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To cite this article: Anne B Loucks (2004): Energy balance and body composition in sports and exercise, Journal of Sports
Sciences, 22:1, 1-14
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Journal of Sports Sciences, 2004, 22, 1–14
Many athletes, especially female athletes and participants in endurance and aesthetic sports and sports with
weight classes, are chronically energy deficient. This energy deficiency impairs performance, growth and health.
Reproductive disorders in female athletes are caused by low energy availability (defined as dietary energy intake
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minus exercise energy expenditure), perhaps specifically by low carbohydrate availability, and not by the stress
of exercise. These reproductive disorders can be prevented or reversed by dietary supplementation in
compensation for exercise energy expenditure without any moderation of the exercise regimen. Energy balance
is not the objective of athletic training. To maximize performance, athletes strive to achieve an optimum sport-
specific body size, body composition and mix of energy stores. To pursue these objectives, athletes need to
manage fat, protein and carbohydrate balances separately, but it is impractical for athletes to monitor these
balances directly, and appetite is not a reliable indicator of their energy and macronutrient needs. To guide their
progress, athletes need to eat by discipline and to monitor specific, reliable and practical biomarkers of their
objectives. Skinfolds and urinary ketones may be the best biomarkers of fat stores and carbohydrate deficiency,
respectively. Research is needed to identify and validate these and other markers.
compiled in the same normalized units (Burke et al., pass what might be called the ‘laugh test’ (Goldberg et
2001). These data were compiled before 1971, between al., 1991).
1971 and 1989, and since 1990. The latter data offer Considering the lack of confidence in studies of
insight into the dietary habits of athletes since the energy balance in athletes, it is surprising that few have
publication of the 1991 IOC consensus recommenda- included biochemical measurements to validate energy
tions. If these data are to be believed, however, one intake and expenditure data, because under-reporting
observation is particularly noteworthy. With the notable would not account for biochemical evidence of energy
exception of cross-country skiers, female athletes deficiency. In several studies characterizing reproduc-
consume only about 70% as much energy and tive disorders in female athletes, metabolic substrates
carbohydrate – normalized for body weight – as do and hormones have been measured, and they tell a
male athletes (see Figs 1 and 2). consistent story of chronic energy and carbohydrate
Many investigators have been sceptical of data from deficiency (Myerson et al., 1991; Loucks et al., 1992;
the dietary records of female athletes, because studies Jenkins et al., 1993; Laughlin and Yen, 1996, 1997; De
comparing such data to estimations or measurements of Souza et al., 2003). Female athletes display a spectrum
their energy expenditure have repeatedly found appar- of metabolic substrate and hormone abnormalities
ently huge negative energy balances, some exceeding 4 indicative of the mobilization of fat stores, the slowing
MJ × day71 in athletes with stable body weights of metabolic rate and a decline in glucose utilization,
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(Mulligan and Butterfield, 1990; Wilmore et al., 1992; with more extreme abnormalities in amenorrhoeic
Edwards et al., 1993; Beidleman et al., 1995; Hill and athletes and less extreme abnormalities in regularly
Davies, 2002). Such large discrepancies have been menstruating athletes. So, while some might question
interpreted as indicating that female athletes grossly whether lower energy and carbohydrate intakes might
under-report their dietary intake. In support of this be appropriate for women if their energy and carbohy-
allegation, investigators have cited certain other special drate expenditures are less than those of men, the
sub-populations that have been found to under-report, biochemical data from these studies demonstrate that
but a meta-analysis of studies comparing dietary female athletes are, indeed, chronically energy deficient.
