ArticlePDF Available

Low Energy Availability in Athletes: Understanding Undereating and Its Concerns

March 2023
Nutrition Today 58(2):51-57

DOI:10.1097/NT.0000000000000603

Authors:

Megan Kuikman

Australian Catholic University

Louise Mary Burke

Australian Institute of Sport (AIS)

Relative Energy Deficiency in Sport (REDs) is a syndrome of impaired physiological function due to low energy availability (LEA) such that there is insufficient energy intake after subtracting the cost of energy expended through exercise. There are no universal criteria to identify an athlete with REDs. Rather, physiological outcomes and functional impairments that occur because of LEA are used for identification purposes. Once an athlete is identified with REDs, treatment should focus on addressing the underlying cause of LEA. This may include increasing energy intake and/or decreasing exercise energy expenditure as well as addressing factors that may exacerbate LEA. Much has been uncovered about the negative consequences of LEA. Early models were for women, whereas newer models include athletes of both sexes. More research is needed to increase the understanding of LEA so that the model of REDs and best practice guidelines to prevent, identify, and treat REDs will continue to evolve.

Content uploaded by Megan Kuikman

Content may be subject to copyright.

Low Energy Availability in Athletes

Understanding Undereating and Its Concerns

MeganA.Kuikman,MSc

Louise M. Burke, PhD, APD

Relative Energy Deficiency in Sport (REDs) is a syndrome of

impaired physiological function due to low energy avail-

ability (LEA) such that there is insufficient energy intake

after subtracting the cost of energy expended through ex-

ercise. There are no universal criteria to identify an athlete

with REDs. Rather, physiological outcomes and functional

impairments that occur because of LEA are used for identi-

fication purposes. Once an athlete is identified with REDs,

treatment should focus on addressing the underlying cause

of LEA. This may include increasing energy intake and/or

decreasing exercise energy expenditure as well as address-

ing factors that may exacerbate LEA. Much has been un-

covered about the negative consequences of LEA. Early

models were for women, whereas newer models include

athletes of both sexes. More research is needed to increase

the understanding of LEA so that the model of REDs and

best practice guidelines to prevent, identify, and treat

REDs will continue to evolve. Nutr Today 2023;58:51–57

FROM THE FEMALE ATHLETE TRIAD

TO RELATIVE ENERGY DEFICIENCY

IN SPORT

Seminal studies in the 1980s demonstrated that female

athletes with functional hypothalamic amenorrhea—the

absence of menses or irregular menstrual cycles—had

reduced bone mineral density (BMD) compared with

eumenorrheic athletes

and that BMD improved with the

resumption of menses.

Although the cause of menstrual

dysfunction in athletes was unknown and was initially

thought to be associated with eating disorders, this was later

updated to recognize inadequate energy intake resulting

from a variety of causes. Indeed, the term energy availabil-

ity was introduced to sports nutrition,

to reflect the energy

available to support the body's physiological functions by

subtracting the energy expended through exercise from

the athlete's total energy intake.

Energy availability is cal-

culated mathematically from the following calculation:

Energy Availability ¼

Energy Intake Exercise Energy Expenditure

Fat Free Mass

Energy availability differs to energy balance (energy intake

minus total energy expenditure) in that energy balance

represents an output from physiological systems and does

not considerthat physiological systems may be suppressed

by inadequate energy intake, which in turn may decrease

total energy expenditure.

The negative consequences of

low energy availability (LEA) were first described by the fe-

male athlete triad model as an interrelated occurrence of

LEA, impaired bone health, and menstrual dysfunction in

female athletes.

Later, the International Olympic Commit-

tee introduced the expanded model of Relative Energy De-

ficiency in Sport (REDs) as a syndrome of “impaired phys-

iological function including, but not limited to, metabolic

rate, menstrual function, bone health, immunity, protein

synthesis and cardiovascular health”underpinned by

LEA.

The expanded model of REDs was introduced to re-

flect that LEA can have negative outcomes on a larger

range of body systems and is a concern for male athletes

as well as female atheltes.

7,8

Notably, the intention was

not to replace the female athlete triad with REDs but rather

to encompass it within a larger model of potential health

and performance consequences. More recently, the triad

has been updated to include the male athlete.

Figure 1

summarizes the evolution of the various models involving

LEA in sport.

The negative consequences of LEA may

also impact those that do not train for a specific sport, such

as recreational exercisers,

or those with occupations re-

quiring physical work, such as military personnel.

In addition to new insights gained from clinical practice

and sports nutrition research, the 2023 update on REDs is

considering lessons gleaned from the theory of life his-

tory.

This branch of evolutionary science proposes that,

during periods of inadequate food procurement, human

survival is underpinned by the ability to partition energy

supplies to the biological processes that are of critical im-

mediate need.

1–3

Indeed, humans are conditioned to

adapt to periods of LEA by downregulating biological

Megan Kuikman, MSc, is a dietitian. She did her Master of Science at the

University of Guelph. She is now completing her PhD under Louise Burke

at Australian Catholic University.

Louise Burke, PhD, APD, is a sportsdietitian and Chair of Sports Nutrition

in the Mary MacKillop Institute for Health Research at Australia Catholic

University.

The authors have no conflicts of interest to disclose.

Correspondence: Megan A. Kuikman, MSc, Mary MacKillop Institute for

Health Research, Australian Catholic University, Melbourne, Victoria,

Australia 3000 (Megan.Kuikman@myacu.edu.au).

DOI: 10.1097/NT.0000000000000603

1.0 CPEU and 2.0 ANCC Contact Hours

Volume 58, Number 2, March/April 2023 Nutrition Today

Downloaded from http://journals.lww.com/nutritiontodayonline by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsI

Ho4XMi0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC1y0abggQZXdgGj2MwlZLeI= on 04/30/2023

processes that are considered at least temporarily unnec-

essary.

