Introduction
Relative energy deficiency in sports (RED-S) is a more comprehensive term for the condition previously known as the female athlete triad (FAT) ( Fig. 13.1 ). In 2014 the International Olympic Committee (IOC) issued a consensus statement outlining and expanding FAT to a broader definition known as RED-S, which describes the sequelae of the energy imbalance that can occur in athletes (both recreational and professional) who do not meet their daily nutritional needs. This expanded definition reflects emerging evidence that the condition can occur in both males and females and the physiologic impairments extend beyond the components of the triad—energy availability, menstrual function, and bone health. The IOC also suggested that low energy availability can have direct effects on physical health but also overall athletic performance. RED-S recognizes that symptoms occur along a spectrum and that identification of subclinical symptoms should prompt early intervention and treatment to minimize the risks of long-term disease. ,
This chapter will provide an overview of RED-S, including existing definitions, epidemiology and risk factors, proposed pathophysiology, clinical signs and symptoms, screening evaluation, and management. We also provide information about research gaps and special considerations when treating this population. Of note throughout the chapter, male and female refers to sex assigned at birth to reflect the existing literature. This chapter will focus on females given that this is a book covering important topics in pediatric and adolescent gynecology.
Management/treatment
RED-S is defined as any impairment in physiologic functioning caused by relative energy deficiency. This can include menstrual function, bone health, gastrointestinal conditions, hematologic findings, immune function, cardiovascular health, physical injury, impaired athletic performance, and psychological stress. The energy deficiency may be an unintentional mismatch between energy intake and energy spent through exercise or may be intentional because of the presence of disordered eating. Low energy availability (EA) is the hallmark of RED-S; energy availability can be defined as follows :
Energy Availability=Energy Intake (in kcal)−Exercise EnergyExpenditure (in kcal)Fat-Free Mass (in kg)
Prevalence and epidemiology
It is hard to assess the overall prevalence of RED-S due to the spectrum of the disease as athletes may have any number of the components and not necessarily all at the same time. Although any athlete can have issues with energy deficiency, athletes in individual sports and those that focus on weight class, leanness, size/appearance, and endurance are thought to be most at risk. There are also concerns that focusing on a single sport at an earlier age can also increase the athlete’s risk of inadequate/low EA. Several large-scale studies have looked at the population thought to be at most risk—elite female collegiate athletes. Earlier studies looking at triad components in this population found that 27% of athletes reported menstrual disturbance, 6% had low bone mineral density (BMD), and 16% had sustained at least one stress fracture. Later studies looking at the broader RED-S criteria in elite female athletes found that 50% to 80% of athletes reported some component of RED-S, with menstrual dysfunction, bone health, and anxiety being the most common symptoms. It is also important to note that one does not have to be an elite athlete to be at risk for low EA, as one study demonstrated a risk of low EA in up to 45% of recreational athletes.
Etiology and pathophysiology
Low EA is the primary driver and etiology of RED-S. A mismatch between energy taken in through diet and calories expended through exercise results in the downstream sequelae observed in athletes. It can be difficult to accurately assess EA in a person because of the reliability of self-reported intake data and the specialized tools needed for accurate EA measurement. Therefore measuring EA is not routinely recommended. Data suggest that in an active female, adequate energy availability is ≥45 kcal/kg of fat-free mass (FFM) per day, and negative physiologic changes are observed when EA is ≤30 kcal/kg/FFM per day. Low EA may be voluntary, with intentional inadequate oral intake. But for some athletes, inadequate intake is unintentional and not the result of disordered eating, compulsive exercise, or weight control behaviors. Athletes who involuntarily under-fuel and fail to increase caloric and nutritional intake when they increase exercise through additional training or competition requirements may also be predisposed to RED-S ( Fig. 13.2 ).
