (nine forwards, six backs) players (20.5 ± 0.4 y, 167.1 ± 1.8 cm, 74.9 ± 2.9 kg) were monitored for a 7-day period (one fitness, two heavy training, one light training, one game, and two recovery days) during their regular season. The average EI throughout the week for all 15 players was 2158 ± 87 kcal. There were no significant differences between days, but the lowest EI (1921 ± 227 kcal) occurred on the mid-week recovery day and the highest on game day (2336 ± 231 kcal). The average TDEE was 2286 ± 168 kcal (~6% > EI). The mean energy availability (EA) over the 7-day period was 31.1 ± 3.6 kcal/kg FFM/day for the group. Of the players, 14% were in the optimal EA range (>45 kcal/kg FFM/day); 34% were in the moderate range (≥30–45 kcal/kg FFM/day); and 52% had a poor EA of <30 kcal/kg FFM/day. Carbohydrate (3.38 ± 0.36 g/kg/day, 45% of EI); fat (1.27 ± 0.12 g/kg/day, 37% of EI); and protein (1.38 ± 0.12 g/kg/day, 18% of EI) consumption remained similar throughout the week (p > 0.05). The players consumed 6% less energy than they expended, providing poor to moderate EA; therefore, daily carbohydrate intake recommendations were not met.
... The distinction between athletes and non-athletes must be made in terms of highly variable exercise behavior. Athletes undertaking high training volume and low energy availability may occur without disordered eating due to unintentionally failing to consume sufficient energy (Loucks et al., 2011). In agreement with the present findings, interestingly a high prevalence of orthorexia symptoms via ORTO-15 was also found in the non-athletic healthy eating community on Instagram (Turner and Lefevre, 2017) and yoga practitioners (Herranz Valera et al., 2014;Carmo, 2019, 2021). ...
... The distinction between athletes and non-athletes must be made in terms of highly variable exercise behavior. Athletes undertaking high training volume and low energy availability may occur without disordered eating due to unintentionally failing to consume sufficient energy (Loucks et al., 2011). In agreement with the present findings, interestingly a high prevalence of orthorexia symptoms via ORTO-15 was also found in the non-athletic healthy eating community on Instagram (Turner and Lefevre, 2017) and yoga practitioners (Herranz Valera et al., 2014;Carmo, 2019, 2021). ...
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The article aims to summarize the literature about the profile of risk of orthorexia in athletes using the ORTO-15 questionnaire. The search was performed at PubMed, Embase, Web of Science, and Sport Discus databases, using the terms "orthorexia" AND "athletes" with the respective entry terms. A multistage process of selection followed the PRISMA 2020 recommendation. A total of 688 articles were identified, and six studies were available for the final process. The prevalence of risk for orthorexia was assessed by the articles by the ORTO-15 questionnaire and ranged between 38 and 35 points. The comparison between male and female athletes and, athletes and non-athletes was not significant in the six articles. In conclusion, the review highlights that athletes from different sports, included in the review, do not present a risk of orthorexia nervosa considering the cutoff of 40 points, but not 35 points. Also, athletes present the same orthorexic behavior compared to non-athletes, demonstrating that orthorexia is an issue that needs to be considered in the general population. Moreover, a special focus should be given on the ORTO-15 questionnaire, about the sensitivity to diagnose the prevalence of orthorexia, especially in athletes.
... exercise, lays an important issue for the health and success of sports nutrition strategies [12]. Consequently, each athlete/exerciser is different, and there is not an optimal diet that covers the requirements of every athlete at all periods. ...
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... Interestingly, the present study found that the dietary energy deficit of the elderly (≥ 51 years old) is only about 10% (Table 4), which is due to the fact that residents of this age group mostly followed the "local traditional diet" characterized by a high intake of Tsampa (roasted highland barley flour), cultural-specific beverages (Tibetan sweet tea and yak buttered tea), potato, and yak beef (28). Dietary energy is essential for physiological processes, including locomotion, thermoregulation, reproduction, and growth (35). Prolonged periods of energy deficit can negatively impact health and performance, because low energy availability can alter endocrine signaling from the central nervous system (i.e., decreased release of gonadotropin releasing hormone to suppress reproductive function) in response to acute changes in cellular fuel oxidation and peripheral hormones (36), muscle growth and repair, hemoglobin synthesis, bone formation and repair, immune function, and cardiovascular function were affected significantly (37). ...
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We aimed to evaluate patterns of bone mineral accrual among a cross-sectional sample of female adolescent runners and girls participating in a nonendurance running sport. One-hundred and eighty-three interscholastic competitive female athletes (age 16.0 +/- 0.1 years), 93 endurance runners and 90 nonrunners, completed a menstrual and sports history questionnaire, had their height and weight measured, and underwent a dual-energy X-ray absorptiometry scan for the measurements of body composition and bone mass. For the majority of analyses, the girls were separated into four groups according to their age (13 to 14 years, 15 years, 16 years, and 17 to 18 years). Runners' height, weight, body mass index (BMI), percent body fat, lean tissue mass, number of menstrual cycles in the past year, and months of participation in a non-lean-build/variable-impact-loading sport were significantly lower than mean values for nonrunners. Although bone mass rose at all sites in the nonrunners between the ages of 13 to 14 years and 17 to 18 years, no such increase was noted in the runners. Runners compared with nonrunners exhibited significantly lower body weight and height-adjusted total body and lumbar spine bone mineral content (BMC) values and lower bone mineral density (BMD) Z-score values among the older (16 years and/or 17 to 18 years) but not younger (13 to 14 years and/or 15 years) age groups. These findings suggest that the runners, in contrast to the nonrunners, exhibited a suppressed bone mineral accrual pattern, which supports the notion that female adolescent endurance runners may be at risk for inadequate bone mass gains and thus a low peak BMD.
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The effects of prolonged treadmill running on appetite, energy intake and acylated ghrelin (an appetite stimulating hormone) were examined in 9 healthy males over the course of 24h. Participants completed 2 experimental trials (exercise and control) in a randomised-crossover fashion. In the exercise trial participants ran for 90 min at 68.8 + or - 0.8% of maximum oxygen uptake followed by 8.5 h of rest. Participants returned to the laboratory on the following morning to provide a fasting blood sample and ratings of appetite (24 h measurement). No exercise was performed on the control trial. Appetite was measured within the laboratory using visual analogue scales and energy intake was assessed from ad libitum buffet meals. Acylated ghrelin was determined from plasma using an ELISA assay. Exercise transiently suppressed appetite and acylated ghrelin but each remained no different from control values in the hours afterwards. Furthermore, despite participants expending 5324 kJ during exercise there was no compensatory increase in energy intake (24 h energy intake; control 17,191 kJ, exercise 17,606 kJ). These findings suggest that large energy deficits induced by exercise do not lead to acute compensatory responses in appetite, energy intake or acylated ghrelin.