13,14

Some of these perturbations to body systems

might be considered mild and/or transient, representing

adaptive physiological plasticity. Meanwhile, problematic

exposure to LEA, the duration and exposure to which may

vary according to characteristics of the individual and the

body system, leads to the health and performance impair-

ments described in the REDs and triad models.

8,9

IDENTIFYING ATHLETES WITH REDS

Early identification of REDs is critical for preventing the

numerous health and performance consequences of LEA.

Despite LEA being the underlying cause of REDs, directly

calculating an athlete's energy availability is not recom-

mended for identification purposes because of the errors

and methodological challenges of calculating energy in-

take, exercise energy expenditure, and fat-free mass.

10,15

Furthermore, we now recognize that there is no single

threshold for the magnitude/duration of LEA that is associ-

ated with problematic outcomes.

10,15

Rather, validated

tools and/or symptoms of LEA should be used for identifi-

cation purposes. Within the clinical setting, the REDs Clin-

ical Assessment Tool can be used by trained medical pro-

fessionals to assess an athlete's risk of REDs

; an updated

version of this will be released with the 2023 REDs update.

Although only available for use with women, the Low

Energy Availability in Females Questionnaire can also

be used to identify athletes who are at an increased risk

of LEA and require further assessment.

Both of these

tools focus on the biochemical markers and functional

impairments that may occur because of LEA, such as men-

strual dysfunction, reduced or low BMD, and recurring

bone stress injuries. Although physique characteristics

such as low body weight, low levels of body fat, or weight

loss are often identified as being of concern, some athletes

with REDs may have a stable and seemingly “normal”body

mass. A diagnosis (or a failure to diagnose) should never

be assumed solely on body mass and composition. Given

the effects of LEA on various metabolic and endocrine

systems, biochemical markers such as such as testoster-

one (male), triiodothyronine, insulinlike growth factor-1,

cortisol, and others may assist in developing the picture

of REDs.

4,18,19

However, care needs to be taken when

using these markers for diagnostic purposes because they

may be impacted by factors beyond that of LEA, and these

are not always included in routine biochemical assessments.

Table 1 highlights functional impairments, biochemical

markers, and behavioral and psychological changes that

may be used as indicators of LEA. However, there is a need

for further research to identify valid and reliable markers of

energy status, their thresholds for concern, and strategies

to allow differential diagnoses (ie, causes of perturbations

unrelated to REDs).

Take-Home Message: Although LEA

is the underlying cause of REDs, cal-

culations of energy availability should

not be used for identification pur-

poses. Rather, the physiological out-

comes and functional impairments

that occur because of LEA should be

used to identify athletes with REDs.

CAUSES OF LEA

The underlying cause of LEA should be determined in

athletes with REDs because this will guide treatment deci-

sions and the need for a multidisciplinary team. Low energy

availability may be caused by unintentional undereating,

intentional food restriction for performance or health pur-

poses, mismatches between food availability and exercise

commitments, and/or pathological eating and exercise be-

haviors, as highlighted in Figure 2. It is important to note

that LEA and subsequent changes in body composition

and performance may trigger restrictive eating practices

and disordered eating behaviors.

20,21

As such, causes of

LEA should not be assumed to occur in isolation.

Unintentional Undereating

Athletes may unintentionally consume insufficient energy

leading to the inadvertent development of LEA. Possible

FIGURE 1. Overview of the evolution of models related to energy deficiency in athletes.

52 Nutrition Today

Volume 58, Number 2, March/April 2023

Downloaded from http://journals.lww.com/nutritiontodayonline by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsI

Ho4XMi0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC1y0abggQZXdgGj2MwlZLeI= on 04/30/2023

scenarios that may lead to unintentional undereating in-

clude the following

•Increases in training load: Increased exercise energy expendi-

ture does not always lead to a compensatory increase in energy

intake, which may be due to hormonal changes in response to

exercise that suppresses appetite.

•Poor nutrition literacy: Athletes may have poor nutrition knowl-

edge, including lack of knowledge on how to prepare or choose

foods that meet energy requirements.

•Restricted food choices: Athletes who have food intolerances

and allergies, or restrict dietary choices because of religious/

cultural/ethical considerations (eg, vegetarianism/veganism) or

fussy palates, may find it more difficult to meet energy require-

ments from the available food supply. This is particularly seen when

the athlete is outside their usual food environment (eg, travel).

•Small eating windows: Some sports may impede an athlete's

ability to consume sufficient energy. For instance, sports with

lengthy training sessions may restrict the eating window, or ath-

letes may restrict food intake because of concerns that food will

lead to gastrointestinal distress during exercise.

•Mishandled injury: Injured athletes may reduce energy intake

because of perceived reductions in energy needs with a re-

duced training load. Yet, an athlete may actually have increased

energy requirements to support injury repair or because of in-

creased energy expenditure due to ambulation (ie, use of

crutches) or rehabilitation program.

•Travel or other changes to food environment: Traveling for com-

petition or training camps may lead to insufficient energy intake

by interfering with an athlete's normal eating patterns, or foods

that an athlete typically consumes may be unavailable.

•Food insecurity: Athletes may not have the financial resources to

buy foods or easy access to foods that meet energy require-

ments. For instance, athletes may spend large portions of their

day at training facilities where food may be up-priced and/or

only offer food of poor nutritional quality

In the previously mentioned situations, athletes should

work with an accredited sports dietitian to address the fac-

tors leading to insufficient energy intake. This will likely

TABLE 1 Indicators Suggestive of Low

Energy Availability

Functional

impairments

Menstrual dysfunction in women

Low sex drive or lack of morning erectile

function in men

Low bone mineral density or reduced

bone mineral density compared with

previous measurement

Recurring bone stress injuries

Low BMI or body fat levels and/or

substantial weight loss

Reduced body temperature and increased

sensitivity to cold

Gastrointestinal issues such as

constipation or bloating

Biochemical

markers

Decreased: testosterone (male),

triiodothyronine, insulinlike growth factor

1, insulin, leptin, ferritin

Increased: growth hormone, cortisol,

LDL cholesterol

Behavioral

changes

Restrictive eating behaviors such as

cutting out food groups or

measuring foods

Avoiding food-related social activities and

secretive behavior regarding food intake

and/or exercise

Additional training above what is

required and/or inability to take rest days

Psychological

changes

Becoming withdrawn and reclusive

Anxiety, irritability, and difficulties

concentrating

Body image dissatisfaction and

distortion

Abbreviations: BMI, body mass index. LDL, low-density lipoprotein.