Although every bodily system is affected by low EA, the triad components have been most studied and described in the literature. Low EA appears to alter the function of the hypothalamic-pituitary-ovarian (HPO) axis by disrupting the pulsatile secretion of gonadotropin-releasing hormone (GnRH), which then affects the downstream secretion of luteinizing hormone (LH) and follicle-stimulating hormone (FSH). Loss of pulsatile LH and FSH secretion results in ovulatory dysfunction and decreased estradiol production ( Fig. 13.3 ). Physiologically, menstrual suppression is an adaptive conservation mechanism to the low EA state, whereby available energy is directed to more essential bodily functions. , This disruption is referred to as functional hypothalamic amenorrhea (FHA), and restoration of EA will restore HPO axis function and ovulation. The exact mechanism is unclear, as there is variability among athletes in terms of the degree or duration of low EA that triggers HPO dysfunction. Other RED-S endocrine effects described include alterations in thyroid function, decreases in insulin secretion, and elevations in cortisol secretion. The anorexigenic and orexigenic hormones of leptin, peptide YY, and ghrelin can also be affected (see Fig. 13.3 ).
Optimal hormonal status (estrogen, testosterone, growth hormone, insulin, and insulin-like growth factor [IGF]-1) is needed to establish and maintain healthy bones. Estrogen plays a critical role in bone development, particularly internal endocortical bone. Estrogen also affects both bone osteoblastic and osteoclastic activity, forming healthy bone and achieving peak bone mass. FHA leads to overall reduced ovarian estradiol production, which can disrupt bone development. Impaired bone health in female athletes with low EA is well established. Although exercise and mechanical loading are known to improve bone health, , , physical activity in the face of inadequate EA will ultimately decrease bone strength. Athletes with menstrual dysfunction are more than twice as likely to develop a stress fracture compared with their eumenorrheic counterparts. Studies have found that low EA as a consequence of calorie restriction may be more harmful for bones compared with excessive exercise. Athletes with low EA demonstrate documented decreases in BMD and disruptions to bone turnover markers and bone microarchitecture; these changes are associated with an increased risk of bone stress injury. Female athletes with low EA and impaired menstrual function have been shown to have lower BMD at the hip, femoral neck, spine, and whole body. , This impairment is associated with menstrual dysfunction, which can range from oligomenorrhea to amenorrhea; these bone changes are not seen in eumenorrheic athletes. The resulting changes in BMD may lead to increased fracture risk. , Although low EA may occur independent of low weight and body mass index (BMI), there is an increased incidence of low BMD observed in females with BMI <17.5 kg/m 2 or weight <85th percentile for age/sex. The risk for injury is higher in athletes with low EA who also have the triad of disordered eating, menstrual dysfunction, and low BMD.
Screening
Screening requires that coaches, trainers, and health care providers working with athletes have an awareness and a high index of clinical suspicion about the manifestations of low EA, which may or may not be associated with disordered eating behaviors ( Fig. 13.4 ). Prior research has shown a general lack of awareness of the disorder. Annual preparticipation examinations should include an assessment of symptoms associated with low EA and RED-S, including regular screenings for any change or disruption in menstrual function, recurrent or nonhealing stress injuries, and disordered or restrictive eating patterns. A normal weight does not exclude the possibility of low EA, and all athletes should be comprehensively asked about their eating and exercise behaviors. The American Academy of Pediatrics preparticipation history form ( https://www.aap.org/en/patient-care/preparticipation-physical-evaluation/ ) incorporates questions looking at specific risk factors, and the IOC has developed a Clinical Assessment Tool (RED-S CAT) that assesses risk factors for RED-S as well as outlining criteria for sports participation and/or return to play , ( Fig. 13.5 ).
