Key words
young athlete - low energy availability - exercise - bone health
Search Strategy
Medline, SPORTDiscus and CINAHL databases were searched from 1 January 2016 to 8 June
2021 and included all study designs and was limited to English language. The search
was based around the terms ([adolescent OR young adult OR student OR teen OR child
OR minor OR youth] AND [relative energy deficienc* OR RED-S OR REDS OR
female athlete triad OR male athlete triad OR energy intake deficienc* OR
low energy availability OR bone density OR ((bone or skelet*) AND (mass OR
health OR density OR metabolism)). 759 unique articles were identified, and all were
assessed for relevance to this narrative review. References of included papers were
also assessed for other relevant papers.
Introduction
Relative energy deficiency in sport (RED-S)
The International Olympic Committee (IOC) defined RED-S as a syndrome of health
and performance impairments resulting from an energy deficit [1]. Previously, the limited definition of the
female athlete triad, consisting of low energy availability (in early literature
limited to anorexia), osteoporosis and amenorrhoea, restricted the
identification of the multi-system problems and presentations that can arise
from a consistent negative energy balance. Importantly, it also did not address
the occurrence within males. RED-S has achieved greater recognition in recent
years since the original IOC consensus statement and subsequent update [1]
[2]. A consensus
statement for male athletes (the male athlete triad) has also been produced
[3]
[4]. The full
RED-S syndrome is now recognised as encompassing effects on metabolic rate,
menstrual, bone, cardiovascular and gastroenterological health, immunity and
mental well-being.
Low energy availability (LEA)
LEA is the foundation for development of RED-S. It occurs when there is
insufficient energy available for optimum health and to support sport
performance, after exercise energy expenditure (EEE) is subtracted from the
total energy intake (EI) and normalized to fat free mass (FFM)
[5]. LEA has been
defined as<30 kcal/kg/FFM/day, with
optimal energy availability thought to be
45 kcal/kg/FFM/day, however there is significant
individual variability [6]. Studying energy
availability has many practical difficulties, there is no standardized way of
measuring EA outside of the laboratory setting [7]. Energy intake can be estimated from dietary records (typically done
over three to seven days) and exercise energy expenditure from activity records,
heart rate and/or accelerometry (for example wearable devices), however,
under- or over-estimates can arise from inaccuracies in both self reporting and
accelerometry data. FFM can be estimated by skin fold measurement or
bio-electrical impedance analysis. Dual-energy X-ray absorptiometry (DXA) is
considered a more accurate estimate of FFM [7] but
may not be available to measure FFM alone in the clinical setting.
Most published research in this area relates to adult females, rather than adult
males or the adolescent population specifically. However, during adolescence,
nutritional requirements are probably at their greatest compared to any other
stage of life [8]. Adolescent metabolism
encompasses the energy cost of growth, basal metabolic rate and
active/exercise energy expenditure. If the total energy intake falls
below the threshold of requirement it may cause growth stunting, pubertal delay
and affect bone mass accrual. The calorie requirements for adolescent males are
higher than for females to fulfill the higher rate of growth and increased lean
body mass [8]. Emerging evidence suggests that in
males, greater energy restriction is required to cause compensatory metabolic
adaptations to this energy deficit [3].
Physical activity in adolescence
Adolescence is the time of development spanning the onset of puberty until
adulthood. It encompasses biological and social maturation from 10–19
years old [9], and is a key time for developing
healthy behaviours that will continue in adult life. The benefits of exercise in
adolescence are broad and well recognised. Physical activity in adolescence
correlates with healthier body composition (including in
overweight/obese children and adolescents [10]), increased bone mineral density (BMD) and improved physical
performance in adulthood [11], and can mitigate
the risks of long-term medical conditions. Healthy male and female adolescent
athletes have significantly greater BMD than their normal peers [12]
[13]. Physical
activity also has a positive effect on mental health and wellbeing in
adolescents, and conversely sedentary behaviour is associated with reduced
wellbeing and depression [14].
Recognition of RED-S in adolescence
Since the IOC definition of RED-S [1] there has
been more research looking at the prevalence of the condition and its
components. It is likely that, due to its highly variable presentation, under
reporting, and previous lack of recognition that males could also be affected,
that the true prevalence is underestimated. RED-S is frequently inadvertent and
caused by a lack of knowledge about the fuelling needs of a highly active and
growing adolescent. The consequences of this negative energy balance are
compounded by sporting myths, including the effects of exercise on menstruation,
and exacerbated within sports with a certain aesthetic and real or perceived
weight restrictions.