FIGURE 2. Low energy availability may occur in a range of scenarios in which there is a decrease in energy intake and/or an increase in exercise

energy expenditure.

Volume 58, Number 2, March/April 2023 Nutrition Today

Downloaded from http://journals.lww.com/nutritiontodayonline by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsI

Ho4XMi0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC1y0abggQZXdgGj2MwlZLeI= on 04/30/2023

include education to increase an athlete's nutrition knowl-

edge and food literacy, and the creation of personalized

food plans that take into consideration an athlete's food

preferences, unique training situation, and budget. The

sports dietitian may also need to work alongside an

athlete's coach and support team to implement targeted

strategies to increase energy intake, such as making foods

that an athlete finds appealing more readily available.

Intentional Food Restriction

Some athletes may restrict food intake with the intention

to manipulate body composition for performance and/or

health purposes and, in the process, develop LEA. This

may be particularly prevalent for sports where a low body

mass and/or body fat level may offer a performance ad-

vantage, such as the following

•Gravitational sports: long-distance running, road and mounting

cycling, ski jumping, jumping in athletics

•Weight division sports: wrestling, lightweight rowing, judo, boxing

•Aesthetically judged sports: figure skating, diving, gymnastics,

synchronized swimming, body building

Athletes seeking to manipulate body composition for

performance and/or health purposes should work with

an accredited sports dietitian to ensure that targeted weight

goals are appropriate and nutritional strategies implemented

do not compromise long-term health.

Eating Disorders or Disordered Eating

It is commonly accepted that the energy restriction due to

an underlying eating disorder or disordered eating can lead

to the development of LEA.

Whereas an eating disorder

meets the diagnostic criteria according to the Diagnostic

and Statistical Manual of Mental Disorders, Fifth Edition,

disordered eating is problematic eating behaviors that fail

to meet these diagnostic criteria.

Disordered eating is more

prevalent than clinical eating disorders and includes path-

ogenic behaviors to control weight, preoccupation with

“healthy”eating, and/or a cognitive focus on burning cal-

ories when exercising.

Although eating disorders and

disordered eating are also a concern for male athletes, es-

pecially those competing in weight-sensitive sports,

the

relationship between disordered eating and LEA has not

been thoroughly examined in male athletes. Clearly, this

is an area that needs further research.

Unanswered Increase in Exercise Volume

Most athletes undertake a periodized training program

that includes periods of intensified exercise. Although this

may be tolerated, when short-lived and supported by a

change in dietary intake, some athletes are either unaware

of their new energy requirements or unable able to access

additional food in their environment. This is often the case

when the athlete travels to specialized training camps/

competition where there is a change in their food avail-

ability (eg, limited catering or financial limits). It may also

occur when the athlete moves to a new training squad or

increases their sporting commitment and is unaware of

new nutritional needs and/or does not experience a com-

mensurate change in appetite.

Pathological Exercise Behaviors

Pathological exercise behaviors, such as compulsive exer-

cise or exercise dependence, can also contribute to the

development of LEA. The terms compulsive exercise and

exercise dependence are often used interchangeably de-

spite differences in these behaviors. Compulsive exercise

represents an urge to perform exercise with the intent to

escape the anxiety that arises from the imagined negative

consequences of not exercising, whereas with exercise

dependence, exercise is an addictive behavior that is in-

trinsically motivated through an influence on positive

affect.

Both exercise dependence and compulsive exer-

cise commonly occur secondary to disordered eating such

that exercise is being used as a way to control weight.

Although there is evidence that problematic exercise be-

haviors may lead to the development of LEA,

29,30

few

studies have looked at the role of pathological exercise

behaviors independent of an eating disorder or disor-

dered eating in the development of LEA. One study found

that, for both male and female athletes, only when exer-

cise dependence was secondary to disordered eating

was an increased risk of LEA and associated health out-

comes seen.

Furthermore, athletes with both exercise de-

pendence and disordered eating were at an even greater

risk of LEA and associated health outcomes compared with

athletes with disordered eating in isolation.

As such,

when determining underlying causes of LEA in athletes,

both an athlete's relationship with food and exercise must

be assessed for pathological behaviors.

Take-Home Message: There are mul-

tiple causes of LEA in athletes that

may co-occur. These include inten-

tional undereating, unintentional un-

dereating, or pathological eating and

exercise behaviors. Identifying un-

derlying causes of LEA is essential for

implementing treatment strategies.

TREATMENT STRATEGIES

Given that LEA is the underlying cause of REDs, treatment

must correct LEA. However, because of the substantial

54 Nutrition Today

Volume 58, Number 2, March/April 2023

Downloaded from http://journals.lww.com/nutritiontodayonline by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsI

Ho4XMi0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC1y0abggQZXdgGj2MwlZLeI= on 04/30/2023

error involved with calculating energy availability and the

lack of a validated threshold that is considered “optimal”

for athletes, treatment should not be aiming to achieve a

specific threshold of energy availability.

Rather, treat-

ment should focus more broadly on increasing energy in-

take and/or reducing exercise energy expenditure.

This

includes implementing strategies targeting the underlying

cause of inadequate energy intake or excessive energy ex-

penditure, as highlighted previously. However, beyond in-

creasing energy availability, treatment strategies may also

target factors that exacerbate and/or independently affect

the health outcomes of LEA.