assessments to measurements of energy expenditure It is to be emphasized here that ‘efficiency’ is the
by doubly labelled water found that women do not wrong concept to apply to pathologic adjustments to
under-report more than men (Trabulsi and Schoeller, chronic energy deficiency. Scarce metabolic fuels
2001). Some investigators have questioned the methods consumed in locomotion are unavailable for important
used to measure energy intake and expenditure. physiological functions such as immune function,
Indeed, the study that found virtually identical energy growth and maintenance functions such as tissue
intakes in female and male cross-country skiers took turnover, as well as reproductive development and
extraordinary pains to achieve accurate measurements function. For example, 50% of peak bone mass is
of energy intake (Sjodin et al., 1994). As a result of such deposited during adolescence, but energy deficiency
concerns, quantitative criteria have been developed to reduces the rate of bone formation by suppressing
assess whether reported energy intakes in studies of growth factors and increases the rate of bone resorption
various numbers of athletes over various lengths of time by suppressing reproductive hormones. The resulting
** **
CHO Intake (g CHO á kgÐ1
** **
p<0.01 p<0.01 p<0.01 p<0.01
Energy Intake (kJ á kgÐ1
300 10
BW á day Ð1)
BW á dayÐ1)
200
5
100
0 0
Running Swimming XC-Skiing Running Swimming XC-Skiing
Fig. 1. Energy intakes of male and female endurance athletes Fig. 2. Carbohydrate (CHO) intakes of male and female
in running, swimming and cross-country skiing (Burke et al., endurance athletes in running, swimming and cross-country
2001). skiing (Burke et al., 2001).
Energy balance and body composition in sports and exercise 3
mg á dlÐ1
40 20
30
20 10
10
0 Pre Late Post 0 Pre Late Post
(a) (b)
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Fig. 3. (a) Energy intake and (b) prealbumin concentration in male wrestlers (*) and weight-matched controls (*) before (Pre),
late during (Late) and after (Post) the wrestling season. Dashed lines indicate the normal range of prealbumin (reproduced with
permission from Roemmich and Sinning, 1997a).
GH IGF-I Free T
10 500 40
8 400 30
6 300
ng á mlÐ1
ng á mlÐ1
pg á mlÐ1
20
4 200
10
2 100
suppressed prealbumin. Prealbumin is a classic bio- hormone resistance is another classic sign of energy
marker of starvation. deficiency. As in energy-deficient female athletes, the
Figure 4 shows the corresponding measurements of reproductive systems in these under-nourished male
growth hormone, IGF-I and testosterone in these athletes are also suppressed, as evidenced by the decline
wrestlers. During the season, the male wrestlers display in testosterone to below the normal range. As might be
growth hormone resistance, with suppressed IGF-I expected with reduced anabolic stimulation by testos-
concentrations despite elevated growth hormone, as do terone and IGF-I, the wrestlers’ fat-free mass, and their
female athletes with menstrual disorders. Growth mid-arm and mid-thigh cross-sectional areas, all
Energy balance and body composition in sports and exercise 5
declined during the season. As a result, their arm and LH pulse frequency, whereas low energy availability
leg strength and power declined by an average of 13% suppressed LH pulse frequency, regardless of whether
(Roemmich and Sinning, 1997a), in conflict with the the low energy availability was caused by dietary energy
belief that weight loss conveys a competitive advantage. restriction alone or by exercise energy expenditure
We have investigated the independent effects of alone. (Similar results were obtained when half of the
energy availability and exercise stress on reproductive reduction in energy availability was caused by dietary
function in exercising women (Loucks et al., 1998). All energy restriction and half by exercise energy expendi-
previous investigations of the ‘activity–stress paradigm’ ture.) Low energy availability also suppressed T3,
had confounded the stress of exercise with its energy insulin, IGF-I and leptin (Hilton and Loucks, 2000),
cost by having animals exercise longer and longer for while it increased growth hormone and cortisol in a
smaller and smaller food rewards. Furthermore, despite pattern very reminiscent of amenorrhoeic and luteally
60 years of research on exercise stress, there was still no suppressed eumenorrhoeic athletes. Unexpectedly, the
objective definition of exercise stress itself. As shown in effects of low energy availability on LH pulse frequency
Fig. 5, we defined energy availability operationally as and on the metabolic hormones in the exercising
dietary energy intake minus exercise energy expendi- women were smaller than those in the dietarily
ture, and we defined exercise stress operationally and restricted women, even though their balanced and
independently as everything associated with exercise, deprived energy availabilities were exactly matched, and
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except exercise energy expenditure. Habitually seden- no-one had ever hypothesized that exercise would be
tary women of normal body composition were assigned protective of reproductive function. Further investiga-
to sedentary or exercising groups and were adminis- tion revealed that the exercising women had a higher
tered balanced and deprived energy availability treat- carbohydrate availability (defined observationally as
ments in random order under controlled conditions in dietary carbohydrate intake minus exercise carbohy-
the laboratory. drate oxidation), due to a glucose-sparing alteration in
After 4 days, blood was sampled at 10 min intervals skeletal muscle fuel selection during energy deprivation.
