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Brazilian Journal of Education, Technology and Society (BRAJETS) – Especial Section, “Disability, Education, Technology and Sport”
2018, Vol. 11, No. 01, Jan-Mar. http://dx.doi.org/10.14571/brajets.v11.n1
Br. J. Ed., Tech. Soc., v.11, n.1, Jan.-Mar., p.195-203, 2018
DOI http://dx.doi.org/10.14571/brajets.v11.n1.195-203
ENERGY AVAILABILITY IN FEMALE ATHLETES WITH DISABILITIES: A
NARRATIVE REVIEW
DISPONIBILIDADE ENERGÉTICA EM ATLETAS MULHERES COM DEFICIÊNCIA:
REVISÃO NARRATIVA
Claudia Ridel Juzwiak
Universidade Federal de São Paulo (Unifesp)
Santos, SP Brazil
claudia.juzwiak@unifesp.br
Daniel Paduan Joaquim
Universidade Federal de São Paulo (Unifesp)
Brazilian Paralympic Committee
São Paulo, SP, Brazil
daniel_paduan@hotmail.com
Ciro Winckler
Universidade Federal de São Paulo (Unifesp)
Santos, SP Brazil
ciro.winckler@unifesp.br
Abstract.
Research on female athletes has increased, with the main focus on Low Energy Availability (LEA) and Female Athlete
Tri ad (TRIAD), however there is a gap in knowledge about LEA and related conditions such as eating disorder, menstrual
dysfunction and bone health in athletes with disabilities. The literature suggests that those athletes, depending on the type of
disability, have a higher risk of developing LEA. In this way, the objective of this review is to describe the impact of LEA on health
and performance of female athletes, with special focus on athletes with disabilities. A narrative review of the literature was
conducted using as search terms LEA and TRIAD components - bone health and menstrual dysfunction - in female athletes. The
narrative review yielded 24 studies on the subject, of those, 10 original studies, in which LEA was diagnosed in female athletes,
only one referring to athletes with disabilities. Literature indicates the complexity in estimating EA, since the methods used to
determine its components may present inaccuracies, especially for athletes with disabilities. Further researched is needed to assess
EA in female athletes, especially with disabilities, as well as the improvement of EA's assessment and screening methods.
Keywords:
low energy availability; female athletes; athletes with disabilities.
Resumo.
A pesquisa sobre mulheres atletas aumentou, com o foco principal na baixa energia disponível (LEA) e na tríade da
mulher atleta (TRIAD), no entanto, há uma lacuna no conhecimento sobre LEA e condições relacionadas, como distúrbios
alimentares, disfunção menstrual e saúde óssea em atletas com deficiências. A literatura sugere que esses atletas, dependendo do
tipo de deficiência, tenham maior risco de desenvolver LEA. Desta forma, o objetivo desta revisão é descrever o impacto da LEA
na saúde e desempenho das atletas mulheres, com foco especial em atletas com deficiência. Uma revisão narrativa da literatura foi
conduzida usando como termos de busca os componentes LEA e TRIAD - saúde óssea e disfunção menstrual - em atletas
mulheres. A revisão narrativa produziu 24 estudos sobre o assunto, desses, 10 estudos originais, nos quais LEA foi diagnosticada
em atletas mulheres, apenas um referente a atletas com deficiência. A literatura indica a complexidade na estimativa de EA, uma
vez que os métodos utilizados para determinar seus componentes podem apresentar imprecisões, especialmente para os atletas
com deficiência. Pesquisas adicionais são necessárias para avaliar EA em atletas mulheres, especialmente com deficiências, bem
como a melhoria dos métodos de avaliação e seleção da EA.
Palavras-chave:
baixa energia disponível; atletas do sexo feminino; atletas com deficiência.
INTRODUCT ION
In the last decades, the idea about women being less capable of engaging in sports at all levels has
changed (Slater et al., 2016), with an increase in their participation in Olympic and Paralympic sports
(Matzkin, Curry & Whitlok, 2015; Blauwet, 2015). For instance, in London 2012 Olympics, there was an
increase of 44% in women's participation in comparison with the last two decades (IOC, 2017). In the
Paralympic Games, only two females participated in archery in their first edition in 1948, while in London
2012, there were 1501 female athletes representing eighteen of the twenty sports of the summer games
program (Blauwet, 2015). For the Paralympic Games in Rio de Janeiro 2016, the number of female athletes
increased by 9.9% when compared to London, 2012 (IPC, 2016).
