Hungry runners – low energy availability in male endurance athletes and its impact on performance and testosterone: mini-review

Abstract

Low Energy Availability (LEA) arises from the inability to cover energy needs and requirements of training or normal physiological functions. This value differs from the energy balance, which takes into account the total daily energy intake compared to all the energy expended, regardless of the amount of fat-free mass. Insufficient energy consumption affects recovery, adaptation processes, increases the risk of injury or illness, so all of this can negatively affect performance. This mini-review is written on research articles in Pubmed database related to LEA in endurance-trained men and its impact on performance and testosterone. This article also clarifies the prevalence of LEA in male endurance athletes and its correlation to Relative Energy Deficiency in Sports (RED-S). LEA occurs in male endurance athletes and correlates with decreased testosterone levels, decreased bone density and also Resting Metabolic Rate. In endurance-trained men, there is great potential for the negative consequences of low energy availability. It can also be said that there are possibilities for primary screening, so we recommend regular check-ups of blood markers, body structure and keeping not only training but also dietary records, which can increase awareness of an adequate energy balance.

Ethical Publication Statement

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Lower body weight can be beneficial for some athletes, especially in endurance, weight-bearing and aesthetic sports disciplines. Sundgot-Borgen and Torstveit (2010)¹ recognised few cases of intentional weight loss or limitation of energy intake to increase endurance performance, relative strength or aesthetics. On the other hand, in this context, we are aware of several risks and consequences of insufficient energy intake for athletes. The effort to achieve the best possible body composition for sport performance may result in Low Energy Availability (LEA). Chronic low energy intake in sport and its consequences for health and performance have been the subject of several studies, most often due to the potential to increase the risk of injury or illness. In the context of exercise-related health risks, LEA has been extensively described in female athletes as a part of the female athlete triad in relation to bone health and menstrual function.² Recently, the International Olympic Committee (IOC) has expanded the triad concept with the term Relative Energy Deficiency in Sports (RED-S) to address the accompanying consequences with LEA on health and performance in both sexes.³ For the purpose of this review, we understand RED-S as a wider spectrum of manifestations affecting components such as the level of resting metabolism, immunity, proteosynthesis, cardiovascular health or other psychological, endocrine and gastrointestinal factors in general. The etiology of RED-S is very complex, but a major aspect of the syndrome is low energy availability, whether associated with or without eating disorders or disordered eating. Research on LEA in male athletes has gained popularity since their official inclusion in the RED-S model by the IOC.³ At the same time, it was described and became the subject of research within the American College of Sports Medicine (ACSM), where this model is recognized as the "Male Sports Triad".(4,5) Despite the slight difference between the concepts from the IOC and ACSM, the term RED-S syndrome will be used in this review. LEA occurs when an energy deficit exists to such an extent that the body has insufficient energy available to meet the needs of training and normal physiological functioning. This is different from energy balance, which takes into account total energy intake compared with all energy expended irrespective of fat-free mass.⁶ Energy Availability (EA) was defined as the amount of energy that remained available to support bodily functions and physiological processes after deducting the energy required for training. It is calculated using the energy intake, subtraction of the energy needed for training and subsequently divided by the value of fat-free mass in kilograms.⁷

Fig 1.

Formula for calculating Energy Availability (Ackerman et al., 2018.(3) Koehler et al., 2016).¹⁰

EA = Dietary energy intake (kcal) minus Exercise energy expenditure (kcal) divided by Fat-Free Mass (kg)