This may include minimiz-

ing within-day energy deficiency, avoiding periods of low

carbohydrate availability, reducing fiber intake, and ensur-

ing adequate intake of bone-building nutrients.

Exam-

ples of these interventions and proposed mechanisms of

action are highlighted in Table 2. In addition to these nutri-

tional interventions, athletes with compromised bone health

may also consider including mechanical bone stress, such

as strength or resistance exercise, within their training pro-

gram to increase BMD.

Replacing energetically demand-

ing aerobic exercise sessions with less energetically de-

manding strength or resistance training sessions may also

aid in the recovery process by decreasing exercise energy

expenditure and, in turn, increasing energy availability.

Finally, athletes may benefit from the inclusion of therapy,

such as cognitive behavioral therapy, to address psycho-

genic stress that may be contributing to LEA and to assist

athletes in making behavioral changes.

Treatment will of-

ten require a multidisciplinary team of health professionals

with ongoing follow-up to ensure progress is being made.

Take-Home Message: Just as calculat-

ing energy availability should not be

used for diagnostic purposes, achiev-

ing a specific threshold of energy

availability should not be the goal of

REDs treatment. Rather, treatment

should focus on more broadly in-

creasing energy intake and/or de-

creasing training load, and may also

include interventions aimed at exac-

erbating factors of LEA.

TABLE 2 Nutritional Interventions for Treatment of REDs Aimed at Factors That

Exacerbate Low Energy Availability

Exacerbating Factor Mechanism Nutrition Intervention

Within-day energy

deficiency

The more time over 24 h spent in a negative energy

deficit is associated with markers of LEA.

Consume adequate energy around exercise

Consume breakfast upon waking, and a meal or

snack every 3-5 h

Low carbohydrate

availability

Low carbohydrate availability may impair bone

turnover and immune system function

independent of energy availability.

Consumption of carbohydrates over isoenergetic

amounts of fat results in higher levels of leptin, which

plays a critical role in the function of the HPG axis.

Ensure overall daily carbohydrate requirements are

being met

Ensure adequate carbohydrate intake before,

during, and after exercise

Undertake specific sessions of training with low

glycogen/overnight fasting with care and only

when properly integrated into a periodized

training program

Excessive fiber intake High-fiber diet may increase satiety, making it

difficult to meet energy requirements.

Excessive fiber intake may reduce estrogen

reabsorption and contribute to menstrual dysfunction.

Consider replacing high-fiber foods with lower

fiber options

Limit the consumption of high-fiber foods at meals

that may be displacing more energy-dense

food options

Inadequate intake of

bone-building nutrients

Independent of energy availability may

compromise bone health.

Ensure adequate intake of nutrients important for

bone health

Consider having the vitamin D status of an

athlete assessed

If insufficient intake of bone-building nutrients in

diet, consider supplementation

Abbreviations: HPG, hypothalamic-pituitary-gonadal; LEA, low energy availability; REDs, Relative Energy Deficiency in Sport.

Volume 58, Number 2, March/April 2023 Nutrition Today

Downloaded from http://journals.lww.com/nutritiontodayonline by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsI

Ho4XMi0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC1y0abggQZXdgGj2MwlZLeI= on 04/30/2023

PREVENTION

Creating a healthy sport culture that maintains athletes'

physical and mental health is critical for the prevention of

REDs. This involves increasing awareness of REDs through

education to all involved in athlete care, such as coaches,

trainers, and parents, and having a zero-tolerance policy

for toxic training environments or practices that include

body shaming, overexercising, and underfuelling.

Creat-

ing a healthy sport culture may involve coaches focusing

on enhancing athletic performance via nondieting strate-

gies such as mental approaches, selecting team captains

who have a healthy relationship with food and their body,

and deemphasizing talk centered around body weight,

food restriction, and/or dieting.

Finally, coaches should

not be involved in assessing the body composition of ath-

letes, but rather, athletes who express a desire to change

body composition should be referred to a sports dietitian

who can ensure that safe nutrition changes are made.

Take-Home Message: To prevent

REDs, all involved in athlete care

are responsible for creating a healthy

sport culture that ensures athlete

health is the top priority.

CONCLUSION AND FUTURE DIRECTION

Much has been uncovered about the implications of LEA

on athlete health and performance over the past 40 years.

Low energy availability must be taken seriously given

the health and performance consequences that could ulti-

mately derail an athlete's career. Despite the considerable

research advances within this area, much more is still

needed. In particular, research is needed that will lead to

a better understanding of the impact of LEA in male ath-

letes and how this differs from female athletes, as well as

research that will lead to valid and reliable markers of

LEA that can be used for identification purposes. As the

understanding of LEA continues to evolve, so will the

model of REDs, and best practice guidelines for identifica-

tion, treatment, and prevention.

Acknowledgments

We acknowledge support of this work by the Wu Tsai Human

Performance Alliance and the Joe and Clara Tsai Foundation.

REFERENCES

1. Drinkwater BL, Nilson K, Chesnut CH 3rd, Bremner WJ, Shainholtz

S, Southworth MB. Bone mineral content of amenorrheic and

eumenorrheic athletes. N Engl J Med. 1984;311:277–281.

2. Drinkwater BL, Nilson K, Ott S, Chesnut CH III. Bone mineral

density after resumption of menses in amenorrheic athletes.

JAMA. 1986;256(3):380–382.

3. Loucks AB, Verdun M, Heath EM. Low energy availability, not

stress of exercise, alters LH pulsatility in exercising women.

J Appl Physiol. 1998;84(1):37–46.

4. Areta JL, Taylor HL, Koehler K. Low energy availability: history,

definition and evidence of its endocrine, metabolic and physio-

logical effects in prospective studies in females and males. Eur J

Appl Physiol. 2021;121(1):1–21.