With the greater participation of female in sports, especially athletes with disabilities, there is a growing
need for a deeper understanding and attention to minimize athletes' health problems and injury risk. In the
case of athletes with disabilities, there may be specific problems related to the different types of impairments
that should be taken into consideration (Blauwet, 2015; Slater et al., 2016).
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In recent years, research on female athletes has emerged with a focus on low energy availability (LEA),
and its relationship to the Female Athlete Triad (TRIAD), and more recently, to the Relative Energy
Deficiency in Sport (RED-S): LEA has been considered as the prime factor in both syndromes (Souza et
al., 2014; Mountjoy et al., 2015; Slater et al., 2016). However, it is important to recognize that studies on
LEA and people with disabilities are scant (Broad & Burke, 2013).
The consequences of the energy deficiency in athletes, mainly female, has been discussed by the
International Olympic Committee since 1993 (Loucks, Kiens & Wright, 2011; Slater et al., 2016). The
TRIAD was initially described as a set of symptoms that consisted of eating disorder, amenorrhea, and
osteoporosis (ACSM, 2007; Matzkin, Curry & Whitlok, 2015). In 2007, the American College of Sports
Medicine (ACSM) reviewed the concept of TRIAD and described it as the interrelationship of three
components: LEA with or without eating disorder, low bone density and dysfunction of the menstrual cycle
(Souza et al., 2014; Mountjoy et al., 2015). In 2014 a new position on the subject was published, with a
proposal of risk assessment to assist professionals in the identification and follow-up of TRIAD (Mountjoy
et al., 2014; Souza et al., 2014).
Due to its importance, the objective of this review is to describe studies on LEA in female athletes,
especially female athletes with disabilities, and their impact on health and performance, allowing a greater
understanding of the subject to the professionals that work with this population, as well as to encourage
further research.
METHOD
A literature review was conducted from February to March 2017, using PubMed and Virtual Health Library
databases, to identify articles focused on LEA in female athletes with and without disabilities, conducted in
the last 10 years. The TRIAD components - bone health and menstrual dysfunction - were also researched
in association with LEA in female athletes, with a primary focus on female athletes with disabilities. We
included in the scope of the research original articles, reviews, book chapters and thesis (master/doctoral)
using the following terms: “low energy availability”, “bone mineral density” “menstrual dysfunction”,
“eating disorder”, “female” and “athletes” or "para athletes" (focusing on four major groups of “visual
impairment”, “cerebral palsy”, “spinal cord injury” and “limb deficient or amputee”). The initial search
resulted in a total of 99 search results. Three book chapters identified in the references of the articles and a
master's thesis were also included, totaling 103 results. The references were than selected according to the
following inclusion criteria: studies published in English, Spanish and Portuguese, and conducted with
female athletes. Results with animal studies, clinical studies, studies with intervention (i.e. dietary
supplements), non-athlete population, and male subjects were excluded, totaling 79 results. After deleting
the duplicated articles, the final selection resulted in 24 search results (20 articles, three book chapters and
a master's thesis) as demonstrated in Figure 1.
Figure 1. Review organization.
ENERGY AVAILABILIT Y IN FEMALE ATHLETES WITH DISABILITIES
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RESULTS
Energy Availability
Energy Availability (EA) is defined as the energy intake (EI in kcal) minus the energy expenditure with
exercise (EEex in kcal), divided by Fat Free Mass (FFM in kg), with values equal and above
45kcal/kgFFM/day considered as adequate (Broad & Burke, 2013; Souza et al., 2014), while values below
30kcal/kgFFM/day are considered as LEA (Broad & Burke, 2013).
LEA is described as an energy deficit, in which the body does not have enough energy to meet the
physiological process’ energy demands after the energy necessary to exercise is discounted from the
equation (Melin et al., 2014; Mountjoy et al., 2015). This concept distinguishes itself from the energy balance
(EB) concept, since athletes can be in negative energy balance due to suppression of physiological functions,
in an attempt to restore the energy balance (EB = 0 kcal) and/or the stability of the body mass (Souza et
al., 2014; Slater et al., 2016).