for 24 h for the assessment of LH pulsatility, upon Endocrine markers of energy deficiency have also
which ovarian function critically depends. As shown in been found in a prospective study of young, healthy,
Fig. 6, the stress of exercise had no suppressive effect on lean men during the US Army’s 8-week course for
training and selecting the elite combat unit leaders
known as Rangers (Friedl et al., 2000). This course is
conducted in four consecutive 2-week stages in forest,
mountain, desert and swamp environments. Besides
environmental exposures to heat and cold, soldiers are
exposed to workloads demanding sustained high energy
20 0
-1
15
*
-2
Pulses á dayÐ1
-3
10
-4
5 -5
Fig. 5. Experimental design. Dietary energy intake (I) and
exercise energy expenditure (E) were controlled to achieve
balanced (B = 45 kcal × kg71 FFM × day71) and deprived
0
(a)
S X
-6
-7
(b)
* *
S X
(D = 10 kcal × kg71 FFM × day71) energy availability
(A = I7E) treatments. Deprived energy availability was
Fig. 6. (a) Luteinizing hormone (LH) pulse frequency in
achieved by dietary restriction alone in sedentary women (S)
sedentary (S) and exercising (X) women with the same energy
and by exercise energy expenditure alone in exercising women
availability. (b) Reduction in LH pulse frequency caused by
(X) (1 kcal = 4.18 kJ) (reproduced with permission from
low energy availability in sedentary (S) and exercising (X)
Loucks et al., 1998).
women. *P 50.01 (adapted from Loucks et al., 1998).
6 Loucks
expenditures (18 MJ × day71 measured by doubly of their exercise regimen (Williams et al., 2001). All
labelled water), sleep deprivation (54 h × day71) and these results show that low energy availability, not the
chronic energy deficiency (4 MJ × day71 average nega- stress of exercise – and neither dietary energy intake nor
tive energy balance). Participants lose 13% of body exercise energy expenditure alone – is what disrupts the
weight, including 51% of fat mass and 6% of fat-free reproductive system in men and women, as well as
mass. Illness, infections and injuries are commonplace. female monkeys, and that this disruption can be
These rigours are so extreme that only 30% of prevented by dietary supplementation in compensation
participants finish the course. Figure 7 shows the for exercise energy expenditure without any moderation
schedule of alternating weeks of controlled semi- of the exercise regimen (or other stresses).
starvation and refeeding and the timing of blood We have also investigated the dose-dependent effects
sampling in relation to total daily energy expenditure of energy availability on LH pulsatility and on metabolic
and average energy intake during the course. substrates and hormones in exercising women (Loucks
Figure 8 shows the effects of all these factors on and Thuma, 2003). Figure 9 shows the experimental
metabolic and reproductive hormones. Note that effects design in which energy availability was set at 10, 20, 30
on reproductive as well as metabolic hormones follow and 45 kcal × kg71 FFM × day71, by having all partici-
the feeding schedule, despite continued exercise and pants perform 15 kcal × kg71 FFM × day71 of exercise at
environmental stresses. One week of controlled refeed- 70% V̇O2max (similar to running 7 miles) while
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ing during the course and one week of ad libitum consuming 25, 35, 45 or 60 kcal × kg71 FFM × day71
refeeding after the 8-week course fully restored both of dietary energy (where FFM = fat-free mass). All
metabolic and reproductive hormones to their initial participants were administered the balanced energy
values. Note that the restoration of reproductive availability treatment (45 kcal × kg71 FFM × day71) and
function during week 5 occurred despite the continua- one of the restricted energy availability treatments in
tion of the exercise and other stresses in the training random order.