5. Loucks AB, Kiens B, Wright HH. Energy availability in athletes.

JSportsSci. 2011;29(suppl 1):S7–S15.

6. Otis CL, Drinkwater B, Johnson M,Loucks A, Wilmore J. ACSM

position stand: the female athlete triad. Med Sci Sport Exerc.1997;

29(5):i–ix.

7. Mountjoy M, Sundgot-Borgen J, Burke L, et al. The IOC consen-

sus statement: beyond the female athlete triad—relative energy

deficiency in sport (RED-S). Br J Sports Med. 2014;48(7):491–497.

8. Mountjoy M, Sundgot-Borgen JK, Burke LM, et al. IOC consen-

sus statement on relative energy deficiency in sport (RED-S): 2018

update. Br J Sports Med. 2018;52(11):687–697.

9. Nattiv A, De Souza MJ, Koltun KJ, et al. The male athlete triad—a

consensus statement from the female and male athlete triad coa-

lition part 1: definition and scientific basis. Clin J Sport Med.2021;

31(4):335–348.

10. Burke L, Fahrenholtz I, Garthe I, Lundy B, Melin A. Low energy

availability: challenges and approaches to measurement and

treatment. In: Burke L, Deakin V, Minehan M, eds. Clincal Sports

Nutrition. 6th ed. Sydney, Australia: McGraw Hill Education; 2021.

11. Slater J, McLay-Cooke R, Brown R, Black K. Female recreational

exercisers at risk for low energy availability. Int J Sport Nutr Exerc

Metab. 2016;26(5):421–427.

12. Edwards VC, Myers SD, Wardle SL, et al. Nutrition and physical

activity during british army officer cadet training: part 1—energy

balance and energy availability. Int J Sport Nutr Exerc Metab.

2022;32(3):204–213.

13. Shirley MK, Longman DP, Elliott-Sale KJ, Hackney AC, Sale C,

Dolan E. A life history perspective on athletes with low energy

availability. Sports Med. 2022;52(6):1223–1234.

14. Pontzer H. Energy constraint as a novel mechanism linking exer-

cise and health. Phys Ther. 2018;33(6):384–393.

15. Burke LM, Lundy B, Fahrenholtz IL, Melin AK. Pitfalls of conducting

and interpreting estimates of energy availability in free-living athletes.

IntJSportNutrExercMetab. 2018;28(4):350–363.

16. Mountjoy M, Sundgot-Borgen J, Burke L, et al. RED-S CAT. Rel-

ative Energy Deficiency in Sport (RED-S) Clinical Assessment

Tool (CAT). Br J Sports Med. 2015;49(7):421–423.

17. Melin A, Tornberg ÅB, Skouby S, et al. The LEAFquestionnaire:

a screening tool for the identification of female athletes at risk for

the female athlete triad. Br J Sports Med. 2014;48(7):540–545.

18. McCall LM, Ackerman KE. Endocrine and metabolic repercus-

sions of relative energy deficiency in sport. Curr Opin Endocr

Metab Res. 2019;9:56–65.

19. Elliott-Sale KJ, Tenforde AS, Parziale AL, Holtzman B, Ackerman

KE. Endocrine effects of relative energy deficiency in sport. Int J

Sport Nutr Exerc Metab. 2018;28(4):335–349.

20. Langbein RK, Martin D, Allen-Collinson J,Crust L, Jackman PC.

“I'd got self-destruction down to a fine art”: a qualitative explora-

tion of relative energy deficiency in sport (RED-S) in endurance

athletes. JSportsSci. 2021;39(14):1555–1564.

21. Sundgot-Borgen J. Risk and trigger factors for the development of

eating disorders in female elite athletes. Med Sci Sports Exerc.

1994;26(4):414–419.

22. Sundgot-Borgen J, Meyer NL, Lohman TG, et al. How to mini-

mise the health risks to athletes who compete in weight-sensitive

sports review and position statement on behalf of the Ad Hoc

Research Working Group on Body Composition, Health and

56 Nutrition Today

Volume 58, Number 2, March/April 2023

Downloaded from http://journals.lww.com/nutritiontodayonline by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsI

Ho4XMi0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC1y0abggQZXdgGj2MwlZLeI= on 04/30/2023

Performance, under the auspices of the IOC Medical Commis-

sion. Br J Sports Med. 2013;47(16):1012–1022.

23. Wells KR, Jeacocke NA, Appaneal R, et al. The Australian Insti-

tute of Sport (AIS) and National Eating Disorders Collaboration

(NEDC) position statement on disordered eating in high perfor-

mance sport. Br J Sports Med. 2020;54(21):1247–1258.

24. American Psychiatric Association. Diagnostic and Statistical Manual

of Mental Disorders. 5th ed. Arlington, VA: American Psychiatric

Association; 2013.

25. Reardon CL, Hainline B, Aron CM, et al. Mental health in elite

athletes: International Olympic Committee consensus statement

(2019). Br J Sports Med. 2019;53(11):667–699.

26. Karrer Y, Halioua R, Mötteli S, et al. Disordered eating and eating

disorders in male elite athletes: a scoping review. BMJ Open Sport

Exerc Med. 2020;6(1):e000801.

27. Cook B, Hausenblas H, Freimuth M. Exercise addiction and

compulsive exercising: relationship to eating disorders, substance

use disorders, and addictive disorders. In: Brewerton TD, Dennis

AB, eds. Eating Disorders, Addictions and Substance Use Disorders.

New York, NY: Springer-Verlag Berlin Heidelberg; 2014:127–144.

28. Trott M, Jackson SE, Firth J, et al. A comparative meta-analysis of

the prevalence of exercise addiction in adults with and without

indicated eating disorders. Eat Weight Disord. 2021;26(1):37–46.