LEA can be a consequence of an inadequate manipulation of the EI, whether intentional or not, and
can happen when there is an eating disorder, when the athlete is trying to reduce body mass and fat
percentage, or when the athlete is incapable of adjusting EI to an increase in EEex (Broad & Burke, 2013;
Souza et al., 2104). LEA may trigger changes in basal metabolic rate, menstrual function, bone health,
protein synthesis, immunity and cardiovascular health, with a consequent decrease in performance (Broad
& Burke, 2013; Souza et al., 2014; Mountjoy et al., 2015).
Low Energy Availability
LEA is particularly common in sports that require body mass control (e.g. combat sports, running), in
sports in which the aesthetic component is an important factor (e.g. rhythmic gymnastics, ballet, skating
and synchronized swimming), and gravitational sports, in which a high body mass restricts movement
against gravity (e.g. artistic gymnastics, cross-country skiing, mountain-biking and jumping in athletics)
(Mountjoy et al., 2014; Matzkin, Curry & Whitlok, 2015; Muia et al., 2016).
There are few studies in which all LEA components (EI, EEex and FFM) were evaluated. Table 1
summarizes the findings of studies conducted in female athletes.
Reed, Souza & Williams (2013) investigating the prevalence of EA during one season of a female soccer
team of the first division, observed a prevalence of LEA of 26%, 33% and 12% of the athletes, respectively
in pre, during and post-competition periods. The authors reported that LEA in pre-competitive and
competitive periods occurred due to the decrease in food intake, while the increase of the EA in the post-
competitive period was due to the reduction in the EEex.
Melin et al. (2015) evaluated the effects of LEA and menstrual dysfunction in female endurance athletes
on energy metabolism. Athletes who presented low/reduced EA demonstrated a lower resting metabolic
rate, besides the reduction of pulses of luteinizing hormone (LH) values in comparison to the athletes with
adequate EA. Muia et al. (2016) evaluated Kenyan adolescent runners and observed that 17.9% of athletes
presented LEA associated with eating disorder, 8.9% had LEA associated with menstrual dysfunction, and
3.3% of athletes presented clinical signs of eating disorder and menstrual dysfunction.
Koehler et al. (2013), evaluated EA in 185 female young athletes and its relationship with leptin, insulin,
insulin-like growth factor 1 (IGF-1), and triiodothyronine (T3). The authors observed a high concentration
of leptin in athletes with LEA. In contrast, insulin, IGF-1 and T3 did not differ between athletes with LEA
and adequate EA.
Joaquim (2016) assessed eight track & field female Paralympic athletes with visual impairment, all
runners, during four days and found two athletes with LEA, two with adequate energy intake and four, in
a vulnerable range (between 30 and 45 kcal/kg FFM). In this unprecedented study with Paralympic athletes,
food intake was assessed using 24-hour photographic register (conducted by the researcher), exercise energy
expenditure was measured using actigraphy, and FFM was estimated using skinfolds and Jackson & Pollock
equations.
It is important to emphasize the complexity of estimating EA, since the methods used to determine its
components may present inaccuracies (Souza et al., 2014). The FFM (kg) estimate is the most challenging
in athletes with disabilities because of the types of impairment and their specificities, and the absence of a
gold standard for measurements (Blauwet et al., 2017). Therefore, to date there is little information about
LEA and its consequences on athletes with disabilities.
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Table 1. Review about Energy Availability.
Authors
Age
Public
Body
composition
EEex (kcal/hour)
EI (kcal/day)
EA (kcal/kgFFM/day)
Hoch et al
2009
80 female athletes of varied
sports
DXA
PA record converted in MET
3-days food diary
36% of the athletes presented reduced EA*, 6% of which
presented LEAα
Koehler et al
2013
185 female athletes
of different modalities
BIA
PA record converted in MET
6-days food registry
EA Mean value: 20.5 kcal/kgFFM/d
Reed, Souza
& Williams
2013
19 soccer players
DXA
Heart rate monitor and PA
record
3-days diet logs
EA mean value 35.2 kcal/kgFFM/d - middle of the season and
44.2 kcal/kgFFM/d - end of the season
Coelho et al
2014
24 tennis players
DXA
PA record converted in MET
3-day food record
87.5% of the athletes presented reduced EA*, 33.3% of which
presented LEAα
Melin
et al
2014
84 female endurance
athletes
DXA
Heart rate monitor
7-days food record
63% of the athletes presented reduced EA*.