In both males and females, the risk of LEA is higher in sports where leanness or
weight targets are important for performance, aesthetics or meeting a weight
category. Higher rates have been reported in elite athletes compared to
recreational athletes [15], but other studies have
concluded that intensity and training volume, independent of competition level,
are more important [16]. In a multi-sport cohort
of elite young female athletes (age 15–32 years, mean age 19 years),
80% of 112 athletes had a least one symptom within the RED-S model [17]. Although the cause could not specifically be
attributed to LEA, it should be considered as an underlying factor in the wide
variety of clinical and psychological symptoms that were highly prevalent in
this young group. This is consistent with previous work where the presence of at
least one component of the female athlete triad was reported as up to
60% in female high school athletes [18].
As with females, males participating in sports which require sustained high
energy expenditure, such as cycling, soccer, rowing, and endurance running, or
those participating in sports with weight classes such as combat sports or
jockeys, are thought to be at increased risk of LEA [2]
[19]
[20]
[21]
[22].
Knowledge and Perceptions of RED-S in
Adolescents
Knowledge and Perceptions of RED-S in
Adolescents
What are adolescent athletes’ perceptions of RED-S?
Despite the high numbers of adolescent athletes being at risk of, LEA and its
consequences, knowledge is low [23]. A survey of
712 adolescent and young adult runners, dancers and figure skaters found that
only 12% had heard of the female athlete triad and only 7% were
able to name 2 of the 3 components of the triad [24]. Misconceptions surrounding menstruation are common, with surveys
identifying that 28–56% of female adolescent athletes think that
losing periods is a normal response to a high level of athletic training [23]
[25]
[26]. A qualitative study in current and former
United States (US) collegiate female distance runners highlighted a culture that
supports the pursuit of the ideal ‘runner body’ through
restrictive eating and excessive training, and a ‘lighter is
faster’ mentality that is learnt early in careers. The coach-athlete
relationship and power dynamic may have a substantial impact on athlete
behaviour, mental health and wellbeing [27].
How much do coaches of adolescent athletes know
about RED-S?
Knowledge of RED-S, the athlete triads or consequences of LEA, amongst coaches
and those working with adolescent athletes is generally low. Misconceptions
amongst coaches regarding menstruation, nutrition and body weight/shape
are seen frequently [28]
[29]
[30]. One survey in the US found
only 8% of coaches and 38% of athletic trainers were able to
correctly identify all components of the triad [31]. Similar findings were present in a survey of 123 US high school
coaches, with 24% aware of the female athlete triad but only 14%
able to identify all three components [28], and in
a study of 106 coaches in Singapore only 2 were able to identify the three
components. 85% had not heard of the female athlete triad at all, and
89% were not able to identify at least one component [29]. A survey of US Collegiate Head Athletic
Trainers found that 98.6% of respondents had heard of the female athlete
triad but only 32% had heard of RED-S [32].
Contributing factors may include the perceived low priority of RED-S amongst
coaches and within organisations, as well as lack of coach education [33]. Many high school coaches in the US lack formal
health education [28], and a review of five
national sporting organisations in Australia found only one (rowing) had formal
education on RED-S within their coach accreditation pathways [34]. Only 7% of Summer Olympic
International Sports Federations undertake health-related programmes, guidelines
or research activity into RED-S [35].
What do health professionals know about RED-S?
Knowledge and confidence in managing RED-S is generally low amongst health
professionals. A study from 2006 in US physicians from various specialties found
that overall, 48% were able to correctly identify the three components
of the female athlete triad whereas only 9% felt comfortable managing
it. Gynaecologists and paediatricians had lower rates of knowledge and comfort
in management compared to orthopaedics surgeons and physical medicine and
rehabilitation physicians [31]. A more recent
survey found that 37% of physicians, again from a variety of
specialties, had heard of the female athlete triad and 51% reported
feeling comfortable treating or referring on a patient with female athlete triad
[36]. Amongst physicians and allied health
professionals attending a US sports medicine conference, 76% were aware
of the female athlete triad and 29% aware of RED-S, but less than a
third were comfortable managing these athletes [37]. Additionally, in a study of 370 US high school nurses, less than
a third had heard of the female athlete triad and only 19% were able to
identify its three components [38]. Taken together
these studies demonstrate a need for improving education and training across the
multi-professional sporting environment.