When there are concerns for disordered eating behaviors or other psychiatric diagnoses, it is appropriate to have those athletes further assessed by a provider with expertise in the treatment of eating disorders. Several questionnaires have been developed to assess eating behaviors and attitudes in athletes, although they have not been universally validated for all ages, sexes, and levels of athletes. These include the SCOFF, the Eating Attitudes Test (EAT), the Eating Disorder Screen for Primary Care (ESP), the Eating Disorder Examination Questions (EDE-Q), the Brief ED in Athletes Questionnaire (BEDA), and the Low Energy Availability in Females Questionnaire (LEAF-Q) ( Table 13.1 ).
| Questionnaire | Validated | Behavior Based 1 | Symptom Based 2 | Diagnostic vs. Screening Tool |
|---|---|---|---|---|
| Low Energy Availability in Females Questionnaire (LEAF-Q) | Yes, with endurance-trained female athletes | N/A | Provider assessment of symptoms related to low energy availability—GI symptoms, menstrual dysfunction, injury history | Screening |
| Eating Disorder Inventory (EDI) – Drive for Thinness (DT) | No | Self-report of disordered eating attitudes | N/A | Screening |
| Eating Disorder Examination – Questionnaire (EDE-Q) | Yes, for nonactive males and females | Self-report of eating disorder behaviors | N/A | Screening |
| Brief Eating Disorder in Athletes Questionnaire – BEDA-Q | Yes, in adolescent female elite athletes | Self-reported assessment of weight loss intention and history of dieting | Self-reported assessment of body image concerns, desire for weight loss | Screening |
| RED-S Risk Assessment | No | Provider assessment of eating disorder behaviors | Provider assessment of symptoms related to low energy availability—GI symptoms, menstrual dysfunction, injury history | Screening and return-to-play guidelines |
| Eating Disorder Screen for Primary Care (ESP) | Yes: primary care patients, university students, and athletes | Provider assessment of eating disorder behaviors | N/A | Screening |
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Do you restrict your intake to change your weight?
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Do you ever eat in secret or hide/hoard food?
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Do you ever binge, overeat, or feel like you lose control when eating?
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Do you ever do anything to “get rid of” food/calories that you’ve taken in—purging, excessive exercise, diet pills, or laxatives?
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Are you actively trying to lose weight?
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Does your weight affect the way you feel about yourself?
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Do you feel guilty after eating?
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Are you preoccupied with the desire to be thinner?
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Do you have any dizziness with standing?
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Do you have fatigue or headaches?
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Do you have frequent abdominal pain, fullness, or bloating?
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Do you have any issues with constipation?
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Do you have any missed periods or prolonged periods of amenorrhea?
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Have there been any significant changes in your weight in the last 6 months?
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Have you had absences from your athletic training or been restricted from participation in sports because of injury?
A menstrual history should be taken in all female athletes with attention to questions about contraceptive use that may alter bleeding patterns. Age at menarche, menstrual frequency, episodes of missed menses, and duration of periods should be evaluated. Many athletes assume that amenorrhea is normal. However, it is not appropriate for athletes to have a change in their menstrual pattern or amenorrhea when their activity levels increase, and those who experience this should be further assessed for the presence of low EA and/or disordered eating. FHA in RED-S is a diagnosis of exclusion, and other causes of menstrual dysfunction, including pregnancy or contraceptive use, should be assessed before making a RED-S diagnosis.
Manifestations and clinical presentation
Athletes with RED-S can present with a variety of symptoms given all the bodily systems that are affected by low EA. Athletes may present with alterations in their vital signs, including bradycardia, hypotension, orthostasis, or hypothermia. They may also present with decreased energy, fatigue, near syncope, or syncope. Bradycardia may be difficult to assess based on the low resting heart rate present in many elite athletes. Resting metabolic rate is often reduced in athletes with EA as an energy conservation mechanism. As outlined earlier, athletes may also present with changes to their menstrual pattern, which can range from shorter/lighter periods to complete amenorrhea. Athletes may also present with a stress fracture and/or stress injury. Weight loss may be a presenting feature for some individuals, and even in athletes in whom weight loss is appropriate, it is important to ask how patients are losing weight and monitor for precipitous changes in weight, especially if they are associated with other signs of low EA as described earlier. In athletes who have not yet completed their growth and development, particularly those athletes less than 18 years of age, lack of weight gain or arrest of growth should always be a concern. Patients may present with gastrointestinal symptoms such as nausea, early satiety, abdominal pain, constipation, or bloating ( Table 13.2 ).
