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Open access Original article BMJ Open Sport Exerc Med: first published as 10.1136/bmjsem-2019-000523 on 29 March 2019. Downloaded from
Clinical evaluation of education relating
to nutrition and skeletal loading in
competitive male road cyclists at risk of
relative energy deficiency in sports
(RED-S): 6-month randomised
controlled trial
1 2 1 3
Nicola Keay, Gavin Francis, Ian Entwistle, Karen Hind
To cite: Keay N, Francis G, AbsTrACT What are the key new findings of this study?
Entwistle I, et al. Clinical Objective To clinically evaluate education to improve
evaluation of education relating eating behaviour and skeletal loading exercise in
to nutrition and skeletal male cyclists at risk of poor bone health and impaired ► Changing both nutrition and skeletal loading exercis-
loading in competitive male performance due to relative energy deficiency in sports. es over a race season resulted in significant changes
road cyclists at risk of relative Methods Early race season, 50 competitive male road in lumbar spine bone mineral density.
energy deficiency in sports ► Based on British Cycling points won over the sea-
(RED-S): 6-month randomised cyclists were matched, in pairs, based on Z-scores for son, reducing energy availability was associated
controlled trial. BMJ Open lumbar spine bone mineral density (BMD). One member of with negative cycling performance; increasing ener-
Sport & Exercise Medicine each pair was randomly allocated to receive educational
2019;5:e000523. doi:10.1136/ interventions. After the season, 45 cyclists returned for gy availability was associated with superior cycling
bmjsem-2019-000523 performance.
dual-energy X-ray absorptiometry scans and blood tests. ► For cyclists to change their behaviours to achieve copyright.
► Additional material is Least significant change was applied to identify clinically better health and performance, psychological barri-
published online only. To view meaningful BMD changes. Cyclists completed a follow- ers (fear of performance decrements) were a greater
please visit the journal online up sport-specific questionnaire and clinical interview to impediment than physical factors (eg time).
(http:// dx. doi. org/ 10. 1136/ ascertain adherence to the interventions.
bmjsem- 2019- 000523). results The questionnaire and clinical interview
categorised behaviour changes as positive, negative or How might this study impact clinical practice
Accepted 5 March 2019 unchanged. Positive changes in nutrition and skeletal in the future?
loading were associated with a statistically significant
increase of 2.0% in lumbar spine BMD; 7 of 11 cyclists’ ► Athletes at risk of relative energy deficiency in
increases were clinically meaningful. Negative changes sports (RED-S), including male athletes, should be http://bmjopensem.bmj.com/
in both behaviours were associated with a significant assessed for low energy availability.
decrease of 2.7% in lumbar BMD; all nine cyclists’ ► Our sport-specific energy availability questionnaire
BMD decreases were clinically meaningful. Regarding combined with clinical interview (SEAQ-I) provides a
© Author(s) (or their performance, taking account of functional threshold power, practical, effective clinical tool to identify and man-
employer(s)) 2019. Re-use changes in nutritional behaviour accounted for gains or age cyclists at risk of RED-S.
permitted under CC BY-NC. No losses of 95 British Cycling racing points. Cyclists reported ► We suggest the approaches in this study can be
commercial re-use. See rights psychological barriers to change in behaviours, specifically
and permissions. Published by applied more broadly to provide sports-specific/
BMJ. fear of negatively impacting performance. dance-specific educational support on nutrition-
1 Conclusions Educational nutritional and skeletal loading al and exercise strategies to improve health and
Department of Sport and interventions can improve bone health, well-being and
Exercise Sciences, Durham race performance in male cyclists over a 6-month race performance. on January 5, 2023 by guest. Protected by
University, Durham, UK ► Our findings will be made available to athletes,
2 season. Psychological support may be required to help
Science4Performance, London, coaches, parents and healthcare professionals
UK some athletes change behaviour. through educational online resources on RED-S,
3
Department of Sport and such as the British Association of Sport and Exercise
Exercise Sciences and the Medicine, www.Health4Performance.co.uk and
Wolfson Institute for Health and via the TrainBrave campaign to raise awareness of
Wellbeing, Durham University, InTrOduCTIOn RED-S.
