Introduction
It is essential for athletes to consume sufficient energy, at specific time points (pre, during and post-exercise) to sustain health and performance [
1]. Certain groups of athletes are at a higher risk of having energy intakes that fail to fully satisfy the higher physiological requirements of exercise [
2]. This failure can result in energy deficiency status (result of insufficient caloric intake and/or excessive energy expenditure [
3]) and low energy availability (LEA), which is defined as an individual mismatch between energy intake and exercise, leading to insufficient energy to support normal physiological function [
2]. Long-term energy deficiency status can negatively impact athletic performance, menstrual function, bone health, metabolic rate, exercise recovery, immunity, cardiovascular function, and mental health [
4,
5].
It has been proposed that LEA may be the driving factor for menstrual disruptions, and may be a major contributing factor to the Female Athlete Triad [
6]. In 2007, The American College of Sports Medicine (ACSM) published a position stand on the Female Athlete Triad that identified three interrelated components—LEA with or without disordered eating, menstrual dysfunction, and low bone mineral density [
4]. In 2014, the concept of The Female Athlete Triad was expanded to include the multiple performance detriments, and health-related problems experienced by both male and female athletes, in a new model referred to as Relative Energy Deficiency in Sport (RED-S), which has LEA at its core [
7]. In the same year, the Low Energy Availability in Females Questionnaire (LEAF-Q) was developed, which is a validated screening tool (78% sensitivity and 90% specificity) for the identification of female endurance athletes at increased risk of LEA [
8]. It is recommended that the LEAF-Q is implemented in combination with a validated eating disorders/disordered eating screening tool [
9], such as the Eating Disorder Inventory-3 Referral Form (EDI-3 RF) [
10]. In addition, measurement of LEA-related biomarkers (e.g., leptin, triiodothyronine (T3), estradiol, testosterone and cortisol) can objectively quantify variables that may contribute toward an individual’s energy deficiency status [
11].
Aesthetic sports are defined as those which require well-developed physical capacities (power, speed, endurance, flexibility) as well as technical skill and artistry [
12]. In such sports, elite performers typically exhibit a low fat mass, and/or a low body weight, and the scoring has a subjective component. Due to the important role of body shape and appearance in aesthetic sports, athletes often fail to satisfy energy requirements, by limiting energy intake or increasing energy expenditure through excessive exercise training to achieve body composition goals [
13], which may elevate the risk of LEA [
14].
Chinese elite athletes have previously won Olympic and World Championship medals in aesthetic sports, including trampolining, diving, and rhythmic gymnastics. It has been established that athletes who perform at a high level in aesthetic sports (e.g., rhythmic gymnastics, synchronized swimming, diving, and dancing) in Western countries are at a higher risk of LEA [
12,
15‐
18], however the prevalence of LEA in populations of Chinese athletes has not been established. In China, recreational sports such as Latin dance and aerobics are very popular among women of various ages, and Chinese women participate in such recreational sports in order to maintain physical and mental health, and change their body composition [
19]. Severe weight loss programs and unintentional heavy exercise are two factors which may increase the risk of LEA [
20], and may within this population. Given the potential for risk of LEA in both elite and recreational Chinese athletes, it is necessary to investigate the incidence of the risk of LEA in aesthetic sports, across these two population groups.
The primary aim of this study was to investigate the risk of LEA in female Chinese athletes in aesthetic sports, for elite athletes (ELA) and recreational athletes (REA) using the LEAF-Q, and to assess the risk of an eating disorder, using Eating Disorder Inventory-3 Referral Form (EDI-3 RF). The secondary aim was to quantify (in 14 ELA), body composition, bone mineral density (BMD), and several serum biofactors (estradiol (E2), triiodothyronine (T3), testosterone, cortisol, leptin and ferritin) to determine their relationship with LEA risk.
Methods
Participants
A total of 166 athletes from aesthetic sports, including 52 ELA (age = 20 ± 3 y) from 3 different sports (trampolining, rhythmic gymnastics, aerobics) volunteered to participate in this cross-sectional study. Subjects classified as ELA had recently (within 12 months) competed in a national or international championship event. There were 114 (age = 20 ± 2 y) recreational athletes (REA) from 5 different sports (rhythmic gymnastics, aerobics, dance sport, cheerleading and dance). All REA were currently participating in these sports at Beijing Sport University (BSU). Those classified as REA were not participating at the national/elite level or not classified as an ELA by a sporting organization, but were participating regularly (at least 3 times per week) in one of the selected aesthetic sporting disciplines. Inclusion criteria comprised female participants, aged > 15 years, and regular participation in one of the aesthetic sports, as per the classification criteria stated above for ELA and REA. Participants were excluded from the study if they had a history of chronic illness or metabolic disease. The sub-group of 14 ELA were all current Chinese National Team members, and all were preparing for the 2020 Tokyo Olympic Games. All participants gave signed informed consent in accordance with the latest version of the Declaration of Helsinki and all experimental procedures were approved by the BSU ethics committee (2019109H).