programme. Figure 10 shows the dose-dependent effects of energy
In a study of another group of candidates in a availability on LH pulsatility. Luteinizing hormone
Rangers training course, strength, power and vertical pulse frequency was suppressed and amplitude in-
jump all declined by *20% during the course (Nindl et creased below a threshold of energy availability between
al., 1997), showing that sustained energy deficiency 20 and 30 kcal × kg71 FFM × day71. Figure 11 shows the
substantially impairs physical performance. dose-dependent effects of energy availability on meta-
Meanwhile, experiments have shown that increasing bolic substrates and hormones. Statistical analysis
exercise energy expenditure induces amenorrhoea in
female monkeys and that dietary supplementation then
restores their menstrual cycling without any moderation
50
25 IGF-I T3
Effects (%)
0
6000 -25
5000 -50
Daily Energy Intake
TDEE
-75
(kcal á dayÐ1)
4000
AEI -100
3000 50
2000 25 LH T
Effects (%)
0
1000 -25
0 -50
1 2 3 4 5 6 7 8 -75
Week -100
0123456789 0123456789
Fig. 7. Energy intake and expenditure during the US Army Week Week
Rangers training course. TDEE = total daily energy expendi-
ture determined by doubly labelled water; AEI = average Fig. 8. Effects of US Army Rangers training course on
energy intake from controlled feeding. Arrows indicate blood metabolic (IGF-I and T3) and reproductive (LH and testos-
sampling times (1 kcal = 4.18 kJ) (reproduced with permission terone (T)) hormones. Error bars indicate+1 standard error
from Friedl et al., 2000). (adapted from Friedl et al., 2000).
Energy balance and body composition in sports and exercise 7
60 (I)
50
Energy Intake and Expenditure
ta ke
r g y In
Ene
(kcal á kgÐ1 FFM á dayÐ1)
50 tary
D ie
40 trol
led 25 Amplitude/3
Effects (%)
n
Co
30 0
20
Frequency
10 -25
Controlled Exercise Energy Expenditure (X)
0
0 5 10 15 20 25 30 35 40 45 50 -50
Energy Availability (kcal á kgÐ1 FFM á dayÐ1)
Dietary Enery Intake Minus Exercise Energy Expenditure
0 10 20 30 40 50
Ð1
Energy Availability (kcal á kg FFM á dayÐ1)
Fig. 9. Experimental design. Women were assigned to
contrasting energy availability treatments of 45 and 10, 45
and 20, and 45 and 30 kcal × kg71 FFM × day71. All partici- Fig. 10. Incremental effects of low energy availability on LH
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pants performed 15 kcal × kg71 FFM × day71 of exercise at pulse amplitude (*, top) and LH pulse frequency (*,
70% V̇O2max under supervision while their dietary energy bottom). Effects are expressed relative to values at
intake was controlled to achieve the intended energy avail- 45 kcal × kg71 FFM × day71. Effects on LH pulse amplitude
ability treatments (1 kcal = 4.18 kJ) (reproduced with permis- have been divided by three for graphical symmetry. As energy
sion from Loucks and Thuma, 2003). #The Endocrine availability declines from energy balance at approximately
Society. 45 kcal × kg71 FFM × day71, effects begin at a threshold at
approximately 30 kcal × kg71 FFM × day71 and become more
extreme as energy availability is further reduced below
20 kcal × kg71 FFM × day71 (1 kcal = 4.18 kJ) (reproduced
showed that the dose-dependent effects on LH pulsa- with permission from Loucks and Thuma, 2003). #The
tility were most similar to those on the metabolic Endocrine Society.