29. Torstveit MK, Fahrenholtz IL, Lichtenstein MB, Stenqvist TB,

Melin AK. Exercise dependence, eating disorder symptoms and

biomarkers of Relative Energy Deficiency in Sports (RED-S)

among male endurance athletes. BMJ Open Sport Exerc Med.

2019;5(1):e000439.

30. Lichtenstein MB, Andries A, Hansen S, Frystyk J, Stoving RK.

Exercise addiction in men is associated with lower fat-adjusted

leptin levels. Clin J Sport Med. 2015;25(2):138–143.

31. Kuikman MA, Mountjoy M, Burr JF. Examining the relationship

between exercise dependence, disordered eating, and low en-

ergy availability. Nutrients. 2021;13(8):2601.

32. Kuikman MA, Mountjoy M, Stellingwerff T, Burr JF. A review of

nonpharmacological strategies in the treatment of relative energy

deficiency in sport. Int J Sport Nutr Exerc Metab. 2021;31(3):

268–275.

33. Hooper DR. The application of heavy strength training in rel-

ative energy deficiency in sport. J Sci Sport Exerc. 2019;1(3):

195–202.

34. Jetté M, Sidney K, Blümchen G. Metabolic equivalents (METS) in

exercise testing, exercise prescription, and evaluation of func-

tional capacity. Clin Cardiol. 1990;13(8):555–565.

35. Ackerman KE, Stellingwerff T, Elliott-Sale KJ, et al. #REDS (Rel-

ative Energy Deficiency in Sport): time for a revolution in sports

culture and systems to improve athlete health and performance.

Br J Sports Med. 2020;54(7):369–370.

36. Sundgot-Borgen J, Garthe I. Elite athletes in aesthetic and Olym-

pic weight-class sports and the challenge of body weight and

body compositions. JSportsSci. 2011;29(suppl 1):S101–S114.

For more than 83 additional continuing education articles related to Nutrition topics, go to NursingCenter.com/CE.

Nursin

Continuin

Professional Develo

men

INSTRUCTIONS

Low Energy Availability in Athletes: Understanding Undereating and Its Concerns

TEST INSTRUCTIONS

•Read the article. The test for this nursing continuing professional

development (NCPD) activity is to be taken online at www.nursingcenter.

com/CE. Tests can no longer be mailed or faxed.

•You'll need to create an account (it's free!) and log in to access My

Planner before taking online tests. Your planner will keep track of all your

Lippincott Professional Development online NCPD activities for you.

•There's only one correct answer for each question. A passing score for

this test is 7 correct answers. If you pass, you can print your certificate

of earned contact hours and access the answer key. If you fail, you have

the option of taking the test again at no additional cost.

•For questions, contact Lippincott Professional Development:

1-800-787-8985.

•Registration deadline is March 1, 2026

CONTINUING EDUCATION INFORMATION FOR REGISTERED DIETICIANS

AND DIETE TIC TECHNICIANS, REGISTE RED:

The test for this activity for dietetic professionals is located online at

http://alliedhealth.ceconnection.com. Lippincott Professional Development

(LPD) is a Continuing Professional Education (CPE) Accredited Provider

with the Commission on Dietetic Registration (CDR), provider

number LI001. Registered dietitians (RDs) will receive

1.0 continuing professional education units (CPEUs)

for successful completion of this program/material,

CPE Level 2. Dietetics practitioners may submit evaluations

of the quality of programs/materials on the CDR website:

www.cdrnet.org. LPD is approved as a provider of continuing

education for the Florida Council for Dietetics and Nutrition,

CE Broker # 50-1223.

PROVIDER ACCREDITATION

Lippincott Professional Development will award 2.0 contact hours for this

nursing continuing professional development activity.

Lippincott Professional Development is accredited as a provider of

nursing continuing professional development by the American Nurses

Credentialing Center's Commission on Accreditation.

This activity is also provider approved by the California Board of

Registered Nursing, Provider Number CEP 11749 for 2.0 contact hours.

Lippincott Professional Development is also an approved provider of

continuing nursing education by the District of Columbia, Georgia, West

Virginia, New Mexico, South Carolina, and Florida, CE Broker #50-1223.

Your certificate is valid in all states.

Payment: The registration fee for this test is $21.95.

Disclosure Statement: The author and planners have disclosed no

potential relevant financial relationships or otherwise.

Volume 58, Number 2, March/April 2023 Nutrition Today

Downloaded from http://journals.lww.com/nutritiontodayonline by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsI

Ho4XMi0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC1y0abggQZXdgGj2MwlZLeI= on 04/30/2023

Resting Metabolic Rate and Substrate Utilization during Energy and Protein Availability in Male and Female Athletes

Article

Full-text available

Mar 2024

Active athletes frequently develop low energy (LEA) and protein availabilities (LPA) with consequent changes in the vital metabolic processes, especially resting metabolic rate (RMR) and substrate utilization. This study investigated the association of energy and protein intakes with RMR and substrate utilization in male and female athletes and those with LEA and LPA. Sixty athletes (35% female, 26.83 ± 7.12 y) were enrolled in this study. Anthropometric measurements and body composition analysis were reported to estimate fat-free mass (eFFM). Dietary intakes were recorded by two-day multiple-pass 24 h recall records and three-day food records and then analyzed by food processor software to calculate protein intake (PI) and energy intake (EI). Indirect calorimetry was used to measure RMR and percentages of substrate utilization. Activity–energy expenditure (AEE) was assessed by using an Actighrphy sensor for three days. Energy availability was calculated using the following formula (EA = EI − AEE/eFFM). The correlation of EI and PI with RMR and substrate utilization was tested with Pearson correlation. In the LEA group, both EI and PI correlated positively with RMR (r = 0.308, 0.355, respectively, p < 0.05). In addition, EI showed a positive correlation with the percentage of fat utilization. In the male and sufficient-PA groups, PI correlated positively with the RMR and negatively with the percentage of protein utilization. In conclusion, the percentage of LEA is markedly prevalent in our sample, with a higher prevalence among males. Athletes with LEA had lower fat utilization and lower RMR, while those with sufficient PA showed lower protein utilization with excessive PI. These findings may explain the metabolic responses in the cases of LEA and LPA.