Melin
et al
2015
40 female athletes
endurance sports
DXA
Heart rate monitor and PA
record
7-days food record
17 athletes presented reduced EA (mean values:
38.5kcal/kgFFM/d) and 8 presented LEA (mean values
19.1kcal/kgFFM/d)
Viner et al
2015
4 female cyclists
DXA
Heart rate monitor and PA
record
3-days dietary
records
EA mean values: pre-season 26.2kcal/kgFFM/d, competition
24.5kcal/kgFFM/d off-season 23.8kcal/kgFFM/d
Muia
et al
2016
61 female athletes and 49
female non-athletes
Skinfold
PA diary
5-days weighed
dietary record
EA mean values: 36.5kcal/kgFFM/d for athletes and
39.5kcal/kgFFM/d for non-athletes
Silva &
Paiva
2016
67 rhythmic gymnasts
BIA
PA record
24-hour food recall
29.7kcal/kgFFM/d for gymnasts 16-18 year sold and
32.2kcal/kgFFM/d for gymnasts 19- 26 years old
Joaquim
2016
8 female Paralympic
sprinters
Skinfold
PA monitor
4-days
photographic
register
EA median values: 32.5 kcal/kgFFM/d
DXA: dual-energy X-ray absorptiometry; BIA: Bioelectrical Impedance Analysis; PA: Physical activity
*<45kcal/kg/FFM/day; α <30 kcal/kg/FFM
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Blauwet et al. (2007) alert to the fact that some athletes with disabilities may present a higher risk of
developing LEA due to type of impairment (Broad & Burke, 2013; Mountjoy et al., 2014). In a pioneering
review on LEA and its consequences on athletes with disabilities, these authors indicated that athletes with
cerebral palsy have increased energy expenditure due to the presence of athetosis, spasticity, or ataxia, while
motor alterations in the oral functionality, can reduce food intake and consequently energy, increasing risk
of LEA. Athletes who are limb deficient, especially those bipedal, have a higher energy expenditure due to
the inefficacy of walking, which increases EEex and may increase the risk of LEA if intake is not properly
adjusted.
LEA and Menstrual Dysfunction
Menstrual function is an important health aspect of female athletes (Blauwet et al., 2017). The desired
status – eumenorrhea - is defined as the regular menstrual cycle, which occurs between 21 and 35 days
(Mountjoy et al., 2014; Matzkin, Curry & Whitlok, 2015). The absence of menstruation is known as
amenorrhea. Primary amenorrhea occurs when menarche is not present up to 15 years of age and secondary
amenorrhea is the absence of three menstrual cycles after menarche, while oligomenorrhea is considered
when less than nine menstrual cycles occur in one year (Márquez & Molinero, 2013; Matzkin, Curry &
Whitlok, 2015).
LEA, associated with low body fat stores and intense exercise, can lead to menstrual disorder. This is
due to the reduction in the levels of hormones such as gonadotrophin releasing hormone (GnRH) and LH,
which suppresses the hypothalamic-pituitary-ovary axis causing reduction in estradiol levels and menstrual
dysfunction (Nazem & Ackerman, 2012; Márquez & Molinero, 2013; Mountjoy et al., 2014; Matzkin, Curry
& Whitlok, 2015). A fast reduction of body fat can also compromise menstrual function, as the consequent
alteration in leptin has a positive effect on GnRH production, regulating the release of gonadotrophins,
and contributing to amenorrhea (Nazem & Ackerman, 2012; Mountjoy et al, 2014).
The prevalence of menstrual dysfunction in athletes varies among different sports groups, however it
is higher than in non-athletes (Dadgostar et al., 2009; Mountjoy et al., 2014). Dadgostar et al. (2009)
evaluated the prevalence of amenorrhea and oligomenorrhea in Iranian athletes of different sports and
observed that a higher prevalence of menstrual dysfunction in athletes who seek a lean body and a low
body fat percentage. The authors highlighted the need to develop a constant work of nutritional education
with athletes.