substrates glucose and b-hydroxybutyrate and to the
metabolic hormones cortisol and growth hormone, and
contrasted with the dependencies displayed by the other In athletes, body weight is not a reliable indicator of
metabolic hormones. These results support the hypoth- either energy or macronutrient balance. Because
esis that reproductive function reflects the availability of protein and glycogen stores are associated with much
metabolic fuels, especially glucose, which may be more body water than are fat stores, for example, a
signalled in part by activation of the adrenal axis. They weight gain due to small increases in protein or
also suggest that athletes may be able to prevent glycogen energy stores can counterbalance the weight
menstrual disorders by maintaining energy availabilities loss due to larger reductions in fat energy stores during
above 30 kcal × kg71 FFM × day71. negative energy balance. Energy balance, itself, conveys
little information about an athlete’s present status or
progress towards multiple objectives that may be in
Energy balance is not the objective opposite directions for different components of body
composition.
Athletic performance is maximized, in part, by a sport- For several reasons, the nutritionist’s expression of
specific (and in team sports, position-specific) optimum the first law of thermodynamics (energy balance =
body size, body composition and mix of stored energy intake 7 energy expenditure) and quantitative
metabolic fuels. Sprinters have no use for fat stores, information about energy intake and expenditure (even
for example, whereas runners in ultra-endurance events if it is accurate) are of little practical use to athletes who
need them for fuel, swimmers need them for buoyancy aim to achieve selective changes in their body size and
and cold-water swimmers need them for insulation. composition and in their stores of specific fuels. To
Commonly, aspiring competitive athletes do not man- begin, it is not feasible for athletes to measure their
ifest these optima for their chosen sports and much of energy intake and expenditure accurately on a day-to-
their training aims to modify their bodies to achieve day basis as a method for managing their athletic
them. Considering the initial conditions of many training. Major metabolic processes activated in re-
athletes in many sports, however, their aims are often sponse to diet and exercise are out of the athlete’s
to reduce fat mass while increasing fat-free mass and control and perception. Moreover, macronutrients are
glycogen stores. metabolized differently and stored separately so that the
8 Loucks
75 75
Effects (%) 50 >HOB/50 (a) 50
Cortisol (b)
25 25
Effects (%)
0 0
-25 -25
2*Glucose
-50 -50
Insulin
-75 -75
0 10 20 30 40 50 0 10 20 30 40 50
Energy Availability (kcal á kgÐ1 FFM á dayÐ1) Energy Availability (kcal á kgÐ1 FFM á dayÐ1)
75 75
50
(c) 50
(d)
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GH
25 25
Effects (%)
Effects (%)
0 0
IGFI/BP3
-25 -25
IGF-I 2*T3
-50 -50
IGFI/BP1 Leptin
-75 -75
0 10 20 30 40 50 0 10 20 30 40 50
Energy Availability (kcal á kgÐ1 FFM á dayÐ1) Energy Availability (kcal á kgÐ1 FFM á dayÐ1)
Fig. 11. Incremental effects of energy availability on metabolic substrates and hormones. (a) Incremental effects on the metabolic
substrates b-hydroxybutyrate (*, upper left top) and plasma glucose (*, upper left bottom). Effects are shown relative to values at
45 kcal × kg71 FFM × day71. Effects on b-hydroxybutyrate have been divided by 50 and effects on plasma glucose have been
doubled for graphical symmetry. Effects on b-hydroxybutyrate and glucose become progressively more extreme as energy
availability decreases. (b) Incremental effects on the metabolic hormones cortisol (*, upper right top) and insulin (*, upper right
bottom). Effects are shown relative to values at 45 kcal × kg71 FFM × day71. Insulin declines linearly with energy availability, while
effects on cortisol become progressively more extreme as energy availability decreases. (c) Incremental effects on the somatotrophic
metabolic hormones growth hormone (GH) (&, lower left top) and IGF-I (&, lower left bottom) and the ratios IGF-I/IGFBP-1
(~, lower left bottom) and IGF-I/IGFBP-3 (*, lower left bottom). Effects are shown relative to values at 45 kcal × kg71
FFM × day71. Effects on GH and IGF-I tend to flatten out below 20 kcal × kg71 FFM × day71 as growth hormone resistance
becomes more extreme. Both estimates of bioactive IGF-I have declined significantly and substantially at 30 kcal × kg71
FFM × day71. (d) Incremental effects on the metabolic hormones T3 (&, lower right bottom) and leptin (*, lower right bottom).