Durham, UK
Competitive road cyclists are at risk of
Correspondence to developing the health and performance availability can arise unintentionally and/
Dr Nicola Keay; consequences of low energy avaiability or intentionally from restrictive nutrition, as
nickykeayfrancis@ googlemail. described in the relative energy deficiency in cycling is a gravitational sport where low body
1 weight confers a performance advantage, up
com sport (RED-S) clinical model. Low energy
Keay N, et al. BMJ Open Sport Exerc Med 2019;5:e000523. doi:10.1136/bmjsem-2019-000523 1
Open access BMJ Open Sport Exerc Med: first published as 10.1136/bmjsem-2019-000523 on 29 March 2019. Downloaded from
to a point, until cumulative low energy availability leads the exercises. Initially weekly, then monthly, these cyclists
2 3
to adverse clinical outcomes of RED-S. were contacted to check on progress. All cyclists were
The process of bone formation is sensitive to low asked to record any sustained changes in off-bike exer-
4
energy availability. Lacking the early warning sign of cise and nutrition, both baseline and fuelling around
5
stress fracture experienced by runners, impaired bone training.
health in cyclists, as a consequence of low energy avail-
ability and lack of osteogenic stimulus, can become sport-specific energy Availability Questionnaire and Interview
severe.3 Poor bone health has short-term and long-term The clinical assessment of energy availability by SEAQ-I
consequences, with fracture being the most frequent made in our published baseline early race season
6 3
type of injury reported in cyclists. study was significantly associated with lumbar spine
Early identification of cyclists at risk of developing low BMD Z-score in this group of cyclists. We used a similar
energy availability is important in order to intervene approach to devise a follow-up SEAQ-I with input from
to prevent the health and performance consequences the same clinical sports endocrinologist, sports research
of RED-S. As reported in our study of 50 male compet- scientist, registered clinical sports dietitians, cyclists and
itive road cyclists, a Sport-specific Energy Availability coaches for validation of content (see online supplemen-
Questionnaire and Interview (SEAQ-I) was effective in tary file 1).
identifying a low Z-score of lumbar spine bone mineral The follow-up SEAQ-I was conducted at the end of
3
density (BMD), which is recognised as a quantifiable the race season. After the cyclists had completed the
measure of low energy availability as outlined in RED-S questionnaire, the sports clinician interviewed them indi-
7
Clinical Assessment Tool. vidually to verify answers and gather more details on the
However, once male cyclists at risk of RED-S have been responses provided, including the following:
identified, there are currently no clear guidelines on ► Cycling training, race results and quantification of
2
how to effectively manage such athletes. Therefore the any changes in skeletal loading exercises performed,
purpose of this study was to investigate the efficacy of an as per recommendations, or otherwise.
educational intervention, specific to competitive cyclists, ► Nutritional information: any changes in baseline
to ensure adequate energy availability, bone health and nutrition, fuelling around training, as per recom-
performance over the duration of a race season. mendations, or otherwise; intention to change body
weight/composition; addition of any supplements. copyright.
MATerIAls And MeTHOds ► Medical history during study period: number, nature
Participants and site of injuries; number of days off training due
Forty-five adult male competitive cyclists (equivalent to illness.
