In early 2014, the International Olympic Committee (IOC) published a consensus statement that introduced the term "Relative Energy Deficiency in Sport" (RED-S) to describe what is currently called the Female Athlete Triad. The IOC authors intended for RED-S to be a more comprehensive, broader definition, which includes the Female Athlete Triad.

Since then, the two terms have come under scrutiny and reassessment. This article presents a summary of the debate surrounding the Female Athlete Triad and RED-S.

History of the Female Athlete Triad
When the Task Force on Women's Issues of the American College of Sports Medicine (ACSM) was assembled in 1992, the term Female Athlete Triad was created to describe the interrelated pathologies of disordered eating, amenorrhea, and musculoskeletal injuries among female athletes. All three components had to be present simultaneously for a diagnosis of Female Athlete Triad. As a result, many female athletes with only one or two of the triad's components were being overlooked.

In 2007, the ACSM updated the diagnostic guidelines, and the Female Athlete Triad was defined as a spectrum of abnormalities in energy availability (EA), menstrual function, and bone mineral density (BMD). Each of the three components are part of a spectrum ranging from normal to increasing degrees of pathology. Now, the female athlete no longer needs to demonstrate pathology in all three components of the triad to be diagnosed with the syndrome. The presence of one or two of the components on the pathologic side of the spectrum falls under the umbrella of the triad (Fig. 1) and may meet the criteria for diagnosis, prompting further assessment and evaluation for the other components.

In 2014, a Female Athlete Triad consensus paper was published by De Souza et al and the Female Athlete Triad Coalition and endorsed by the ACSM, the American Medical Society for Sports Medicine, and the American Bone Health Alliance.

RED-S
As defined in the IOC's Consensus Statement, RED-S is "impaired physiological function caused by relative energy deficiency, and includes, but is not limited to, impairment of metabolic rate, menstrual function, bone health, immunity, protein synthesis, and cardiovascular health." The statement indicates that the underlying problem is "energy deficiency relative to the balance between dietary energy intake and energy expenditure required to support homeostasis, health, and the activities of daily living, growth and sporting activities."

The IOC Consensus Statement also expands the vulnerable population, discussing the susceptibility of male athletes, athletes of non-Caucasian ethnicity, and athletes with a disability to RED-S.

Both a sport risk-assessment model and return-to-play guidelines were developed. The sport risk assessment model serves as a screening tool and classifies athletes into the following categories:

• high risk—red light
• moderate risk—yellow light
• low risk—green light

The return-to-play model uses similar categories to classify athletes returning to sport. It requires a clinical assessment and uses a step-wise approach of evaluation of health status, evaluation of participation risk, and decision modification.

Both models are flexible enough to be used with males and females and a specific athlete's situation. Additionally, both models have been implemented for all ages and disciplines of athletes at the Norwegian Olympic Training Center since 2012.

What all the fuss is about
In October 2014, an editorial written by Mary Jane De Souza, MD, and colleagues and published in the British Journal of Sports Medicine refuted the IOC Consensus Statement. The authors believe that insufficient evidence exists to warrant the adoption of the RED-S framework. They also note many concerns and errors within the IOC Consensus Statement. Dr. De Souza's primary concerns can be summarized as follows:

• Although important, insufficient scientific evidence exists to support the application of the disorder to men, non-Caucasians, and disabled individuals to the extent that a new theoretical construct should be created. This detracts from the focus on the female athlete, the most susceptible population and the one that experiences the most severe effects.
• The "hub-and-spoke" model illustrating the potential health consequences of RED-S is oversimplified and does not focus on the most severe clinical outcomes—energy deficiency, reproductive disorders, and skeletal outcomes. The model also portrays the physiological systems, functions, and mechanisms as independent, whereas these actually operate with synergistic and antagonistic effects.
• Data on consequences of low EA in the scientific literature are primarily for women only. Furthermore, sex differences (such as testosterone promoting bone growth) protect men against the serious reproductive and skeletal consequences that may affect women at less severe levels of energy deficiency.
• The RED-S risk assessment and return-to-play models lack clarity and quantification. Some risk factors (eg, prolonged abnormally low percent body fat) do not specify a range or target number. In addition, the number of risk factors necessary to qualify a patient for each return-to-play category is not specified. 