Health Consequences of Low Energy
Availability
Health Consequences of Low Energy
Availability
The physiological changes in RED-S reflect a hypometabolic state related to LEA,
conserving energy for essential body systems. Consequences of this may be broad
[2], with suppressed function of energy-requiring
physiological systems such as the menstrual cycle, bone health, decreased resting
metabolic rate, implications for growth and immunological impairment. The
gastrointestinal and cardiovascular systems may also be affected. Psychological
health and wellbeing are closely intertwined with RED-S, with psychological symptoms
occurring both before and after development of a low energy state.
Menstrual function
Menstrual function is a vital sign of adolescent female health and wellbeing
[39] and is a key part of any female
adolescent medical history. Menstruation typically starts between the ages of
11–14 years. Primary amenorrhea is the absence of menses by age 15, and
has a prevalence of 0.3% [40]
[41]. Secondary amenorrhea is the absence of menses
for 3 consecutive cycles in previously normally menstruating females, or 6
months with previously irregular periods, and affects 3–4% of
reproductive aged women [42]
[43]. Menstrual irregularity in the first few years
after menarche is common and can be normal, unlike amenorrhoea which requires
investigation.
Functional hypothalamic amenorrhea (FHA) is suppression of the normal
hypothalamic-pituitary-gonadal (HPG) axis, causing amenorrhoea with no other
demonstrable anatomical or medical cause, and is therefore a diagnosis of
exclusion. It is the most common cause of primary and secondary amenorrhoea in
adolescent females [44]. LEA, rather than the
exercise load itself [45], results in suppression
of gonadotrophin-releasing hormone (GnRH) pulsatility. Less than
30 kcal/FFM/day is associated with low or
low/normal luteinising hormone (LH) and follicle-stimulating hormone
(FSH) and reduced ovarian oestradiol production [46]. In longer-term reduced energy availability (EA), there is a more
linear relationship between energy availability below
45 kcal/FFM day and HPG axis disturbances (including luteal
phase defects, oligomenorrhoea and amenorrhoea) [47]. FHA is often multifactorial, caused by LEA and additionally
influenced by medication and psychosocial stressors. It is an adaptive response
of the human body to preserve reduced energy availability for essential
physiological processes and is therefore a reversible and treatable state [43].
Bone mineral density (BMD) and achieving peak bone mass (PBM)
Osteoporotic fractures are a major public health burden. There were an estimated
158 million people aged over 50 years at high risk of osteoporotic fracture in
2010, and this is thought to double by 2040 [48].
Almost 90% of peak bone mass is achieved by the age of 18 [49], and maintaining this into adulthood can reduce
fracture risk by 50–80% [50]. If
PBM is not achieved, this cannot be compensated for in later life. Genetics
remain the largest predictor of PBM, but LEA, hypoestrogenism, menstrual
dysfunction, poor calcium intake, significant weight loss, subclinical eating
disorders and depot-medroxyprogesterone acetate (DMPA) contraception use can
prevent an individual from reaching this genetically determined PBM [51]
[52]
[53]
[54]. Physical
activity that involves high impact activity in adolescence is well recognised as
having positive effects on BMD [55] but only in
the presence of energy balance. Young wrestling/judo participants and
sprinters have been identified as having higher BMD than endurance athletes and
swimmers, and those who are inactive [56]
[57]
[58]. A low BMD
has been associated with adolescents who have specialised early into endurance
running [59], and risk factors for low BMD in male
adolescent runners include body weight<85% expected, weekly
mileage>30 miles, history of stress fracture and less than one serving
of calcium per day [60]. Horse racing is a weight
restricted sport and 29% of entry level male flat jockeys (mean age 18.5
years) were identified as having Z scores<2 [61], compared to 13% of male jump jockeys where the weight
restriction is less.
Endocrine Effects
The endocrine changes that occur within LEA reflect a hypometabolic state and
physiological stress through interlinked pathways. In female adolescent athletes
there are changes in appetite-regulatory hormones, thyroid function, suppression of
the hypothalamic-pituitary-adrenal (HPA) axis, increased cortisol, and reduction in
the bone stimulatory growth hormone (GH) and insulin like growth factor-1 (IGF-1).