Effects are shown relative to values at 45 kcal × kg71 FFM × day71. The effect on T3 is doubled for graphical clarity. Both T3 and
leptin have declined significantly and substantially at 30 kcal × kg71 FFM × day71. These effects tend to flatten out below
20 kcal × kg71 FFM × day71 (1 kcal = 4.18 kJ) (reproduced with permission from Loucks and Thuma, 2003). #The Endocrine
Society.
conversion of one macronutrient into another for high in n-3 polyunsaturated fats then reversed the
storage does not represent important metabolic path- increase in fat mass within 4 weeks.
ways (Flatt, 1988). Fats eaten above the day’s nutri- Humans can ingest large amounts of carbohydrate
tional requirement are nearly all stored in the body without initiating de novo lipogenesis at rates greater
(Schutz et al., 1989), but not all fats are obesogenic than fat oxidation (Acheson et al., 1982). In humans, de
(Wang et al., 2002). Seven weeks of a high saturated fat novo lipogenesis from excess glucose occurs to only a
diet increased fat mass, whereas an isoenergetic diet negligible degree in the liver (Hellerstein et al., 1991;
equally high in n-3 polyunsaturated fats reduced fat Aarsland et al., 1997). In adipose tissue, it occurs only
mass compared to an isoenergetic low fat diet. Switch- during experimentally imposed sustained, extreme
ing mice from the diet high in saturated fats to the one carbohydrate overfeeding, and then only with low
Energy balance and body composition in sports and exercise 9
efficiency (Macdonald, 1999) until glycogen storage humans, the brain is so large and so metabolically active
capacity has been saturated (Acheson et al., 1988). The that its daily energy requirement exceeds the entire liver
more efficient conversion that occurs after glycogen glycogen storage capacity (Bursztein et al., 1989).
stores are experimentally saturated is unlikely to occur Moreover, muscle glycogen stores are not available to
in everyday life and even less likely in athletes, especially the brain, because glucose stored as muscle glycogen
endurance athletes, who mobilize and oxidize substan- cannot be returned to the bloodstream. This is why liver
tial amounts of glycogen during and after exercise each glycogen stores have to be replenished every day by
day. A transient excess dietary carbohydrate intake dietary carbohydrate. Furthermore, since skeletal mus-
stimulates insulin release, which promotes glucose cle has access to liver glycogen stores, skeletal muscle
uptake and oxidation as well as glycogen synthesis and competes directly against the brain for all available
storage. A transient excess protein intake also stimulates carbohydrate. In a marathon race, working muscle
its own oxidation and, like carbohydrate, is only stored consumes as much glucose in 2 h as the brain requires
short term. in a week. Under conditions in which the brain is
In the tricarboxylic acid cycle, substantial quantities deprived of glucose, physiological mechanisms are
of both fats and carbohydrates are oxidized during and activated to mobilize fat stores and to convert the
after exercise, but the magnitudes and proportions of resulting fatty acids to ketones, which are the brain’s
each depend on the duration of the exercise performed only alternative energy source. Available evidence
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and on the size and macronutrient content of the diet suggests that reproductive function depends not on
(Folch et al., 2001). Considering energy expenditure energy availability in general, but rather on brain
both during and after exercise, glycogen balance is glucose availability (i.e. liver glycogen stores) in
positive only when large carbohydrate-rich meals are particular.