to British Cycling [BC] category 2 or above) who had From the follow-up SEAQ-I, cyclists were assessed in
participated in data collection early in the road race each of the areas of nutrition and skeletal loading as
3 returned at the end of the racing season during implementing either positive change, no change or nega-
season
September and October. tive change. Qualitative information was gathered on
reasons for cyclists being unable to adhere to the recom-
Allocation of cyclists to intervention/no intervention groups mendations for their allocated group. http://bmjopensem.bmj.com/
In the early race season, cyclists were matched, in pairs,
based on Z-scores for lumbar spine BMD. One member sport-specific performance measures
of each pair was randomly allocated to receive educa- Cyclists recorded the number of BC race points won
tional interventions from the lead clinician. Technicians during the study period, together with any race high-
performing the dual-energy X-ray absorptiometry (DXA) lights. The number of points won was verified from the
scans were blinded to the allocation. BC website. For those competing outside of BC races (eg,
Commonwealth Games, European Championships and
educational nutrition and skeletal loading intervention time trial events), an equivalent number of BC points
The nutritional advice (see online supplementary file was estimated, to reflect race performance over the
3) aimed to maintain adequate energy availability, with season. Cyclists also reported their 60 minute functional on January 5, 2023 by guest. Protected by
recommendations for general nutrition and fuelling threshold power (FTP) in watts.
around training sessions. These recommendations had
been approved by registered clinical sports dietitians. bone health measures
The skeletal loading exercises (see online supplementary Body weight was measured to the nearest 0.1 kg using cali-
file 2) were designed to be practical, based on current brated electronic scales (Seca Alpha, Birmingham UK),
8
recommendations to improve bone health, with input and standing height was measured to the nearest 0.1 cm
from qualified Pilates teachers and physiotherapists using a stadiometer (Seca Alpha) with head in Frankfurt
working with cyclists. For cyclists in the intervention plane. Bone health and body composition were evalu-
group, both the nutrition and exercise recommendations ated using DXA (GE Lunar iDXA, GE Healthcare, UK)
were fully explained and written sheets provided. Online according to best practice recommendations for densi-
resources included the sheets and a video demonstrating tometry in athletes, and the same trained, International
Keay N, et al. BMJ Open Sport Exerc Med 2019;5:e000523. doi:10.1136/bmjsem-2019-000523
2
Open access BMJ Open Sport Exerc Med: first published as 10.1136/bmjsem-2019-000523 on 29 March 2019. Downloaded from
Society for Clinical Densitometry (ISCD)-certified Table 1 Descriptive characteristics of cyclists
densitometrist interpreted all examinations to ensure Range: minimum–
consistency of region of interest placement between N=45 Mean±SD maximum
9
baseline and follow-up measures. BMD was evaluated at
the anterior-posterior lumbar spine (L1–L4) and femoral Age (years) 36.2±14.3 18.5 to 72.0
neck. Age-matched BMD Z-scores were derived for each Height (m) 1.80±0.06 1.70 to 1.91
cyclist, at each skeletal site by the DXA software, using Weight (kg) 73.2±6.6 62.1 to 91.2
UK reference population data (GE Lunar Encore V.15.0, 2
Body mass index (kg/m ) 22.5±1.5 18.0 to 25.4
GE Healthcare, Madison, Wisconsin). Precision estimates Training load: average hours 11.2±4.0 5.0 to 20.0
(coefficient of variation) are 0.4% for lumbar spine BMD on bike/week
10
and 0.9% for femoral neck BMD. Body composition was 60 minute FTP (watts) 327±48 195 to 410
derived from a total body scan with precision estimates
being 0.5%–0.9%.11 FTP/kg (watts/kg) 4.5±0.6 2.8 to 5.5
Race results (equivalent BC 194±239 0.0 to 953
endocrine health measures points)
Endocrine and metabolic markers were assessed from Number of injuries 0.4±0.7 0.0 to 3.0
capillary blood samples taken in the morning after Number of days of illness 1.4±2.5 0.0 to 10.0
waking to minimise diurnal variation. Samples were anal-
ysed to determine concentrations of total testosterone, BC, British Cycling; FTP, functional threshold power.
vitamin D (25-hydroxy), free triiodothyronine, albumin,
calcium, corrected calcium and alkaline phosphatase using the D’Agostino and Pearson test. The equivalence
at Surrey University-accredited laboratories using cobas of means of multiple subgroups was tested by analysis of
8000 analyser with interassay coefficient of variation from variance. The significance of the regression coefficients
<2% to 7% for the markers above. Absolute mean values between continuous variables was based on the t-statistic.