Initially, LEA leads to a negative energy balance and thereby weight loss because the body’s energy reserves (e.g., adipose tissue and body proteins) substantially contribute to fuel needs. Energy availability value of less than 30 kcal/kg/FFM/day for five consecutive days has been shown to disrupt hypothalamic-pituitary axis, resulting in elevated cortisol levels, decreased Triiodothyronine (T3) and Luteinizing Hormone (LH), as well as decreased blood markers of bone formation and reduced blood glucose levels.⁸ However, Loucks (2004)⁹ claims that long-term LEA causes metabolic and physiological adaptations in order to reduce total energy expenditure to prevent further weight loss and promote survival, whereby the body obtains a new energy balance steady state. Therefore, an athlete may be weight stable and not excessively low in body mass or body fat levels yet have impaired physiological function secondary to LEA. As we can see there is no difference if LEA occurs due to low dietary energy intake or energy expanded through exercise is too high. In a study investigating EA in female and male athletes from a mix of sports, more than one-half of the athletes had EA values below the suggested threshold of 30 kcal/kgFFM.¹⁰ The concept of adequate energy availability is under-studied in male athletes, although nutritional deficits have been identified in a subset of athletes. The largest pioneering nutritional study which spanned 8 years and evaluated the diet and nutritional adequacy of the diets using 4 to 7-day food logs among 419 elite male and female Dutch athletes competing in endurance, strength, and team sports. The majority of athletes in all sports consumed inadequate levels of carbohydrates, and athletes of both sexes participating in sports emphasizing leanness were observed to exhibit dieting and under-eating throughout the year.¹¹ LEA research in male athletes has gained popularity since their official inclusion in the RED-S model by the IOC.³ Despite the apparent simplicity of the calculation of energy availability, there are several limitations and pitfalls in the exact quantification of each of the components. There is currently no universal agreement on how to precisely quantify these components, and thus across methodologies we can see discrepancies that need to be taken into account.¹² The first is the reliability and objectivity of energy intake in athletes. It turns out that more often it is a tendency to underestimate energy intake with an error rate of up to 21%.¹³ Furthermore, we recognize the measurement of the energy demand of exercise in the free-living conditions of athletes. The method of doubly labeled water appears to be the most reliable, but its availability for athletes is limited. Another option is accelerometers showing a relatively high agreement with the previous method¹⁴ and then there are popular and easiest available devices such as "smart watches" where the error rate can range up to 600 kcal per day.¹⁵ Several authors emphasize that the use of EA as an absolute value and threshold for determining the development of RED-S conditions of the male athletic triad may not be sufficient due to individual variability and tolerance to EA.(4,5)

Fig 2.

Potential influence of Relative Energy Deficiency in Sports on hormones and sports performance - modified and adapted to male endurance athletes (Mountjoy, 2018).³

In conclusion, the assessment of LEA may face several methodological issues, however, we still consider it as an important concept of nutritional counseling in sports.

Prevalence of LEA

Chronic low energy intake can stem from a variety of reasons: i) lack of knowledge about proper nutrition and nutritional sources to achieve energy balance, ii) lack of time to prepare meals, iii) lack of skills in preparing meals, iv) financial reasons, or v) physiological reasons like loss of appetite after training due to suppression of ghrelin production.¹⁶ In these cases, it is not necessarily a matter of intentionally regulating energy income. In general, it does not matter whether it is an intentional or unintentional restriction of energy income. The consequences are identical in both cases. In the case of intentional control or restriction of energy intake, the most common reasons are dissatisfaction with your body and the desire to change body composition.¹⁷ While most LEA and body image studies have focused primarily on women, on the other hand, there is growing evidence that problems with body image and eating habits are also common in male athletes - as we would like to describe in this minireview. Investigations among sport types demonstrated that athletes who participate in sports emphasizing leanness, including endurance sports (cycling and running), appear to have a greater prevalence of Disordered Eating (DE). Among a sample male cyclists and male non-cyclists, cyclists exhibited a significantly higher overall score on the Eating Attitudes Test (EAT)-26 (indicating more DE), and a higher score on the dieting and binge eating EAT-26 sub-factors.¹⁸ In the largest epidemiological study to date which evaluated the prevalence of Eating Disorders (EDs) elite Norwegian male athletes (n=687) and non-athlete controls (n=629) were studied. Results reported an 8 % prevalence of EDs, including anorexia nervosa, bulimia nervosa, ED not otherwise specified, and anorexia athletica, among the 687 male athletes compared with a 0.5 % prevalence among the 629 male non-athlete controls. Ferrand and Brunet (2004)¹⁹ evaluated a sample of 42 elite male cyclists and found that over 57% had an EAT-26 score. Among a sample of male cyclists, Filaire et al. (2007)²⁰ found that 67% were not satisfied with their weight, 41% dieted to lose weight, and others reported laxative use and increased exercise for weight-control purposes. Three investigations in male runners and cyclists identified low caloric intake in athletes, although food and fluid intake surrounding and during competition largely met recommended levels in most reports.(21-23) Similar to weight class and aesthetic sports, several studies have identified similar deficits in male endurance athletes. One report evaluating 37 male adolescent cyclists and controls found that, despite cyclists exercising fivefold more hours per week than controls, their energy intake (2300 kcal/day) did not significantly exceed that of control subjects and appeared to fall below recommended intake levels based on their level of training. Additionally, intake of calcium, vitamin D, iron, and B vitamins were below recommendations for both cyclists and controls. As we could see in the previous chapter LEA is a widespread phenomenon across several sports for both men and women. It seems that there is a lower risk of low EA in team sports and ball games. Studies investigating EA among male adolescent athletes competing in ball or team sports, such as football, soccer, and ice hockey, indicate sufficient absolute (kcal) and relative (kcal/kg) energy intake, ranging from 40 to 60 kcal/kg FFM.(24,25) In this minireview, we focused on the prevalence of low energy availability of endurance-trained men. Details are given in Table 1 below. The concept of adequate energy availability has not been sufficiently studied in male athletes. Despite the fact that women can be considered risky in terms of the consequences of LEA, for men, LEA, hypogonadism and bone health are three interconnected components.⁴ An electronic database of “Pubmed” was chosen to search for relevant studies. This also included backward search according to the references in the included articles. The keywords "energy availability, endurance, testosterone, male hypogonadism, sports performance, hormones" were used to search for relevant resources. The main selection criterion was that the studies had to deal with low energy availability in endurance-trained men. Furthermore, there was a requirement for a publication date between 2017-2022 and the availability of full-text.