Nutrition and Physical Activity During British Army Officer Cadet Training: Part 1-Energy Balance and Energy Availability

Article

Full-text available

Apr 2022
INT J SPORT NUTR EXE

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.

A Life History Perspective on Athletes with Low Energy Availability

Article

Full-text available

Jun 2022
SPORTS MED

The energy costs of athletic training can be substantial, and deficits arising from costs unmet by adequate energy intake, leading to a state of low energy availability, may adversely impact athlete health and performance. Life history theory is a branch of evolutionary theory that recognizes that the way the body uses energy-and responds to low energy availability-is an evolved trait. Energy is a finite resource that must be distributed throughout the body to simultaneously fuel all biological processes. When energy availability is low, insufficient energy may be available to equally support all processes. As energy used for one function cannot be used for others, energetic "trade-offs" will arise. Biological processes offering the greatest immediate survival value will be protected, even if this results in energy being diverted away from others, potentially leading to their downregulation. Athletes with low energy availability provide a useful model for anthropologists investigating the biological trade-offs that occur when energy is scarce, while the broader conceptual framework provided by life history theory may be useful to sport and exercise researchers who investigate the influence of low energy availability on athlete health and performance. The goals of this review are: (1) to describe the core tenets of life history theory; (2) consider trade-offs that might occur in athletes with low energy availability in the context of four broad biological areas: reproduction, somatic maintenance , growth, and immunity; and (3) use this evolutionary perspective to consider potential directions for future research.

Examining the Relationship between Exercise Dependence, Disordered Eating, and Low Energy Availability

Article

Full-text available

Jul 2021

Both dietary and exercise behaviors need to be considered when examining underlying causes of low energy availability (LEA). The study assessed if exercise dependence is independently related to the risk of LEA with consideration of disordered eating and athlete calibre. Via survey response, female (n = 642) and male (n = 257) athletes were categorized by risk of: disordered eating, exercise dependence, disordered eating and exercise dependence, or if not presenting with disordered eating or exercise dependence as controls. Compared to female controls, the likelihood of being at risk of LEA was 2.5 times for female athletes with disordered eating and >5.5 times with combined disordered eating and exercise dependence. Male athletes with disordered eating, with or without exercise dependence, were more likely to report signs and symptoms compared to male controls-including suppression of morning erections (OR = 3.4; p < 0.0001), increased gas and bloating (OR = 4.0–5.2; p < 0.002) and were more likely to report a previous bone stress fracture (OR = 2.4; p = 0.01) and ≥22 missed training days due to overload injuries (OR = 5.7; p = 0.02). For both males and females, in the absence of disordered eating, athletes with exercise dependence were not at an increased risk of LEA or associated health outcomes. Compared to recreational athletes, female and male international caliber and male national calibre athletes were less likely to be classified with disordered eating.

The Male Athlete Triad—A Consensus Statement From the Female and Male Athlete Triad Coalition Part 1: Definition and Scientific Basis

Article

Full-text available

Jun 2021
CLIN J SPORT MED

Objective Investigate the reliability of concussion symptoms captured through ecological momentary assessment (EMA) and compare time with recovery based on 3 definitions of symptomatic recovery and the date of clinical clearance to begin the return-to-play (RTP) process. Design We used a mobile app with EMA to monitor concussion symptoms as part of a multicenter randomized controlled trial. Setting Three sports medicine practices. Participants Patients between 13 and 18 years old with sport-related concussion were prompted to complete the Post-Concussion Symptom Inventory daily over 4 weeks. Interventions None. Main Outcome Measures We compared the elapsed days to reaching the 4 outcomes using scatterplots and Kaplan–Meier curves. Results Among 118 participants, symptoms reported into the app had excellent agreement with symptoms reported at a clinical visit on the same day (intraclass correlation coefficient = 0.97). Most (>50%) participants reached “specific symptom return to preinjury levels,” “overall symptom return to preinjury levels,” and “current symptom resolution” based on EMA symptom reports between several days and 1 week before achieving “clinical clearance to RTP” determined at a clinical visit, which had 100% sensitivity, but between 56.3% and 78.1% specificity, relative to the app-measured symptom outcomes. Conclusions Time until symptom recovery varies based on the chosen definition of symptomatic recovery but is a more precise correlate with clinical clearance to begin the RTP process when defining symptom recovery as a return to a preinjury baseline level of symptomatology. Real-time symptom monitoring may be beneficial clinically, allowing providers to assess patients' recovery status and make more timely and remote treatment recommendations.

"I'd got self-destruction down to a fine art": a qualitative exploration of relative energy deficiency in sport (RED-S) in endurance athletes

Article

Full-text available

Feb 2021

Relative Energy Deficiency in Sport (RED-S) is a syndrome of impaired health and performance that occurs as a result of low energy availability (LEA). Whilst many health effects associated with RED-S have been widely studied from a physiological perspective, further research exploring the psychological antecedents and consequences of the syndrome is required. Therefore, the aim of this study was to qualitatively explore athlete experiences of RED-S. Twelve endurance athletes (female n= 10, male n= 2; M age = 28.33 years) reporting past or current experiences of RED-S, associated with periods of LEA, took part in semi-structured interviews designed to explore: contexts and mechanisms underpinning the onset of RED-S; the subjective experience of RED-S; and contexts and mechanisms influencing “recovery” from RED-S. Regardless of how RED-S was initiated, all athletes experienced a multitude of physiological impairments, accompanied by significant psychological distress. This paper contributes novel understanding of the complex interplay between physiological and psychological components of RED-S from the perspective of information-rich cases. The findings suggest that system-wide educational prevention and awareness interventions are vital for athletes and support personnel, such as coaches, parents, dieticians, psychologists, and sports medicine staff.