The underlying and reversible driver for all these changes is LEA. There is
suppression of the normal diurnal rhythm of the anorexigenic hormone leptin, which
is independent of exercise stress [62], adiponectin is
raised in dancers with LEA [63], the orexigenic
hormone ghrelin is raised in low energy states [64],
and the appetite suppressant Peptide YY is raised in amenorrhoeic athletes [63]. These changes in appetite-regulatory hormones
disrupt the HPA axis resulting in reduced LH pulsatility, low FSH and hypogonadism
[64]
[65]
[66]. In LEA the lower levels of insulin, IGF-1, and GH
result in reduced muscle and bone anabolic effects [67]. Normally these are raised during the developmental adolescent period
of life. Cortisol is raised in LEA, and amenorrheic athletes can demonstrated a
blunted response to adrenocorticotrophic hormone (ACTH) stimulation. Thyroid
function is disrupted with the most consistent changes identified with low
triiodothyronine (T3) levels [63].There is similar but
less extensive research in male adolescent athletes, but emerging data demonstrating
similar effects on leptin, IGF-1, insulin, disruption of the HPG/HPA axis
and testosterone, and changes in spermatogenesis [3]
[63]
[68]
[69].
Psychological Factors in LEA
Psychological Factors in LEA
Psychological comorbidity may occur before or after RED-S is established. Disordered
eating, which often coexists with other mental health conditions, is more common in
adolescent elite athletes than non-athletes, with studies suggesting the personality
traits of athletes convey increased risk [70].
Adolescent females with FHA have a higher incidence of mild depressive traits,
psychosomatic disorders, decreased ability to manage stress [2], and social insecurity, concerns about body image and fear of gaining
weight. These traits overlap with those found more profoundly in adolescents with
eating disorders [71]. In the assessment of RED-S it
is critical that the psychological factors are recognised and addressed within the
multidisciplinary team (MDT) approach.
Performance Consequences and Injury Risk of RED-S
Performance Consequences and Injury Risk of RED-S
Low energy states convey increased risk of nutrient deficiency, fatigue and illness,
as well as impaired performance [72]. Both the range
of physiological systems affected, and the psychological impacts of LEA have a
significant impact on performance by increasing time loss from training due to
illness and injury, and impaired recovery and adaptation to training.
Performance consequences
Ten potential performance consequences of RED-S were highlighted in the IOC
consensus statement [1], encompassing the multiple
physiological systems affected by LEA and RED-S. More recently, decreased
training and endurance response, decreased coordination, impaired judgement and
concentration, irritability and depression has been demonstrated in adolescent
and young adult female athletes (n=1000, mean age 18.9 years) with
self-reported LEA compared with those with adequate EA [72]. There is emerging data from a few small studies reporting links
between reduced performance and adaptation to training, and the presence of
menstrual irregularity and amenorrhoea when compared to eumenorrhoeic peers.
This may prove an important driver for restoration of energy balance [73]
[74]
[75].
Injury risk
Injury rates for adolescent athletes are high, with up to 40% suffering
an injury in a 12-month period [76]
[77]. There is evidence for increased risk of bone
and soft tissue musculoskeletal injury for adolescents with amenorrhoea or other
proxy indicators for LEA. Gram et al. demonstrated that amenorrhoeic gymnasts
(mean age 14.5 years) had a higher risk of injury compared to their
eumenorrhoeic counterparts [78]. Another surrogate
marker, the Drive for Thinness (a subscale of the Eating Disorder Inventory
(EDI)) has been correlated with increased musculoskeletal injury rates in a
college population (18–22 years) [79] and
female high school athletes with disordered eating were identified as twice as
likely to have an injury during a season (n=311) [80]. LEA is one of the modifiable risk factors for
injury in adolescents.
Clinical Presentation of RED-S in Adolescents
Clinical Presentation of RED-S in Adolescents
Clinical assessment for RED-S must be broad and thorough, with a a high index of
clinical suspicion for adolescent athletes at risk of LEA and RED-S. Adolescents
with RED-S may present to a variety of medical and surgical specialties,
physiotherapy, psychology or general practice, and features may also become apparent
to sports coaches or teachers with awareness of the condition and its risks.
We describe the common clinical presentations of adolescents with RED-S in [Table 1]. The potential health consequences (expanding
upon the original Female Athlete Triad) are described in further detail in the 2018
updated IOC Consensus Statement [2]. This has since
been further consolidated, including a self-reported questionnaire study associating
LEA with menstrual dysfunction, poor bone health, cardiovascular and
gastrointestinal issues, metabolic, haematological and psychological conditions in
young adult (15–30 years) female athletes [72].
