Relative Energy Deficiency in Sport
Relative Energy Deficiency in Sport (REDS) is a syndrome of disease characterized by (a) low energy availability or energy deficiency (ED), (b) dysfunctional menstruation and (c) decreased bone mineral density. Formally referred to as the Female Athletic Triad, it was renamed by the International Olympic Committee in 2014 to reflect that that the syndrome can also occur in men.
REDS is most commonly seen in gymnastics, figure skating, ballet, diving, swimming and long distance running. The exact prevalence is difficult to define due to challenges in diagnostic criteria and other overlapping clinical diseases. Disordered eating affects up to 20% of adult female athletes [2]. Primary amenorrhea affects 7% of all college athletes while secondary amenorrhea affects 2-5% of them [3].
Definition & Pathophysiology
Although classically taught as a triad, more accurately defined as a spectrum of illness resulting from a low relative energy availability (EA) due to disordered eating. On one end, healthy eating behaviors with occasional, short term restrictive diets and on the other end, severely abnormal disordered eating with abnormal behaviors, distorted body image, weight fluctuations, medical complications, impaired athletic performance. EA is defined as energy intake (EI) – energy expenditure (EE). Low EI occurs most commonly due to disordered eating and low EI, but can also occur due to increased or mismanaged exercise and training load.
Dysfunctional menstruation can range from light bleeding and abnormal menses, to oligomenorrhea all the way to amenorrhea. This is directly linked to low EA. Functional Hypothalamic Amenorrhea (FHA) is a term often applied to these athletes which is defined by persistent anovulation with no identifiable organic cause. Dysmenorrhea is defined by variad degrees of decreased gonadotropic releasing hormone (GnRH), luteinizing hormone (LH), follicle-stimulating hormone (FSH) resulting in decreased release of estrogen, progesterone and alterations in menstrual cycle.
Decreased bone mineral density (BMD) is the 3rd arm of this triad. Peak bone mass in adults occurs around age 20 and slowly decreases as we age. In athletes, BMD is usually 10-15% greater than non athletes. In athletes with REDS, the decrease in estrogen and progesterone leads to negative effects on bone mineral density increasing risk of stress fractures, injuries, impaired performance and reduced responsiveness to training.

Figure 1. Health consequences of relative energy deficiency in sport (RED-S) showing an expanded concept of the female athlete triad to acknowledge a wider range of outcomes and the application to the male athletes. Psychological consequences can either precede RED-S or be the result of RED-S. (adopted from constantin)
Other Manifestations
Although REDS is defined by the presence of low energy availability, dysmenorrhea and low bone mineral density, there are many other manifestations that athletes may experience. This includes other endocrine dysfunction including insulin, cortisol, growth hormone and thyroid function. Abnormal regulatory appetite hormones including ghrelin, leptin, peptide YY and adiponectin. Impaired glucose metabolism with elevation in free fatty acids and ketones. Dysfunctional muscle protein synthesis.

Figure 2. Potential performance effects of relative energy deficinecy in sport. *Aerobic and anaerobic performance. (adopted from Constantini)
History/ Physical Exam
When obtaining history, it is important to clarify eating habits and caloric intake. Physicians should also ask about body image, recent training changes, history of stress injuries medication and supplement use, sleep patterns and knowledge of energy balance. In women, careful review of menstrual history should be done. Athletes may report a wide range of symptoms including disordered eating, fatigue, hair loss, dry skin, weight loss, increased recovery time, loss of menses, low self esteem and depression.
On a physical exam, you may see lanugo, parotid gland enlargement, dry mucous membranes. Skin can demonstrate hypercarotenemia, acne or hirsutism. Cardiovascular symptoms include bradycardia most commonly and orthostatic hypotension. It is important to document tanner staging and an an external pelvic exam may demonstrate vaginal atrophy
Screening/ Diagnosis
Screening should be performed as part of an annual health exam. Energy availability can be calculated by a dietician or nutritionist, although this can be difficult and imprecise, especially in small framed athletes. Menstrual dysfunction requires a thorough history of menstruation. It is important to check an HCG. If performing lab work, consider hemoglobin, reproductive labs (LH, FSH, prolactin, estradiol), thyroid studies and androgen studies if appropriate. Bone health is measured using dual-energy x-ray absorptiometry (DXA) and calculating a Z-score. Z scores < -1.0 need to be investigated further while > -1.0 are considered low in athletes. Cardiac screening should be performed using an EKG to look for arrhythmias and prolonged QTc.
Management
Management is primarily aimed at prevention. There are many guidelines from the IOC on prevention for individual athletes and guidelines for healthcare professionals and sports organizations. In general, they emphasize healthy eating and body image and develop realistic, healthy goals about weight and body composition. A multidisciplinary team should include sports physician, nutritionist, psychologist, physiotherapist and physiologist.
Treatment is directed at correcting energy imbalance, addressing menstrual dysfunction, improving bone health, psychological interventions when necessary, and improving performance. Correcting energy imbalance is primarily aimed at increasing energy intake. The calculations can be performed by a nutritionist but a simple rule of thumb is to increase daily caloric intake by 300-600 kcal/day. Staff should also decrease training volume and education is critical. Menstrual dysfunction often improves with weight gain and oral contraception can be considered although it does not correct the primary issue of low energy availability. Bone health often improves with weight gain as well, but athletes should be prescribed high impact loading resistance training. Pharmacotherapy should include calcium, vitamin D and there are several others to consider that are not well studied in REDS. Psychiatric interventions usually involve some form of behavioral therapy and often an antidepressant.
Return to Play & Complications
Return to play decisions are driven by the guidelines from the IOC Consensus group, Norwegian Olympic Training Center [1]. Generally speaking, athletes are classified as high-, medium-, or low-risk. High risk athletes should not be cleared to participate, while moderate-risk athletes can return under supervision and frequent re-evaluation. Low risk athletes can return unrestricted with monitoring.
The complications associated with REDS are significant and can not be overstated. They include chronic fatigue, anemia, immunologic (weak immune system, increased risk of infection), cardiovascular, endocrine, reproductive, skeletal, renal and CNS dysfunction. Psychological effects include depression, anxiety and altered perception of normal. Athletes may not be able to return to the same level of competition.
REFERENCES
1. Mountjoy M, Sundgot-Borgen J, Burke L, et alThe IOC consensus statement: beyond the Female Athlete Triad—Relative Energy Deficiency in Sport (RED-S)British Journal of Sports Medicine 2014;48:491-497.
2. Martinsen M, Sundgot-Borgen J. Higher prevalence of eating disorders among adolescent elite athletes than controls. Med Sci Sports Exerc 2013;45:1188–97
3. Abraham SF, Beumont PJ, Fraser IS, et al. Body weight, exercise and menstrual status among ballet dancers in training. Br J Obstet Gynaecol 1982;89:507–10.