The Role of Energy Availability in Reproductive Function in the Female Athlete Triad and Extension of its Effects to Men: An Initial Working Model of a Similar Syndrome in Male Athletes

Abstract

The Female Athlete Triad represents three interrelated conditions of (i) low energy availability (energy deficiency), presenting with or without disordered eating, (ii) menstrual dysfunction, and (iii) poor bone health, each of which can exist along a continuum of severity ranging from mild and moderate subclinical health concerns to severe clinical outcomes, including eating disorders, amenorrhea, and osteoporosis. This review provides a brief overview of the Female Athlete Triad, including updating the current thinking regarding energy availability and how it relates to reproductive function, and sets the stage for an initial working model of a similar syndrome in males that will be based on currently available evidence and will later be defined and referred to as a Male Athlete Triad by the newly re-named Female and Male Athlete Triad Coalition. A primary focus of this paper will be on the physiology of each Triad model with an emphasis on low energy availability and its role in reproductive function, with a brief introduction on its effects on bone health in men. From the data reviewed, (i) a specific threshold of energy availability below which menstrual disturbances are induced is not supported; (ii) it appears that the energetic, reproductive, and bone systems in men are more resilient to the effects of low energy availability compared to those of women, requiring more severe energetic perturbations before alterations are observed; and (iii) it appears that recovery of the hypothalamic pituitary gonadal axis can be observed more quickly in men than in women.

Fig. 1

Comparison of evidence available to date regarding the effects of low energy availability on reproduction and bone health in exercising men. a The Female Athlete Triad represents a spectrum of energy availability, menstrual health, and bone health status. Within each health category, individuals may vary from optimal health (denoted in green) to compromised health (orange) to a pathological health status (red). b Summary of effects of low energy availability on metabolism, reproduction, and bone health in men supporting the possibility that a similar Triad-like condition may exist in exercising men. REE resting energy expenditure, T₃ triiodothyronine, PYY peptide YY, IGF-1 insulin-like growth factor 1, LH luteinizing hormone, P1NP N-terminal propeptide of type I collagen, CTx C-terminal telopeptide type I collagen, BMD bone mineral density, BSI bone stress injury, – indicates no change, ↓ indicates reduced, ↑ indicates increased, ?? indicates unknown

Fig. 2

a Average daily energy deficit (%) experienced across study phases and,  b sum of all menstrual disturbances across the intervention for each group. Data are reported as mean ± SE. a ^aED1 significantly different from EXCON; ^bED2 significantly different from EXCON; ^cED2 significantly different from EXCON and ED1; ^d ED3 significantly different from EXCON, ED1, and ED2. b^asignificantly different from EXCON; ^bsignificantly different from EXCON and ED1. Reproduced from Williams et al. [19], with permission. c Individual EA data and the incidence of MD during intervention and all intervention cycles combined. Y axes notations are 0, no MD indicating an ovulatory cycle; 1, at least one MD indicating a luteal phase disturbance, oligomenorrhea, or anovulation; each dot represents one participant’s average EA and whether that intervention cycle had no or at least one MD. Vertical line denotes the theoretical threshold EA of 30 kcal kg⁻¹ FFM day⁻¹ demonstrated by Loucks et al. [15]. Reproduced from Lieberman et al. [20]. d The predicted probability of experiencing an abnormal menstrual cycle increased to over 50% if energy availability decreased below 30 kcal/kg FFM/day. EA energy availability, EXCON exercising control group, ED energy deficit, Int intervention period, FFM fat free mass, MD menstrual disturbance