Dr. De Souza's rebuttal also encourages the broadening of research on low EA in different athletic populations, but emphasizes that the Female Athlete Triad should remain critically important and should not be confused with or overshadowed by RED-S.

In April 2015, the IOC authors responded with an editorial expanding on the original RED-S Consensus Statement. Their response contended that the term Female Athlete Triad has the following limitations:

• Research has shown that men are affected by relative energy deficiency.
• "Athlete" isolates recreational exercisers and dancers that might not identify themselves as athletes.
• "Triad" is inaccurate because there are more than three negative outcomes of low EA and athletes may only have one or two of the original components.
• It is unclear as to why the three triad components are the most severe clinical outcomes and why other consequences are not given more priority.
• Triad doesn't prioritize energy deficiency despite data showing it as the causative element.
• The Triad model does not portray the interrelatedness of all of the factors.
• In addition, the authors noted the following:
• Although most studies are on female athletes, male athletes are indeed also affected by low EA. Male athletes might have a different set of issues, but any consequences caused by inadequate EA should be worthy of study.
• The RED-S risk assessment and return-to-play conceptual models are simplified because they are meant to be clinical teaching tools, not to show the complex interactions. Additionally, some categories do not specify length or range numbers, because studies on precise numbers do not yet exist. The intention is to give clinicians the flexibility to adapt the models for both male and female athletes, and to use their clinical knowledge and case-specific knowledge to make safe return-to-play decisions.

The IOC authors also published a RED-S Clinical Assessment Tool (RED-S CAT), modeled after the Sport Concussion Assessment Tool (SCAT-3), along with their additions to the RED-S Consensus Statement. The RED-S CAT includes the red light/yellow light/green light sport risk assessment and return-to-play models from the 2014 Consensus Statement, as well as a treatment contract. The IOC authors hope that the RED-S CAT will support and facilitate the management of both male and female RED-S athletes.

Where do we go from here?
We encourage medical professionals to read both the IOC Consensus Statement on RED-S and the consequent rebuttals, and to form their own personal opinions on this bone of contention.

Caroline Hu, BA, is a research assistant for women's sports medicine in the department of orthopaedic surgery at Brigham and Women's Hospital, and a medical student at the University of Minnesota Medical School. Elizabeth G. Matzkin, MD, is surgical director of women's musculoskeletal health at Brigham and Women's Hospital, and a member of the AAOS Women's Health Issues Advisory Board. She can be reached at ematzkin@partners.org

Putting sex in your orthopaedic practice
This quarterly column from the AAOS Women's Health Issues Advisory Board and the Ruth Jackson Orthopaedic Society provides important information for your practice about issues related to sex (determined by our chromosomes) and gender (how we present ourselves as male or female, which can be influenced by environment, families and peers, and social institutions). It is our mission to promote the philosophy that male and female patients experience and react to musculoskeletal conditions differently; when it comes to patient care, surgeons should not have a one-size-fits-all mentality.

References:

• Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini N, et al: The IOC consensus statement: Beyond the Female Athlete Triad—Relative Energy Deficiency in Sport (RED-S). Br J Sports Med 2014 Apr;48(7):491-497. Accessed on November 12, 2015.
• De Souza MJ, Williams IN, Nattiv A, Joy E, Misra M, et al: Misunderstanding the female athlete triad: Refuting the IOC consensus statement on Relative Energy Deficiency in Sport (RED-S). Br J Sports Med 2014 Oct;48(20):1461-1465. Accessed on November 12, 2015.
• Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP; American College of Sports Medicine: American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc 2007;39(10):1867-1882. Accessed on November 12, 2015.
• Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini N, et al: Authors' 2015 additions to the IOC consensus statement: Relative Energy Deficiency in Sport (RED-S). Br J Sports Med 2015 Apr;49(7):417-420. Accessed on November 12, 2015.
• Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini N, et al: The IOC relative energy deficiency in sport clinical assessment tool (RED-S CAT). Br J Sports Med 2015 Apr;49(7):421-423.