Hypogonadism and testosterone disturbances

The Endocrine Society defines male hypogonadism as a clinical syndrome resulting from the failure of the testis to produce physiological levels of testosterone (androgen deficiency) and a normal number of spermatozoa. Hypogonadism (primary, secondary or mixed) is caused by disruption of one or more levels of the hypothalamic–pituitary–gonadal axis.²⁶ Boloña et al. (2007)²⁷ claim that testosterone is associated with various processes in the male organism including androgenic-anabolic it is thought, but not universally accepted that it is a crucial factor for male sexual libido. As has been noted, the definition of hypogonadism in medicine²⁸ differs from the ambiguous definition in the field of sports, where it can be a functional condition and, importantly, this condition is relatively quickly reversible to a normal condition.(29-31) The prevalence of exercise-associated hypogonadotropic hypogonadism and its impact on skeletal health in male athletes is not well understood. This is partly due to the lack of research on this topic and also because the identification of hypogonadism in men is not as clear as in women, where the situation is facilitated by the so-called menstrual dysfunction. In some cases, decreased testosterone levels may still be within the clinically normal range and may be considered an exercise-induced functional state.³² In terms of sports performance, testosterone provides physiological benefits such as increased muscle development, increased erythropoiesis, increased hemoglobin levels, which facilitate the transfer of oxygen in the blood and, last but not least, increased aerobic capacity.³² There are pioneering studies in animal models where has been shown that food deprivation suppresses spermatogenesis. If negative energy balance is associated with disturbances in reproductive function in male runners remains speculative but very likely.(33,34) De Souza (2021)⁵ assumes that alterations in testosterone concentration and spermatogenesis are an initial physiological adaptation caused by insufficient energy intake. When there is a state of chronic negative energy balance, reproductive function might be suppressed in order to prevent energy loss. Further evidence suggests that endurance-exercising males can develop a similar suppression of the reproductive function which we know from women. It is called Exercise Hypogonadal Male Condition (EHMC). EHMC can be viewed as overreaching or overtraining, when the amount of training was not adequately balanced by rest, resulting in physiological or psychological symptoms of maladaptation. Despite the obvious similarities between EHMC, overtraining, the women's athletic triad and RED-S, the differences should be put into perspective. The European College of Sport Science and the American College of Sports Medicine agree that when overreaching or overtraining is suspected, it is important to rule out other hypothetical causes related to negative energy balance or low energy availability. If the cause of the symptoms is an energy deficit, we do not classify this situation in the area of overreaching or overtraining, but it falls under RED-S. Being more physically active has been shown to be beneficial reproductively for men who are sedentary (or have a very low physical activity levels) as it results in improved testosterone levels and libido.³⁵ Conversely, there are many reports suggesting that men who participate in large amounts of endurance exercise training (e.g., marathon running) can have suppressed testosterone and libido.(36-39) The study about associations between endurance training and sexual libido in health men suggest that men with the lowest and mid-range training intensities or with the shorter and mid-range training volumes had greater odds of libido score in compare to their counterparts.⁴⁰ We have strong evidence that male endurance athletes across a range of different disciplines have been shown to exhibit lower levels of reproductive hormones including testosterone.(38,41-43) When Hackney et al. (1998)⁴⁴ compared endurance athletes with sedentary men, they reported significantly lower serum levels of testosterone. As for endurance athletes, levels of testosterone were in the normal clinical range but represented only 55% to 85% of their sedentary counterparts. A cross-sectional study, which is mentioned in Table 1, reported reduced testosterone levels in middle and long-distance runners and race walkers with clinical LEA.¹² It seems that long-term endurance running is also crucial for testosterone levels since 30% reduction in testosterone levels has been reported in athletes with at least 5 years of endurance running compared with athletes with fewer years of training (Hackney & Lane, 2018).⁴⁰ A study of elite long-distance runners showed a correlation between LEA and reduced testosterone levels. Runners who covered 81±14 km per week showed lower levels of total testosterone (9.2±2.3 vs 16.2±3.4 nmol/L) as well as lower EA (27.2±12.7 vs 45.4±18.2 kcal/kg/FFM/day) compared to their inactive counterparts.⁴⁵ In a study of 24 elite distance runners low testosterone levels appeared in 40% (n=10) of athletes and also bone injuries were 4.5 times more prevalent in low-T athletes.⁴⁵ Every subject ran more than 100 km per week. Similarly in a study of 50 road cyclists, there were 10 males with low EA and they had lower testosterone levels than those with adequate EA.⁴⁶ Also, RMR was suppressed in 65% of professional males cyclists despite similar EA and 24-hr energy balance compared with subjects with normal RMR, they spent more time in a severe energy deficit and had larger single-hour energy deficit, which was associated with higher cortisol levels and lower testosterone:cortisol ratio.⁴⁷