Data on menstrual function of para athletes is lacking (Blauwet et al., 2017). Blauwet et al (2017)
reported that non-athletes with spinal cord injury did not show significant impact of the injury on menstrual
function, which resumed months after the injury. The authors also reported that no study examined the
decrease in fertility as a result of LEA.
LEA and bone mineral density (BMD)
Bone is a living tissue composed of connective tissue, protein and deposits of calcium and phosphorus,
having as main characteristic the strength and resistance (Constantini & Lebrun, 2015). Healthy bones are
key to injury prevention and performance optimization (Blauwet, 2015). The literature reviewed shows that
low bone mineral density varies according to the method used to assess it (Matzkin, Curry & Whitlok, 2015;
Slater et al., 2016). The gold-standard method for assessing bone mineral density is the dual-energy X-ray
absorptiometry (DXA) of the lumbar spine and femur (Mountjoy et al., 2014; ISCD, 2015). The
International Society for Clinical Densitometry (ISCD) (2015) indicates a Z-score below -2.5 or less in the
femoral neck as abnormal for osteoporosis, while low bone mineral density (osteopenia) can be defined as
a Z-score between -1.0 and -2.0 associated with low levels of estrogen, stress fractures and nutritional
deficiencies, mainly consumption of inadequate energy, calcium and vitamin D (Márquez & Molinero,
2013).
Healthy athletes may have 5 to 15% higher bone density mass than non-athletes, because exercise plays
an important role in the accretion and increase of bone density. However, it is known that athletes with
amenorrhea have lower bone density (Márquez & Molinero, 2013; Mountjoy et al., 2014). For non-
ambulatory athletes, BMD decrease may be due to low body mass, aggravated by age, and in association
with TRIAD (Blauwet, 2015).
In a review by Blauwet et al. (2017), the authors found only one study that evaluated BMD of track &
field athletes with hemiplegic cerebral palsy, finding no difference between BMD on the affected side and
the unaffected side. Although few information is available on visually impaired athletes’ bone health, there
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200
is a relationship between lack of vision and a higher incidence of fractures by falls. The authors also reported
that no studies on bone mineral density and amputees and short stature were found.
Female athletes with spinal cord injury may present reduced BMD, especially below the injury level
(Blauwet, 2015). This lower bone mineral density has been associated with the reduction of estrogen in
comparison to athletes without disability and there is a relationship between time after injury and a
significant loss of bone mineral density (Blauwet et al., 2017).
DISCUSSION
The results demonstrate the dearth of information regarding LEA, as well as its association with bone
mineral density and menstrual dysfunction in athletes with disabilities. However, LEA is a condition that
athletes with disabilities and the professional team working with them should be fully aware of, both
because it may be present due to factors common to all athletes, but also due to specificities related to some
disabilities.
One of the main reasons for the lack of studies is the complexity of EA assessment. The methods used
for assessment are highly complex or may present a bias in the in athletic population with disabilities (Souza
et al., 2014), and are difficult to apply in the everyday practice. Determining the components of EA in
athletes with disabilities has its own challenge, due to the lack of data available on the different impairments
and exercise modalities.
EI can be assessed by different methods, such as food registers or the 24-hour food recall, however,
for any population, both methods can often generate underestimated intake values due to intentionally or
unintentionally underreporting.
The use of available MET values and equations to determine EEex can be inaccurate due to the
difference in the amount of functional muscle mass in athletes with disabilities and/or other factors related
to the disability, which can influence energy expenditure, such as: level of injury in spinal cord injury
athletes, asymmetry of movements due to gait imbalance due to amputation or type of cerebral palsy (Broad
& Burke, 2013). It has been suggested that the use of technological tools, such as the physical activity
monitors (pedometers and the accelerometers), may assist in EEex assessment, although they are not yet
able to accurately assess (Broad & Burke, 2013) EEex in athletes with disabilities as those devices have
internal programming softwares based on populations without disability, which may not be appropriated.
Furthermore, the FFM (kg) estimate is most challenging in athletes with disabilities because of the types
of deficiency. The assumption of most methods may not be appropriate to those athletes and there is no
gold standard for measurement in this population (Blauwet et al., 2017).