Table 1 Common clinical presentations of RED-S in
adolescents.
|
Common presentations of RED-S in adolescents
|
|
Amenorrhoea (primary/secondary);
oligomenorrhoea*
|
|
Musculoskeletal injury – bone stress
injury/stress fracture; recurrent soft tissue injury
|
|
Weight loss, changes in BMI centile or trajectory of height
and/or weight gain
|
|
Underperformance in sport
|
|
Exercise-related symptoms (e.g. dizziness, palpitations, syncope
– with normal specialist investigations)
|
|
Fatigue; poor sleep
|
|
Psychological – low mood, anxiety, stress, compulsive
behaviours, disordered eating, pre-occupation with body
image
|
|
Gastrointestinal – constipation; diarrhoea
|
*females only; BMI, basal mass index.
Assessment of RED-S in Adolescents
Assessment of RED-S in Adolescents
History
Due to the detailed, and sometimes sensitive, nature of the questioning required,
the history should be explored in a safe and confidential environment. The
history covers contributory factors of underfuelling, as well as any external
stressors, including illness, school, family life and difficult relationships
within home or sporting environments. A summary of the key components of the
history is in [Table 2].
Table 2 Summary guide to history taking in adolescents at
risk of RED-S.
|
History Taking in Adolescents at Risk of RED-S
|
|
Current symptoms/timeline
|
|
Systems review (including fatigue)
|
|
Past medical history
|
|
History of musculoskeletal injuries
|
|
Growth, developmental & pubertal history
|
|
Family medical history
|
|
Drug history (including over the counter and internet
purchases; contraception; supplements & recreational
drugs)
|
|
Physical activity history
|
|
Dietary history
|
|
Psychological symptoms and external stressors (including
symptoms associated with disordered eating)
|
|
Menstrual history*
|
*females only
A full medical history should include any current symptoms and a thorough systems
review reflecting the broad range of potential clinical presentations. This
includes fatigue, gastrointestinal symptoms such as changes in bowel habit,
weight loss, and cardiovascular symptoms such as palpitations, dizziness, and
syncope (which can be a direct result of LEA and its consequences). Coeliac
disease should be considered, as it is linked to fatigue, reduced BMD and bone
stress injury [81]
[82] as well as the more typical gastrointestinal symptoms. Females
should be asked about their past and current menstrual history. Past medical
history should be sought along with history of musculoskeletal injury (soft
tissue and bony; traumatic or bone stress injuries), a full developmental and
pubertal history, and family medical history. Drug history should include
prescribed and independently purchased medications, hormonal contraceptives,
supplements and recreational drugs. It is worth remembering the side-effects of
medication and the potential consequences on energy expenditure, appetite or
menstrual pattern, that are seen, for example, with drugs for depression,
anxiety or attention deficit hyperactivity disorder and biologics for chronic
inflammatory conditions.
A thorough physical activity history is required to ascertain the volume and
intensity of school activities, club training and home exercise. A dietary
history should include food intake (meals/snacks), timing of fuel intake
around exercise and any restrictive or avoidant eating patterns. Sleep quality
and sleep hygiene should be assessed (as key components of well-being and
recovery from training). Psychological assessment should include screening for
depression and anxiety, as well as dietary cognitive restraint, drive for
thinness and purging behaviours, which may be more common in adolescents with
amenorrhea and RED-S. The prevalence of eating disorders is higher in elite
adolescent athletes (especially females), than controls [83]. If an adolescent has suggestion of a significant eating
disorder, such as rapid weight loss, significant concern from carers, purging
behaviours, or physical consequences of malnutrition such as bradycardia,
fainting or additional mental health problems, referral to a specialist child
and adolescent mental health service is suggested [84].
Self-Reported Questionnaires
The practical challenges associated with accurate measure of EA have led to
the use of self-reported and surrogate measures. A large review of
questionnaire-based reporting in athletes demonstrated that, while
intentional energy restriction and disordered eating can be identified, it
is more challenging to identify those with unintentional energy deficiency.
The most commonly used validated questionnaires were Low Energy Availability
in Females Questionnaire (LEAF-Q) and Eating Disorder Examination
Questionnaire (EDE-Q). The authors concluded that such questionnaires can be
used in screening for RED-S, but not diagnosis, and that their effectiveness
may be reduced due to unintentional under-fueling [85]. High drive for thinness (a subscale of the EDI
questionnaire) has been shown to be a surrogate marker for energy
availability correlating with resting metabolic rate and total T3 levels
[86]. More recently it has also been
associated with increased rate of musculoskeletal injuries in 18–22
years female athletes [79]. The drive for
thinness subscale is used in both female and male athletes [87], and is a quick and simple questionnaire to
use in a clinical out-patient setting.
Examination
A thorough physical examination should be undertaken looking at the signs for
RED-S and its differential diagnoses.