consumed, but less positive, of course, on a day of
exercise than on a day of rest when the increased
oxidation of glycogen during and after exercise is Management by objectives
avoided (Folch et al., 2001). Fat balance, on the other
hand, is negative regardless of whether carbohydrate- Separately managing fat, protein and carbohydrate
rich meals are large or small, and more negative on a balances will be even less practical than managing
day of exercise than on a day of rest, regardless of the energy balance if athletes attempt to estimate fat,
exercise intensity (Folch et al., 2001). protein and carbohydrate intakes and expenditures in
Therefore, because macronutrients are metabolized place of energy intake and expenditure. Nor will
differently and stored separately, an athlete needs to athletes be aided much by sophisticated markers of
manage fat, protein and carbohydrate balances sepa- conditions that are not objectives, such as energy
rately to achieve sport-specific body size, body compo- balance. Athletes need specific markers of their status
sition and energy store objectives. To reduce fat mass, and progress towards particular body size, body
athletes need to induce negative fat balance by composition and energy store objectives. Is fat mass
minimizing the intake of saturated fats and maximizing decreasing? Is fat-free mass increasing? Are muscle
the oxidation of fats by exercising for several hours a glycogen stores being adequately replenished? Are liver
day. Since lean body mass may be increasing as fat mass glycogen stores being adequately maintained?
is declining, this may not necessarily involve a reduction Research is needed to validate specific, accurate and
in energy intake, energy balance or body weight. To practical biomarkers for answering such questions.
increase fat-free mass, athletes need to induce positive Ideally, a single measurement of a biomarker would
protein balance by consuming adequate amounts of provide the desired information. For many candidate
complete protein, together with sufficient carbohydrate, markers, however, the normal range in the general
to fuel anabolic processes and by exercising in a specific population is wide compared with the effects of
manner for promoting the development of target improper nutrition. Recall that testosterone was the
skeletal muscle and bone components. Athletes also only hormone outside the normal range in wrestlers
need to consume plenty of carbohydrates to elevate (Roemmich and Sinning, 1997b). Repeated measures
insulin concentrations to promote the uptake of amino of metabolic hormones may be necessary to detect
acids and the synthesis of protein by muscle, as well as changes over time within an individual. Preferably, a
to replenish muscle glycogen stores for future exercise, biomarker would also be inexpensive, convenient to
and to replenish liver glycogen stores for brain as well as administer and minimally invasive. Anthropometric
muscle metabolism. measurements would be preferable to a urinalysis, for
In this regard, it is essential to remember that because example. Urinalysis, in turn, would be preferable to the
fatty acids do not cross the blood–brain barrier, the assay of a blood sample, but even that would be
brain relies on glucose for energy. Furthermore, in preferable to any measurement requiring the infusion of
10 Loucks
Densitometry and electrical impedance can be used Fig. 12. Concentrations for IGF-I at 07.00 h, T3 at 07.00 h,
to monitor fat-free mass, but the most useful biomar- 24 h mean leptin and leptin at 07.00 h in a group of regularly
kers of muscle development may be measures of menstruating women after 5 days at a balanced energy
strength and endurance performance. availability of 45 kcal × kg71 FFM × day71 and after 5 days at
There is considerable interest in metabolic hormone a severely low energy availability of 10 kcal × kg71
FFM × day71 (1 kcal = 4.18 kJ).
concentrations in the blood as biomarkers of carbohy-
drate availability. Concentrations of T3 are determined
by carbohydrate availability, not carbohydrate intake
(Loucks and Callister, 1993). On the usual mixed diet,
T3 is suppressed at a threshold of energy availability
corresponding to a critical carbohydrate availability
(Loucks and Heath, 1994), like LH pulsatility. Leptin,
too, reflects carbohydrate availability. Synthesized in
adipose tissue cells, leptin was originally thought to
communicate information about fat stores (Maffei et
al., 1995). Later reports of leptin varying profoundly
before any changes in adiposity in response to fasting
(Kolaczynski et al., 1996b; Weigle et al., 1997), dietary
restriction (Weigle et al., 1997), refeeding after dietary
restriction (Kolaczynski et al., 1996b; Jenkins et al.,
1997) and overfeeding (Kolaczynski et al., 1996a) led
to the hypothesis that leptin signals information about
dietary intake, particularly carbohydrate intake (Jen-
kins et al., 1997). Since then, we have shown that the
diurnal rhythm of leptin depends instead on the
Fig. 13. The 24-h mean insulin, cortisol, glucose and IGF-I
availability of energy and, more specifically, of
binding protein-1 (IGFBP-1) concentrations in a group of
carbohydrate (Hilton and Loucks, 2000). Research regularly menstruating women after 5 days at a balanced
now indicates that leptin is regulated by the tiny flux energy availability of 45 kcal × kg71 FFM × day71 and after 5
of glucose through the hexosamine biosynthesis path- days at a severely low energy availability of 10 kcal × kg71
way (Wang et al., 1998). FFM × day71 (1 kcal = 4.18 kJ).