A Review of Nonpharmacological Strategies in the Treatment of Relative Energy Deficiency in Sport

Article

Full-text available

Jan 2020

Relative energy deficiency in sport (RED-S) can result in negative health and performance outcomes in both male and female athletes. The underlying etiology of RED-S is low energy availability (LEA), which occurs when there is insufficient dietary energy intake to meet exercise energy expenditure, corrected for fat-free mass, leaving inadequate energy available to ensure homeostasis and adequate energy turnover (optimize normal bodily functions to positively impact health), but also optimizing recovery, training adaptations, and performance. As such, treatment of RED-S involves increasing energy intake and/or decreasing exercise energy expenditure to address the underlying LEA. Clinically, however, the time burden and methodological errors associated with the quantification of energy intake, exercise energy expenditure, and fat-free mass to assess energy availability in free-living conditions make it difficult for the practitioner to implement in everyday practice. Furthermore, interpretation is complicated by the lack of validated energy availability thresholds, which can result in compromised health and performance outcomes in male and female athletes across various stages of maturation, ethnic races, and different types of sports. This narrative review focuses on pragmatic nonpharmacological strategies in the treatment of RED-S, featuring factors such as low carbohydrate availability, within-day prolonged periods of LEA, insufficient intake of bone-building nutrients, lack of mechanical bone stress, and/or psychogenic stress. This includes the implementation of strategies that address exacerbating factors of LEA, as well as novel treatment methods and underlying mechanisms of action, while highlighting areas of further research.

Disordered eating and eating disorders in male elite athletes: a scoping review

Article

Full-text available

Oct 2020

Background Eating disorders (ED) and disordered eating (DE) among male elite athletes share some of the characteristics seen in female elite athletes and the population, but also exhibit some key differences. Objective Scoping review of ED and DE in male elite athletes. Methods In May 2020, a comprehensive systematic literature search was conducted for DE and ED in male elite athletes. Results We identified 80 studies which included 47 uncontrolled, 14 controlled studies, one interventional trial and 18 reviews. Discussion There was a wide range of definitions of DE and a high level of heterogeneity regarding competitive level, age and sport type. In adult male elite athletes, ED prevalence rates up to 32.5% were found, higher than in the general population. Prevalence was not higher in young/adolescent male elite athletes. The most frequently associated factor was competing in weight-sensitive sports. Male elite athletes tended to exhibit less body dissatisfaction than controls and were not always associated with DE. There were no studies looking at the prognosis or reporting an evidence-based approach for the management of DE in male elite athletes. Conclusion Existing literature indicates high prevalence of DE and ED in male elite athletes, with a wide range of aetiopathogenesis. There is a need for longitudinal studies to characterise the pathology and long-term outcomes, as well as develop standardised tools for assessment and treatments.

Low energy availability: history, definition and evidence of its endocrine, metabolic and physiological effects in prospective studies in females and males

Article

Full-text available

Jan 2021
EUR J APPL PHYSIOL

Energy availability (EA) is defined as the amount of dietary energy available to sustain physiological function after subtracting the energetic cost of exercise. Insufficient EA due to increased exercise, reduced energy intake, or a combination of both, is a potent disruptor of the endocrine milieu. As such, EA is conceived as a key etiological factor underlying a plethora of physiological dysregulations described in the female athlete triad, its male counterpart and the Relative Energy Deficiency in Sport models. Originally developed upon female-specific physiological responses, this concept has recently been extended to males, where experimental evidence is limited. The majority of data for all these models are from cross-sectional or observational studies where hypothesized chronic low energy availability (LEA) is linked to physiological maladaptation. However, the body of evidence determining causal effects of LEA on endocrine, and physiological function through prospective studies manipulating EA is comparatively small, with interventions typically lasting ≤ 5 days. Extending laboratory-based findings to the field requires recognition of the strengths and limitations of current knowledge. To aid this, this review will: (1) provide a brief historical overview of the origin of the concept in mammalian ecology through its evolution of algebraic calculations used in humans today, (2) Outline key differences from the ‘energy balance’ concept, (3) summarise and critically evaluate the effects of LEA on tissues/systems for which we now have evidence, namely: hormonal milieu, reproductive system endocrinology, bone metabolism and skeletal muscle; and finally (4) provide perspectives and suggestions for research upon identified knowledge gaps.

The Australian Institute of Sport (AIS) and National Eating Disorders Collaboration (NEDC) position statement on disordered eating in high performance sport

Article

Full-text available

Jul 2020

Identification, evaluation and management of disordered eating (DE) is complex. DE exists along the spectrum from optimised nutrition through to clinical eating disorders (EDs). Individual athletes can move back and forth along the spectrum of eating behaviour at any point in time over their career and within different stages of a training cycle. Athletes are more likely to present with DE than a clinical ED. Overall, there is a higher prevalence of DE and EDs in athletes compared with non-athletes. Additionally, athletes participating in aesthetic, gravitational and weight-class sports are at higher risk of DE and EDs than those in sports without these characteristics. The evaluation and management of DE requires a cohesive team of professional practitioners consisting of, at minimum, a doctor, a sports dietitian and a psychologist, termed within this statement as the core multidisciplinary team. The Australian Institute of Sport and the National Eating Disorders Collaboration have collaborated to provide this position statement, containing guidelines for athletes, coaches, support staff, clinicians and sporting organisations. The guidelines support the prevention and early identification of DE, and promote timely intervention to optimise nutrition for performance in a safe, supported, purposeful and individualised manner. This position statement is a call to action to all involved in sport to be aware of poor self-image and poor body image among athletes. The practical recommendations should guide the clinical management of DE in high performance sport.

#REDS (Relative Energy Deficiency in Sport): time for a revolution in sports culture and systems to improve athlete health and performance

Article

Full-text available