Height, weight and centile body mass index (BMI) can be measured and plotted on a
growth chart. RED-S can occur in the presence of a normal BMI, however
attenuation of expected growth or low body weight (<85% expected
body weight for adolescents) [88] should raise
suspicions of RED-S or other conditions associated with weight loss
Physical signs to look for include, signs of androgen excess and hypo- or
hyperthyroidism, signs of an eating disorder (anorexia nervosa), purging
behavouir, malnutrition, and signs of psychological distress such as self
harm.
Heart rate, lying and standing blood pressure measurements and temperature can
also be considered, particularly in the presence of anorexia nervosa or other
severe eating disorder, and other high risk scenarios such as rapid weight loss
or purging behaviour [84].
Investigations
An initial estimate of FFM can help with the initial assessment and subsequent
nutritional recommendations, if the equipment and expertise is available.
However, in order to optimize a positive body image in adolescent athletes,
routine body composition measurements are not recommended [89].
A pragmatic attempt should be made to estimate energy availability (i.e. do you
think the athlete is energy replete and
consuming≥45 kcal/kg FFM/day?). If information
on physical activity and dietary intake is insufficient from the history,
consider a food and activity diary (including records from wearable devices) for
three to seven days.
The standard blood tests and other initial investigations specific to RED-S, and
its differential diagnoses that we consider, are presented in [Table 3] along with their rational.
Table 3 Initial investigations in RED-S.
|
Initial investigations in RED-S
|
|
Initial blood tests
|
Rationale
|
|
FBC, U+E, LFT, CRP, ESR
|
Routine blood tests for general health and for other causes
of symptoms such as weight loss, fatigue.
|
|
Ferritin
|
Iron deficiency affects bone health, via the GH/IGF-1
axis, hypoxia and hypothyroidism, and other metabolic
pathways including thyroid, reproductive function and
wellbeing [108]. Low ferritin
and iron-deficiency anaemia have been correlated with LEA in
adolescent female athletes [2].
|
|
TFT
|
Impaired thyroid function (particularly reduced T3 levels
[63] has been
demonstrated, sometimes more marked with ovarian
suppression) [75].
|
|
Thyroid function status should also be checked in
amenorrhoeic females, and may help to guide specialist
referral [40].
|
|
LH1, FSH1, prolactin1
|
In primary and secondary amenorrhoea, prolactin, FSH
& LH can help guide specialist referral.
|
|
Total testosterone1/2
|
In females, if signs of androgen excess (as part of
investigation for primary amenorrhoea) [40].
|
|
Testosterone can be reduced in males with energy deficiency
[67].
|
|
Pregnancy test1 (if sexually active)
|
To exclude pregnancy as a cause of amenorrhoea [40]. Can also be performed as a
urine test.
|
|
Other tests to consider
|
|
Bone profile; 25(OH)D
|
25(OH)D status during adolescence is an independent factor
for bone mass gain, muscle force and hand grip strength
[109]. Increasing
observational data propose roles extending beyond
musculoskeletal health and performance; this hormone has an
important role in immunity, cardiovascular health,
neurological function, glucose metabolism and insulin
sensitivity.
|
|
B12, calcium, folate, glucose, inorganic phosphate,
magnesium
|
In addition to routine blood tests above if concerns of
severe eating disorder, rapid weight loss or severe purging
behaviour. However, it may be more appropriate in these
circumstances to seek urgent specialist advice [84].
|
|
IgA and IgA TTG antibody (should have been taking a
gluten-containing diet for>6 weeks)
|
Children & adolescents with coeliac disease have
lower bone mass and density [81] and a the prevalence of coeliac disease was
5% in 100 patients with bone stress injuries
(approximately 5x higher than population estimates) [82].
|
|
DXA
|
We primarily use DXA as part of assessment in bone stress
injuries but can also give information on body composition
and FFM. In adolescents, spine and total body less head are
the preferred skeletal sites. A Z-score of≤2 defines
low BMD for chronological age [110]. DXA is recommended if presenting with
recurrent bone stress injuries, to provide a baseline for
longitudinal monitoring of bone density and response to
treatment (important because the BMD distribution may be
significantly different to age and gender-specific reference
ranges for the general population [12].
|
1 – females only; 2 – males only;
25(OH)D, 25-hydroxy-vitamin D; BMD, bone mineral density; CRP,
C-reactive protein; DXA, dual-energy X-ray absorptiometry; ESR,
erythrocyte sedimentation rate; FBC, full blood count; FFM, fat free
mass; FSH, follicular stimulating hormone; GH, growth hormone; IgA,
immunoglobulin A; IGF-1, insulin-like growth factor-1; LEA, low energy
availability; LFT, liver function tests; LH, luteinising hormone; SHBG,
sex-hormone blinding globulin; T3, triiodothyronine; TFT, thyroid
function test; TTG, tissue transglutaminase; U+E, urea and
electrolytes
An ECG should be considered if high risk of electrolyte abnormalities, for
example anorexia nervosa, rapid weight loss or purging behaviour.