with SD were determined and results were also expressed
as Z-scores, using population mean and SD derived from Patient and public involvement
the definition of the reference range, as covering 95% of The research, clinical and support pathways for male
a normal distribution. athletes at risk of RED-S are lacking compared with provi- copyright.
statistical analysis sion for female athletes. During a pilot study of cyclists,
Analyses were performed using open source pack- these issues were discussed as SEAQ-I was trialled and
12 refined. Male cyclists were instrumental in the initiation
ages Orange (Bioinformatics Lab at the University of this current study through involvement of coaches,
of Ljubljana, Slovenia) and SciPy (Enthought, Austin, and recruitment of team-mates and riders from other
Texas, USA). The data set included categorical and teams. A male cyclist in this study diagnosed with osteopo-
continuous observations, taken from the follow-up rosis due to RED-S wrote a patient voice piece for British
SEAQ-I, blood markers and DXA results. The means and Journal of Sports Medicine. Other cyclists from the study
SD of continuous variables were evaluated and, where experiencing consequences of RED-S contributed to arti- http://bmjopensem.bmj.com/
relevant, compared against appropriate population refer- cles in cycling magazines and to the TrainBrave campaign
ence ranges. to raise awareness. Cyclists and coaches are supportive of
Explanatory analyses identified attributes associated and providing input for an educational website on RED-S
with target variables relating to changes in bone health ( www. Health4Performance. co. uk) backed by the British
and to cycling performance over the racing season. Since Association of Sport and Exercise Medicine, which has
experimental interventions were designed to benefit been developed by the authors of this study.
lumbar spine, the change in lumbar BMD was the target
variable for bone health. The target variable for cycling
performance was the number of BC points attained. resulTs
13 Of the original 50 cyclists, 45 participants returned for on January 5, 2023 by guest. Protected by
In accordance with the ISCD recommendations,
the precision error of DXA measurements was taken follow-up. Descriptive characteristics are shown in table 1.
into account in assessing changes in BMD. A change in
BMD of an individual was considered to be meaningful Follow-up seAQ-I and definition of groups
if exceeding the least significant change (LSC), defined Although the study design randomly allocated half the
9 athletes to receive educational recommendations, it
as 2.77 times precision error. Thus the LSC for lumbar
spine BMD was 1.1%. became apparent during the follow-up SEAQ-I that
Changes were considered only for those of the orig- participants from both groups had followed nutritional
inal 50 participants who attended the second round of and exercise behaviours that deviated from their allo-
DXA scans and provided a second set of blood results. cation in the research protocol. Based on the clinical
The resulting set of paired samples was analysed using assessment from the follow-up SEAQ-I, athletes were clas-
the paired sample t-test, after checking for normality sified in terms of their nutrition and exercise behaviours.
Keay N, et al. BMJ Open Sport Exerc Med 2019;5:e000523. doi:10.1136/bmjsem-2019-000523
3
Open access BMJ Open Sport Exerc Med: first published as 10.1136/bmjsem-2019-000523 on 29 March 2019. Downloaded from
From the follow-up SEAQ-I, the resultant groupings for pre-existing exercise regimens. The difference between
changes in energy availability were classified as negative skeletal loading groups was highly significant (p<0.001).