Energy availability and endurance performance in males

The overall amount of research examining endocrine dysfunctions due to low EA in men is only limited compared to research in women. The most evidence is provided by research into the effect of LEA on the reproductive abilities of men, which we mentioned in the previous text. Ultra-endurance exercise can cause acute decreases in testosterone levels as well as increases in cortisol, suggesting significant suppression of hypothalamic-pituitary axis functions.⁴⁸ Cortisol as one of the markers of endocrine stress is often associated with reduced testosterone circulation. This was seen in male endurance athletes who were exposed to low EA. It was also observed that a higher short-term energy deficit (24 hours) was associated with higher cortisol levels in performance endurance athletes compared to their counterparts with sufficient EA.⁴⁷ A study of elite rowers who underwent a four-week intensive training block with reduced energy supply found worsened regeneration and worsened performance on a 5,000-meter track.⁴⁹ Decreased aerobic and anaerobic performance, weight loss, and reduced RMR have also been shown in trained cyclists with insufficient energy intake during the intense training period.⁴⁹ In male cyclists, long-term low EA at the current higher training load resulted in reduced performance, and no benefit in terms of performance was found due to the amount of body fat.⁵⁰ Regarding the effect on muscle proteins, we know that the stimulation of muscle protein synthesis is supported by anabolic hormones such as insulin and testosterone. On the other hand, glucocorticoids, such as cortisol, increase the turnover of proteins in the body and initiate the breakdown of skeletal muscle proteins.⁵¹ As described by Šarabon et al., (2022),⁵² muscle strength and especially eccentric load is important for runners. The effect of low EA on performance may be more difficult to identify due to the significant effect of lower body weight on performance, thus even leading to a relative improvement in performance. Disease-related training failure is shown to be three times higher in athletes at low EA risk. These athletes lose more than 22 days of training per year, with an average of 7 days for risk-free athletes.⁵³ When evaluating the association between endurance training and sexual libido in men, it has been shown that libido scores are related to the duration and intensity of training, and thus the ability to train longer or harder.⁴⁰ Athletes usually follow a strict regimen and a hard training regimen to optimize athletic performance. In this endeavor, athletes may be malnourished enough to enter a state of low energy availability due to consuming too little energy compared to overpowering over a long period of time.³ This can have devastating effects, including damage to multiple organ systems, lower Bone Mineral Density (BMD), decreased testosterone levels, increased risk of injury, impaired coordination, and decreased athletic performance in many ways.(54,45,50,55)

Final considerations

The LEA seems to be a significant factor affecting the hormonal system and sports performance of endurance trained men. There is a fine line between the benefits of lower body weight and the negative consequences of LEA. This is linked with insufficient testosterone production, reduced libido, decreased bone mineral density. As we can see, the problem of low energy availability is better documented in women and on the contrary understudied in men. Its manifestations in men are more difficult to detect, and that is why we perceive a high need to include screening for nutritional risks as part of regular check-ups with a sports or physical education doctor. At the same time, we dare to say that there is a need for an easily accessible screening tool that can also be used outside of laboratory conditions. The athlete himself may see this as sudden weight changes, performance stagnation, fatigue fractures and digestive problems. It will be crucial for further research to reveal the relationships between a particular level of energy availability per organism - not just during the exercise itself and especially in the long term. More research is also needed for assessing long-term effects of LEA that result from various periods of sports training during the season.

List of acronyms

ACSM

American College of Sports Medicine

BC

Body composition

LEA

Low energy availability

BMD

Bone Mineral Density

DE

Disordered eating

DXA

Dual energy x-ray absorptiometry

EA

Energy Availability

ED

Eating disorders

EEE

Exercise Energy Expenditure

EI

Energy Intake

FFM

Fat Free Mass

IOC

International Olympic Committee

RED-S

Relative Energy Deficiency in Sports

RMR

Resting Metabolism Rate

SHBG

Sex-hormone binding globuline

TST

Testosterone

Funding Statement

Funding: None.