Gynaecological referral is indicated for females with primary amenorrhoea, and it
may be appropriate to consider referral to a gynaecologist or endocrinologist
for secondary amenorrhoea, if a non RED-S aetiology is suspected [40]. Ultrasound scan and sex-hormone binding
globulin could be performed if polycystic ovarian syndrome (PCOS) is suspected.
Estradiol, anti-mullerian hormone and dehydroepiandrosterone (DHEA) sulfate (if
hyperandrogenism present) are not part of standard clinical practice for
investigating amenorrhea in the United Kingdom but are recommended by other
guidelines [90]. Additonal specialist
investigations for ammenorrhea, guided by clinical findings, may include
17-hydroxyprogesterone (late-onset congenital adrenal hyperplasia), insulin-like
growth factor-1 (acromegaly, can also be used in the assessment of low energy
availability but may not be available in all settings) and brain magnetic
resonance imaging (pituitary tumour or other pathology)
Management of RED-S in Adolescents
Management of RED-S in Adolescents
Prevention and education
The presentation of RED-S in adolescents can be complex and multifactorial.
Individuals may present to a variety of medical specialties, as well as sporting
coaches and team staff before a unifying diagnosis is identified. As the
development of this condition can reflect a period of under-fueling and LEA
before specific symptoms appear, there is also a critical window of opportunity
for identification and reversal of these risk factors before RED-S becomes
established. It is very important to develop a healthy environment around
exercise, nutrition and body image in adolescence as this will define the
life-long relationship with food [91].
It has been proposed that education of athletes, team staff and healthcare
professionals should take place to raise awareness of RED-S and its
consequences, improve recognition of at-risk individuals and sports, and
reinforce positive messaging around nutrition, body image and, in females,
menstrual cycles [89].Education sessions may also
provide an opportunity to challenge misconceptions and negative cultures in
sport such as those around thinness and performance. At-risk individuals may be
identified with validated questionnaires at pre-participation screening [85].
Peer education [92] and brief video educational
interventions [93] have been shown to increase
knowledge of RED-S in high-school athletes, but the effect of this on behavior
and longer-term outcomes is unknown. Mobile technology interventions have been
shown to be acceptable and feasible in a population of adolescent and young
adult females [94]. Positive behavioral change at
18-month follow-up was maintained with a short eating disorder intervention in
female college athletes [95]. Encompassing a
broader age range, educational nutritional and skeletal health interventions
were associated with improved bone health, wellbeing, and race performance in
competitive male road cyclists (18.5–72 years) [96]. These results show promise for the use of technological
interventions in the future, a format that is both familiar and acceptable to
the adolescent and young adult population.
Management of established RED-S
Once RED-S is established, the broad aim of treatment is to restore energy
balance by increasing energy intake and/or reducing energy expenditure.
The underlying aetiology of LEA should be identified. We advocate using the
expertise of a MDT, tailored to the needs of the athlete. This is likely to be
coordinated by a sport and exercise medicine physician with input from
dieticians, psychologists, coaches, physiotherapists, and other medical
specialties (such as endocrinology, gastroenterology, gynaecology and
psychiatry), as required. Management is long-term with energy balance typically
taking days to weeks to restore, menstruation weeks to months and bone density
years [2].
Increasing energy intake
For those athletes who are inadvertently under-fueling, education and
practical advice on increasing energy intake may be all that is required to
restore energy balance. It is worth remembering that in adolescent athletes,
energy needs may be higher due to the additional energy demands of growth
and development [2]. The increases in energy
intake required will differ between athletes, but it has been shown that
increasing calorie intake by 250–360 kcal/day is
sufficient to restore menses in female athletes with FHA [97]
[98]. A
‘food first’ approach should be used (rather than
supplements) and increases in energy intake could be achieved by adding
snacks between meals (for example 3 meals and 3 snacks throughout the day),
increasing portion sizes and/or increasing the energy-density of
meals. The timing of meals and snacks are important to avoid prolonged
periods of within-day energy deficit, concentrating on times of energy
expenditure such as around training and competition [99]. In addition to providing energy, the consumption of higher
amounts of carbohydrate may have an additional positive impact on bone
health through attenuation of the post-exercise increase in
β-C-terminal telopeptide of type 1 collagen (CTx) [100], and increases in leptin [101].