(n=11), no change (n=22) or positive (n=12), and for Although the association between changes in lumbar
skeletal loading exercise as negative (n=12), no change BMD with changes in energy availability was slightly
(n=16) or positive (n=17). A positive correlation was higher than with changes in skeletal loading, it was
observed between the nutrition and exercise behaviours difficult to distinguish between the two factors due to
(r=0.78), with change or no change in these behaviours the high correlation between the subgroups. Neverthe-
tending to occur together. less, an increase in both energy availability and skeletal
Psychological factors were important in certain loading led to a markedly better outcome than doing the
subgroups. The 11 cyclists who made positive changes opposite (p<0.001).
in both behaviours reported improved well-being and Figure 1 shows the change in lumbar spine BMD for
feeling stronger on the bike. The 13 cyclists who made no the individual cyclists, grouped according to changes
behavioural changes included 3 riders, initially in chronic in behaviours. The colours refer to nutrition and the
low energy availability, who had been allocated to inter- shapes signify skeletal loading. Significant increases in
vention. These three were unable to sustain the protocol, BMD (exceeding LSC) were found in 7 of the 11 cyclists
citing psychological rather than physical barriers, such implementing positive changes in both behaviours
as stress during the race season and difficulty deviating (green triangles). Conversely, all nine in the group who
from their established training and nutrition schedules. implemented negative changes in both behaviours (red
No cyclists had been advised to reduce either nutrition crosses) showed significant reductions in BMD. In the
intake or reduce off-bike exercise. Nevertheless, nine remainder of the cyclists, three of four who had posi-
riders were assessed as having reduced both. The clinical tively changed one of the behaviours showed significantly
interview revealed that these behaviours were pursued increased BMD, whereas four of six who had negatively
in the belief that performance would improve. However, changed one of the behaviours exhibited significantly
these cyclists reported fatigue, illness and injury. decreased BMD.
bone health and body composition endocrine and metabolic biomarkers
For the study group as a whole, BMD was lowest at the Endocrine and metabolic biomarkers are found in table 3.
lumbar spine (Z-score −0.91). Behavioural group was A significant increase was seen in vitamin D concentra- copyright.
the factor most closely associated with change in BMD tion. Although this could have been due to exposure
at this skeletal site. Table 2 shows the mean change in to sunshine over the summer, the increase was better
lumbar BMD according to the subgroups defined in explained statistically by the increase in the number of
terms of change in energy availability or skeletal loading. cyclists taking sports informed vitamin D supplement
Shown in the bottom row of this matrix, cyclists who had of 1000 IU per day, recommended to participants who
reduced energy availability saw a significant average 2.3% were not already doing so, based on the low readings in
reduction in lumbar BMD over the 6-month interval the early season analysis. A significant increase in free
between scans, compared with a significant 2.2% increase triiodothyronine was found. The mean concentration of
in lumbar BMD for those who had improved energy avail- testosterone remained in the lower half of the reference
ability and little change for those with consistent energy range. No meaningful, statistically significant relation- http://bmjopensem.bmj.com/
availability. The difference between the energy avail- ships were observed between changes in biomarkers and
ability groups was highly significant (p<0.001). In the far the energy availability and skeletal loading behavioural
right column of the matrix, cyclists who had increased subgroups.
skeletal loading saw a significant average 1.4% increase
in lumbar BMD, compared with a significant 2.5% determinants of cycling performance
decrease in lumbar BMD for those who had reduced One cyclist had been signed for a world tour team, three
skeletal loading and no change for those maintaining cyclists gained an elite racing licence, and four riders
on January 5, 2023 by guest. Protected by
Table 2 Percentage changes in lumbar BMD by behavioural group
Energy availability assessment
Negative No change Positive Total
Skeletal Positive NA (0) 0.3 (6) 2.0 (11) 1.4 (17)
Loading No change −0.7 (2) −0.3 (13) 4.9 (1) 0.0 (16)
Exercise Negative −2.7 (9) −1.8 (3) NA (0) −2.5 (12)
Total −2.3 (11) −0.4 (22) 2.2 (12) 0.0 (45)
Percentage change in L1–L4 lumbar BMD (number of observations).
Significant differences were observed between the groups (see text).
BMD, bone mineral density; NA, not available.
Keay N, et al. BMJ Open Sport Exerc Med 2019;5:e000523. doi:10.1136/bmjsem-2019-000523
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