Nevertheless, single measurements of metabolic
hormones do not reliably identify energy-deficient
individuals, because their normal ranges across the
population are wide compared with the effects of energy balanced energy availability of 45 kcal × kg71
71
deficiency on them. For example, Fig. 12 shows FFM × day and again after 5 days at a severely
substantially overlapping distributions of T3, IGF-I, deficient energy availability of 10 kcal × kg71
71
leptin at 07.00 h and leptin averaged over 24 h in a FFM × day . Such repeated measures reveal the effects
group of regularly menstruating women after 5 days at a of energy deficiency on these hormones, but single
Energy balance and body composition in sports and exercise 11
measurements of the hormones in even such extremely Initially, ketones produced as a byproduct of lipolysis in
energy-deficient individuals still fall within the range of the liver are taken up from the blood and metabolized
energy-balanced individuals, and single measurements by the heart, kidney and skeletal muscle so that
in energy-balanced individuals fall within the range of circulating concentrations in the blood remain low. If
energy-deficient individuals. negative carbohydrate balance continues for only a few
Figure 13 shows that the same is also true for 24-h days, however, ketone utilization by these tissues
mean glucose, 24-h mean IGF-binding protein 1 declines, blood concentrations rise making the ketones
(IGFBP1) and 24-h mean cortisol, although 24-h mean available as an alternative metabolic fuel for the brain,
insulin concentration in severely energy-deficient wo- and the ketones begin to pass through the kidneys into
men displays little overlap with that in energy-balanced the urine. Athletes can purchase ‘keto-sticks’ inexpen-
women. Unfortunately, Fig. 14 shows that 24-h mean sively in most pharmacies to monitor their own urinary
insulin fails to identify less energy-deficient women at ketones at home.
the threshold of reproductive disorders at an energy
availability of 30 kcal × kg71 FFM × day71.
The most convenient indicator of sustained carbohy- Summary
drate deficiency may be urinary ketones. Figure 15
shows the distributions of serum b-hydroxybutyrate and Many athletes, especially female athletes and those who
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urinary aceto-acetate concentrations in the same group participate in endurance and aesthetic sports and sports
of women after 5 days at energy availabilities of 45 and with weight classes, are chronically energy deficient.
10 kcal × kg71 FFM × day71. Both serum and urinary
ketones unambiguously identify such severely energy-
deficient individuals. Figure 16 shows that urinary
ketones identify even less energy-deficient individuals
almost equally reliably at 30 kcal × kg71 FFM × day71.
Urinary aceto-acetate is a better discriminator of energy
deficiency than serum b-hydroxybutyrate, because
ketones are not present in the urine under energy-
balanced conditions.
Ketone concentrations rise when fat stores are
mobilized to substitute for deficient glycogen stores.
Fig. 14. The 24 h mean insulin, cortisol, glucose and IGF-I Fig. 16. Serum b-hydroxybutyrate (bHOB) and urinary
binding protein-1 (IGFBP-1) concentrations in a group of aceto-acetate (U AcAc) concentrations at 07.00 h in a group
regularly menstruating women after 5 days at a balanced of regularly menstruating women after 5 days at a balanced
energy availability of 45 kcal × kg71 FFM × day71 and after 5 energy availability of 45 kcal × kg71 FFM × day71 and after 5
days at a low energy availability of 30 kcal × kg71 FFM × day71 days at a low energy availability of 30 kcal × kg71 FFM × day71
(1 kcal = 4.18 kJ). (1 kcal = 4.18 kJ).
12 Loucks
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