Consider input from a dietician in athletes with high energy requirements,
dietary restrictions, more marked disordered eating or other difficulties
increasing energy intake. Athletes with an eating disorder should be
referred to a specialised eating disorder service [102].
Vitamin D and calcium supplementation should be considered alongside the
management of RED-S to optimise bone and musculoskeletal health.
Recommendations for Vitamin D intake in adolescence varies between
5–25 mg daily, however, intakes at the higher end of this
range (15–25 mg/day) are likely to be required to
achieve and maintain 25(OH)D concentrations>50nmol/L [103]
[104].
Supplementation can take place at daily or weekly intervals [105] and if Vitamin D deficiency is present
higher dose replacement may be required. The recommended calcium intake for
adolescents is 1300 mg/day [8]. Caution should be used when recommending supplements, such as
Vitamin D, due to the risk of contamination, for young elite athletes who
may undergo anti-doping testing.
Reducing energy expenditure
If increasing energy intake alone is insufficient to restore energy balance,
then energy expenditure can be reduced by altering training and/or
competition load. Many adolescent athletes play multiple sports, as well as
participating in physical activity at school and active travel. Discussions
with the athlete, parents and coaches can be helpful to understand the
overall physical activity demands on the athlete and their views. It is
important to emphasise the benefits of good recovery and the need for one or
two rest days per week. Training and competition loads may need to be
reduced, and the athlete should be the main decision maker on which
activities they wish to prioritise. Reducing energy expenditure should be
considered in athletes with disordered eating or eating disorder but may not
be necessary in all cases [102].
Hormonal interventions in female athletes
The use of the combined oral contraceptives (COCPs) for improving BMD in
RED-S is not recommended as the evidence of their effects on bone density is
inconsistent and they may mask the return of normal menstruation. The lack
of effect of COCPs on BMD is thought to be due to downregulation of IGF-1
[90]. In studies which included adolescent
athletes, transdermal oestradiol (E2) (which does not affect IGF-1) given
with cyclical oral progestin has been shown to increase bone density,
compared to the combined oral contraceptive pill, in normal weight
oligo-amenorrheic athletes [106] and in
amenorrheic athletes with low body weight [107]. However, in the Nose-Aguro study an even greater
improvement in bone density was seen in athletes who improved their energy
availability and restored normal menstruation. Short-term use of transdermal
estradiol with cyclical oral progestin could be considered if other
non-pharmacological interventions to improve EA are unsuccessful [90].
Other pharmacological interventions
The use of bisphosphonates, denosumab, testosterone or leptin are not
recommended in adolescents due to a lack of data on effectiveness and safety
[4]
[90].
Recombinant parathyroid hormone may be considered for delayed fracture
healing or very low BMD in adult women [90]
but should be avoided in adolescents and young adults with open growth
plates [2].
Conclusion
Low energy availability, frequently due to inadvertent underfuelling, is common in
female and male adolescents. Clinical presentation can be broad and may initially
seem quite non-specific, so athletes may present to several medical professionals
before the unifying diagnosis is identified. Regular screening during the season, or
at times of impaired performance, injury, illness, or other changes may highlight
athletes with features of low energy availability before the condition becomes
established. Promoting awareness and supporting education amongst adolescent
athletes themselves, and in both sporting and medical professionals is key for
prevention, early recognition, and management of low energy availability and RED-S.
Treatment, ideally within the structure of a multidisciplinary team, should
concentrate on restoration of energy balance and individualised management of
specific features. Our take home points are summarized in [Table 4].
Table 4 Take home points.
|
Take Home Points
|
|
RED-S affects male and female adolescent athletes
|
|
RED-S may present to many different medical specialties, as well
as sporting coaches and team staff
|
|
Awareness of RED-S amongst coaches and health care professionals
is low
|
|
Restoration of energy balance, through a MDT educational
approach, is the core of management
|
|
Resumption of menses is the aim in female athletes
|
|
Use of the COCP is not advised in the management of RED-S
|
|
Adjunctive novel therapies are not currently recommended
|
COCP, combined oral contraceptive pill; MDT, multi-disciplinary team; RED-S,
relative energy deficit in sport.