Questionnaires
Low energy availability in females questionnaire (LEAF-Q)
Participants completed the LEAF-Q, which consists of 25 items related to injury history, gastrointestinal function, menstrual function, and the use of contraceptives (e.g., hormonal patches, hormonal ring). There are additional questions on participant demographics, body weight history, previous involvement in sport, training type, and training frequency/volume per week. All completed questionnaires were scored using the LEAF-Q scoring key, with a total score ≥ 8 considered as an increased risk for LEA or Female Athlete Triad. Suggested cut-offs for injuries, gastrointestinal dysfunction and menstrual disturbance are ≥2, ≥2, and ≥ 4, respectively [
8]. Primary amenorrhea is defined as the absence of menarche by the age of 15 years. Secondary amenorrhea is defined as the absence of menses for at least 3 months, and oligomenorrhea is defined as menstrual cycles of longer than 35 days in duration [
4].
Eating disorder Inventory-3 referral form (EDI-3 RF)
Participants completed the validated EDI-3 Referral Form, which is an abbreviated version of the Eating Disorder Inventory-3 (EDI-3) [
10]. The EDI-3 RF includes three scales (drive for thinness, bulimia, body dissatisfaction) and five behavioral symptom questions, which are intended to identify individuals with potential eating disorders or eating pathology. Participants were identified as having a risk of eating disorders based on three criteria: the individual’s body mass index (BMI) only; BMI plus responses to EDI-3 questions about excessive eating concerns; and responses to behavioral questions pertaining to eating disorder pathology [
10].
Body composition and bone mineral density (BMD)
Body composition and bone mineral density were measured using dual-energy X-ray absorptiometry (Lunar iDXA, GE Healthcare, Madison, WI, USA). During the scan, participants remained stationary, in a supine posture, with their arms by their sides and legs together. The typical duration of the whole-body scan was approximately 8–10 minutes (min). BMD was determined for the whole body and for specific body segments (arms, legs, trunk, ribs, hip, and lumbar spine). Low BMD was defined as Z-score between − 1.0 and − 2.0 SD, together with a history of nutritional deficiencies, hypoestrogenism, stress fractures, and/or other secondary clinical risk factors for fracture [
4]. DXA-derived body composition values included body mass, fat mass, and lean mass. BMI was calculated as a ratio of weight to height (kg/m
2).
Blood samples
Blood samples were obtained after an overnight fast, at 7:30–8.10 am, from an antecubital vein. Samples were collected into a 5 ml gel serum tube (Vacuette, Frickenhausen, Germany) and then analyzed for testosterone, cortisol and ferritin concentration, via an enzyme-labeled analyzer (Beckman DXI 800, Beckman Coulter, Fullerton, CA, USA). Measurement of E2, T3 and leptin conducted using ELISA (Infinite F50, Tecan, Switzerland).
Statistical analysis
Data were analyzed using SPSS Statistics, version 21. To determine differences between treatment groups (ELA and REA) and EA status (high-risk and low-risk), parametric data were analyzed using an independent sample t-test, and nonparametric data were analyzed using a Mann-Whitney U-Test. Chi-squared tests were used to determine differences in the prevalence of LEA, ED, injury, gastrointestinal dysfunction, and menstrual disturbance between groups. Pearson correlation coefficients were used to determine the presence of any significant relationships. Differences in body composition, BMD and blood measures between subgroups were analyzed using an independent sample t-test. The statistical significance level was set at p < 0.05.
Conclusions
Our study demonstrates that for Chinese female athletes, elite athletes have a higher risk of LEA than recreational athletes. Further, Chinese elite athletes, who have a higher training volume and training frequency than recreational athletes, have higher LEA risk, menstrual disturbance, and primary amenorrhea than recreational athletes. In addition, LEA risk was found to be associated with decreased E2 concentration and lower bone mineral density. These data may indicate that both elite and recreational groups may require additional education on nutritional strategies which can enhance both performance and health. In conclusion, emphasizing the importance of LEA, and promoting screening and prevention strategies is crucial to achieving the important goal of protecting the health of Chinese athletes involved in aesthetic sports, particularly given the association of LEA with and the potential for a negative impact on health.
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