In search of a tool to evaluate LEA, as well as to identify the TRIAD, Melin et al. (2014), sought to
validate the reliability of the “Low Energy Availability in Female Questionnaire (LEAF-Q)” in female
athletes. The authors concluded the LEAF-Q is an instrument with acceptable sensibility (78%) and
specificity (90%) to assessing/screening the EA in female athletes who may be at risk of TRIAD. Folscher
et al (2015) sought to assess the risk of developing TRIAD in South African marathoners using LEAF-Q.
The authors observed that 44.1% of the athletes presented a risk of developing TRIAD and that one-third
of the athletes were in LEA due to eating disorder. No data were found for LEAF-Q in para athletes.
Further studies validating this instrument in the population of athletes with disabilities should be stimulated.
CONCLUSION
Although in female athletes without disabilities LEA, menstrual dysfunction and low bone mineral density
have been fairly studied, this review has demonstrated the gap in information regarding female athletes with
disabilities. Further research is necessary to elucidate these conditions in this population, as well as to assess
their knowledge on EA.
It is essential to improve the methods used to evaluate EA components in athletes with disabilities. In
addition, it is important for the interdisciplinary team to be aware of the consequences of LEA related to
health and performance and to promote awareness among athletes on the importance of a healthy diet.
Although this review focused the female athletes, research on male athletes, both with and without
should also be stimulated as they can also be at risk of developing RED-S.
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ENERGY AVAILABILIT Y IN FEMALE ATHLETES WITH DISABILITIES
JUZWIAK, JOAQUIM, AND WINCKER (2018)
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MINIBIO
Claudia Ridel Juzwiak (claudia.juzwiak@unifesp.br)
ORCID: https://orcid.org/0000-0003-1101-0063
Nutritionist (1988), Specialist in Clinical Nutrition by the Universidade Católica
de Santos (1996), MSc in Applied Sciences to Pediatrics by the Universidade
Federal de São Paulo – UNIFESP (2001), and PhD in Sciences by the Pediatric
Program of the Universidade Federal de São Paulo (2006). She holds the title of
Specialist in Clinical Nutrition and Sports Nutrition by the Associação Brasileira
de Nutrição - ASBRAN (2008). She developed her Postdoctoral Research
Program in the area of Food Anthropology at the Observatori de l’Alimentació
(ODELA) of the Universitat de Barcelona, sponsored by CAPES (2015). She is
currently an Associate Professor at the undergraduate degree in Nutrition of the
Universidade Federal de São Paulo - UNIFESP and of the Post-Graduation
Programs in “Health Sciences Teaching” and in “Interdisciplinary Health
Sciences”. She is a member of the Brazilian Paralympic Academy. She works in
the areas of sports nutrition and and nutrition education.
Curriculum Lattes: http://lattes.cnpq.br/5232412496774556
Daniel Paduan Joaquim (daniel_paduan@hotmail.com)
ORCID: https://orcid.org/0000-0002-9356-2410
Nutritionist, graduated from the Universidade Católica de Santos (2006). Post-
graduate in Exercise Physiology at the Center for Exercise Physiology Studies
by the Universidade Federal de São Paulo – UNIFESP (2010). He holds a
master’s degree in health sciences by the Interdisciplinary Program in Health
Sciences of the Universidade Federal de São Paulo (2016). He currently works
as nutritionist of the Brazilian Paralympic Committee (CPB). He has experience
in Sports Nutrition with emphasis on Paralympic athletes and in the
development of nutritional education projects.
Curriculum Lattes: http://lattes.cnpq.br/6358823331747866
Ciro Winckler (ciro.winckler@unifesp.br)
ORCID: https://orcid.org/0000-0002-9595-8144
Associate Professor at the Universidade Federal de of São Paulo - UNIFESP.
He works in the undergraduate degree in Physical Education and in the Stricto
Sensu postgraduate program in Human Movement and Rehabilitation Sciences.
PhD in Physical Education, in the area of concentration of Physical Activity,
Adaptation and Health, completed in 2006 at the Universidade Estadual de
Campinas. The master's degree was held in the same institution and finished in
2002. Member of the Brazilian Paralympic Academy. He is currently the
Coordinator of High Performance of the Institution. Participated in 5 editions
Summer Paralympic Games (2000-2016).
Curriculum Lattes: http://lattes.cnpq.br/2067947156482139