Female Athlete Triad or RED-S?

The Female Athlete Triad, a syndrome resulting from the combination of eating disorders (or low energy availability), amenorrhoea/oligomenorrhea and decreased bone mineral density (osteoporosis and osteopenia), is at the center of a recent naming controversy.

Critics say “The Triad” is too restrictive a definition, and that the syndrome should be instead referred to as the “Relative Energy Deficiency in Sports (RED-S)”, citing evidence that low energy availability has a wider range of adverse effects not only in female athletes, but in their male counterparts as well. Not everyone believes that there is enough evidence to back up these claims, however.

Katherine Black, Ph.D., senior lecturer, department of Human Nutrition at the University of Otago in New Zealand and colleagues addressed these conflicting viewpoints in their review article, “Low Energy Availability in Exercising Women: Historical Perspectives and Future Directions” in the February 2017 issue of Sports Medicine.

HERstory: Women and Exercise

To help explain the controversy swirling around the Female Athlete Triad, the authors first delved into the historical development of the syndrome. Despite animal studies as early as the 1930s suggesting that the combination of exercise and poor nutrition can cause ovarian atrophy and adrenal hypertrophy, it wasn’t until the late 1960s that the medical community started to raise concerns over the health and performance of female athletes. This was also coincidentally when women’s participation in sports was on the rise. At the 1964 Tokyo Olympic Games, 13% of the athletes were female compared to the 2.2% at the 1900 games.

One of the biggest studies at the time was by Gyula Erdelyi, a Hungarian medical doctor who looked specifically at the effect sports activities had on the menstrual cycle of the female athlete. The researchers observed a small association between too much sports activities and unfavorable menstrual changes.

The body of research on the menstrual cycle of female athletes continued to grow in the 1970s, however, still little was known about the mechanisms by which sports activity disrupted menstrual activity. It wasn’t until the 1980s and early 1990s that the connection was made between disordered eating behaviors, amenorrhea and reduced bone mass, and it was through the work of Anne Loucks, Ph.D., professor at Ohio University and colleagues that a better understanding of low energy availability was developed. They showed that it wasn’t exercise alone, but low energy availability that caused these health concerns.

Triad vs. RED-S

In 1992, the American College of Sports Medicine (ACSM) gathered a group of leading experts to create the first position stand on the health of female athletes, and it was during these meetings that the term, “the female athlete triad” was first coined. The purpose of the position statement which was published in 1997 was to make physicians, trainers and anyone who treats female athletes aware of this syndrome defined as “the combination of disordered eating, amenorrohea and osteoporosis found in physically active girls and women.”

From the beginning there were concerns about the definition. Some critics of the original position statement worried that the definition of the Triad was too restrictive focusing on only three components.

To better promote education and research on the adverse effects of low energy availability in women, the Female Athlete Triad Coalition (FATC) was formed in 2002 and in 2005 the International Olympic Committee (IOC) released its first position statement on the Triad which expanded on the ACSM’s 1997 position stand, but also included risk factors and prevention strategies. Meanwhile the ACSM had also been working on updating their 1997 position stand since 2003, but publication was delayed due to concerns that promoting the Triad would dissuade women from participating in sports. The British Journal of Sports Medicine published an article in June of 2006 entitled, “The myth of the female athlete triad” in which this concern as well as others was voiced.

The new ACSM position stand finally published in 2007 included the idea that each of the three components of the Triad worked on a continuum, recognizing that a female athlete might be at risk for the syndrome even without being diagnosed with an eating disorder, and that she might experience menstrual cycle disruption without amenorrohea or osteopenia without a diagnosis of osteoporosis. The new statement also emphasized how energy availability can be reduced by extreme dietary restriction, excessive exercise or a combination of both and that female athletes need to avoid low energy availability because it has been proven to negatively affect reproductive function and bone health.

During this time, there was also a growing interest in whether male athletes experienced low energy availability in a similar way to female athletes. The data so far though has been conflicting. One particular study of male cyclists and runners reported that 63% had osteopenia and the male cyclists were three times more likely to have osteopenia of the spine than long distance runners. Another U.S study found that male cyclists had lower free testosterone levels.

The differing views of the Triad really heated up in 2014 when both the FATC and IOC put out markedly different consensus statements on the Triad. The FATC consensus statement included diagnosis, treatment and return to play guidelines for the Triad, while the IOC included a proposal to rename the syndrome RED-S to encompass a larger range of adverse effects including those on the immune, gastrointestinal, cardiac and endocrine systems. IOC also recognized that male athletes might also suffer from the negative effects of lower energy availability too. Critics of the updated IOC statement, however, point out a lack of substantiating evidence.

Call for More Research

Dr. Black and colleagues emphasized in their paper that “while debate over terminology continues, it is important to acknowledge that both parties have a common goal which is to minimize the potential negative health issues amongst male and female athletes, and gain a better understanding of the interplay between energy availability, bone health, the hormonal milieu and associated health problems.”

Dr. Black told OTW that the push for a name change is “mainly to highlight that problems exist beyond just the female athlete with amenorrhea and that those who work with athletes should be aware of these other potential symptoms as a way of potentially highlighting those requiring further investigation before health becomes severely and potentially irreversibly damaged.”

On the concern that women may be discouraged from being physically active, she said that “physical activity is so important for health that really nobody should be discouraged because of the Triad especially as research shows that it is not exercise per-se that is the issue but it is the inappropriate nutritional intakes alongside the exercise which is the problem.”

When it comes to the idea that male athletes are susceptible to low energy as well, she said that more research is needed. “Unlike females we do not have a marker for low energy in males. It seems like they are more robust to being in a state of low energy availability which may mean they can tolerate low energy availability for longer and no study has been able to show [longer term effects],” she said.

“Given the dearth of information on males we are still trying to determine the appropriate markers, study duration and degree of low energy availability therefore the different study protocols will result in conflicting findings.”

Black and her colleagues are also conducting more research themselves. She said, “Including males in the study design is going to be important as we need to get an understanding of the problems in male athletes too, which will probably include many of the symptoms described by RED-S. I think early screening tools to identify those (males and females) at risk is needed in the applied setting. We also need to think and test strategies to intervene should issues be discovered.”

Overall though, Black said, “The researchers have come a long way in our understanding of the issues of energy availability and that the problem is probably a lot broader than initially thought. Therefore given this broader population and potentially the greater number of symptoms associated with it we really need to increase awareness of the health implications in order to help those at risk.”