Low energy availability: history, definition and evidence of its endocrine, metabolic and physiological effects in prospective studies in females and males

Abstract

Energy availability (EA) is defined as the amount of dietary energy available to sustain physiological function after subtracting the energetic cost of exercise. Insufficient EA due to increased exercise, reduced energy intake, or a combination of both, is a potent disruptor of the endocrine milieu. As such, EA is conceived as a key etiological factor underlying a plethora of physiological dysregulations described in the female athlete triad, its male counterpart and the Relative Energy Deficiency in Sport models. Originally developed upon female-specific physiological responses, this concept has recently been extended to males, where experimental evidence is limited. The majority of data for all these models are from cross-sectional or observational studies where hypothesized chronic low energy availability (LEA) is linked to physiological maladaptation. However, the body of evidence determining causal effects of LEA on endocrine, and physiological function through prospective studies manipulating EA is comparatively small, with interventions typically lasting ≤ 5 days. Extending laboratory-based findings to the field requires recognition of the strengths and limitations of current knowledge. To aid this, this review will: (1) provide a brief historical overview of the origin of the concept in mammalian ecology through its evolution of algebraic calculations used in humans today, (2) Outline key differences from the 'energy balance' concept, (3) summarise and critically evaluate the effects of LEA on tissues/systems for which we now have evidence, namely: hormonal milieu, reproductive system endocrinology, bone metabolism and skeletal muscle; and finally (4) provide perspectives and suggestions for research upon identified knowledge gaps.

Keywords: Energy availability; Energy balance; Exercise; Nutrition; RED-S; Triad.

Fig. 1

Unit-less illustration of an individual’s daily energy balance and energy availability (EA) when exercising and maintaining an energy balance of zero. Energy intake and exercise energy expenditure (EEE) are accounted for equally in both concepts, but energy balance also accounts for all other components of energy expenditure. The illustration represents parameters of a hypothetical case of an individual performing ~ 1 h of purposeful exercise, with energy expenditure from dietary induced thermogenesis and non-exercise activity thermogenesis that are 10% that of energy intake and 40% of resting metabolic rate, respectively. Cold-induced thermogenesis, has not been incorporated in the figure due to minimal energy expenditure in thermo-neutral conditions, though in cold conditions contribution can be significant. EA energy availability, EEE exercise energy expenditure, NEAT non-exercise activity thermogenesis, DIT dietary induced thermogenesis, RMR resting metabolic rate

Fig. 2

Relationship between energy availability (EA) and changes in body weight after 3–5 days (a) using the concept of low energy availability dose’ summarising data from studies manipulating energy availability and measuring weight pre-post intervention (Areta et al. ; Ihle and Loucks ; Koehler et al. ; Kojima et al. ; Loucks ; Loucks and Heath ; Loucks and Thuma ; Loucks and Verdun ; Loucks et al. ; Murphy and Koehler ; Papageorgiou et al. 2017, 2018). The shading of the circles is representative of the female ratio in each study -dark grey means only women and white only men; the error bars reflect the SEM of the weight loss (if available). Low energy availability dose defined as the total amount of EA under 45 kcal/kg LBM/day. There is a strong correlation between low energy availability dose and decrease in body weight. b Exemplifies two different ways of obtaining − 90 kcal/kg LBM low energy availability dose: with 3 days of 15 kcal/kg LBM/day EA (3 days × − 30 kcal/kg LBM/day) or 6 days of 30 kcal/kg LBM/day EA (6 days × − 15 kcal/kg LBM/day)

Fig. 3

Graphical summary of the effects of short-term (3–5 days) low energy availability (EA) on hormones, blood-borne substrates and skeletal muscle as evidenced in prospective studies. Low energy availability is a powerful stressor that triggers marked hormonal and metabolic responses. Down-regulation of key energy homeostasis-related adipokine leptin may lay upstream of and partially modulate the hypothalamic-pituitary-thyroid, hypothalamic-pituitary–gonadal and GH-IGF-1 axes. LEA also modulates markers of bone formation (decrease), resorption (increase), substrate availability and reduces skeletal muscle protein synthesis. Different tissues/systems are affected in different ways, and this response seems to vary between males and females, potentially due to divergent susceptibility to different levels of EA in different tissues and genders. Male or female gender symbol specifies that research supporting the direction of change (or lack thereof) has been conducted or reported on that gender specifically. β-HOB Beta hydroxybutyrate, FSH follicle stimulating hormone, GH growth hormone, IGF-1 insulin-like growth-factor 1, LH luteinizing hormone, T₃ triiodothyronine. Bone formation markers refers to osteocalcin, carboxy-terminal propeptide of type 1 procollagen (P1CP) and N-terminal propeptide of type 1 procollagen (P1NP). Bone resorption markers refers to C-terminal telopeptide of type 1 collagen (β-CTX) and aminoterminal telopeptide of type 1 collagen (NTx)