The Application of Heavy Strength Training in Relative Energy Deficiency in Sport
A combination of high levels of physical activity, low sex hormone concentrations and subsequent low bone mineral density is commonplace in athletic populations. Low bone mineral density can lead to an increased risk of stress reactions or fractures, which can significantly reduce sport participation time. The use of heavy strength training has been effective at increasing bone mineral density in older, frail osteoporotic populations, and there is evidence that it would also be effective in athletic populations with low bone density. In addition to potentially reducing the risk of stress reactions and fractures, heavy strength training may be beneficial for endurance performance, including when being used as a replacement for some of the endurance activities. Thus, individuals exhibiting symptoms associated with the Female Athlete Triad, the Exercise Hypogondal Male Condition or Relative Energy Deficiency in Sports should consider implementing heavy strength training as part of their exercise regimen.
KeywordsRelative energy deficiency in sports Exercise hypogonadal male condition Female athlete triad Bone density Strength training Running economy
Overview and Prevalence
A reduction in concentrations of circulating sex hormones associated with high levels of physical activity has been known to exist in females  and males  for several decades. In 1978, a strong correlation was observed between incidence of amenorrhea (loss of menstrual cycle) and weekly training mileage in female collegiate track and field and cross country runners . After multiple studies investigated the effects of exercise on reproductive function in females, researchers sought out to assess whether similar outcomes were seen in men. The resulting study successfully demonstrated this analogous effect in males, after revealing a reduced circulating testosterone concentration in endurance trained men when compared to sedentary controls . Since these early observations, the study of exercising women and the potential causes and effects of the loss of the menstrual cycle became known as the Female Athlete Triad, with position stands published by the American College of Sports Medicine (ACSM) in 1997  and updated in 2007 , in addition to the formation of the Female Athlete Triad Coalition who published a consensus statement in 2014 . The study of sex hormones in males, however, has received considerably less attention. In 2005, the terminology of the Exercise Hypogonal Male Condition (EHMC) was proposed by Hackney et al.  and later research described these apparent parallels with the Female Athlete Triad in men . In recent years, there has been a push to incorporate the conditions in men and women under one term, Relative Energy Deficiency in Sport (RED-S) [37, 38] due to the suggestion that low energy availability (EA) is the sole cause of these conditions in both males and females. EA is defined as energy intake (kcal) minus exercise energy expenditure (kcal), divided by fat free mass (FFM, kg) and is considered to be low when under 45 kcal/kg FFM per day. However, this is not universally accepted for many reasons, including the large contrast in literature pertaining to females compared to males, with more than 30 years of studies on females, compared to research on males still in its infancy . Recent investigations suggest that exercise associated reductions in testosterone are related in part simply to years in training, where those participating in regular endurance exercise for 5 years or more have statistically significantly lower testosterone than those participating for 2 years . In this particular study, 27 of the subjects had been participating for 15 years or more, and it appears unlikely that these subjects could have been participating in endurance activity for such a substantial time period with chronically low EA. Here, the authors suggest endurance training results in a resetting of the hypothalamic pituitary gonadal axis to facilitate lower testosterone production, rather than necessarily a result of low EA. This is further supported by the testosterone concentrations reported in males participating in the Ironman World Championships, where many men demonstrated clinically low testosterone concentrations, but clearly have been able to perform at an elite level without reduced performance or debilitating bone injuries . Despite the lack of agreement on the terminology used in the literature and the differences in the criteria of these different terms, the conditions in males and females ultimately describe an interrelationship between high levels of physical activity, a reduction in circulating sex hormone concentrations and ultimately, the potential for a reduction in bone mineral density (BMD).
In terms of the prevalence of these conditions, in a study of 67 women exercising more than 2 h per week, 50% of the subjects demonstrated abnormal menstrual cycles, compared to 4.2% in a sedentary control group . In another study comparing 24 exercising women with sedentary controls, 46% of the exercising women had inconsistent menstrual cycle classifications from cycle to cycle, compared to 0% of controls . In a study of competitive women distance runners, 36% of the 91 women met criteria for abnormal menses . Thus, it appears that in females, approximately one-third to one half of highly active women demonstrate menstrual irregularities.
In males, the incidence of low testosterone has not been studied as extensively and on as large of sample sizes, and thus prevalence numbers are not readily available. Several early studies on male runners demonstrated reduced circulating testosterone concentrations when compared to sedentary populations [19, 22, 36, 50], but these testosterone concentrations were not below the reference values for low testosterone suggested by the Endocrine Society of 264 ng/dL or 9.4 nmol/L . More recently, highly competitive male athletes have been assessed competing in ultramarathon events [24, 32, 33]. For example, 13 of the 24 men competing at the Kona Ironman World Championships were shown to be in either the “gray zone” or be suggestive of deficiency . While the other studies referenced did not specifically report individual baseline testosterone concentrations, the mean testosterone concentrations are much nearer the threshold for testosterone deficiency, such as 12.3 nmol/L  and 14.9 nmol/L  than the early studies that were not assessing competitive ultramarathon runners, suggesting that the training required for high level competition in ultramarathon events increases the prevalence.
The identification of the condition in males, even with a reduced circulating testosterone concentration is also not straightforward. Where a menstrual irregularity is a clear symptom of some form of a pathology, a lower than reference value testosterone concentration is not in and of itself a concern and must be accompanied with symptoms of testosterone deficiency, such as reduced libido, sexual dysfunction and low BMD to be considered clinically hypogonadal . Thus, unless both the testosterone concentrations and the symptoms of hypogonadism are assessed, any diagnosis of exercise hypogonadism in men is not possible, again making prevalence numbers extremely difficult to ascertain.
Ultimately, combinations of high physical activity, reduced circulating sex hormone concentrations and low bone mineral density are quite common in athletic populations. The purpose of this review is to illustrate the potentially important role of heavy strength training when individuals demonstrate low bone density associated with the Female Athlete Triad (Triad), Exercise-Hypogonadal Male Condition or Relative Energy Deficiency in Sport conditions.
Bone Mineral Density
Summary of recommendations from the International Society of Clinical Densitometry and American College of Sports Medicine in identifying low bone mineral density and osteoporosis
T-score or Z-score
Men aged 50 years and older
Osteoporosis: − 2.5 or lower
Men younger than age 50 years
Osteoporosis: − 2.0 or lowera
Female athlete triad
Low BMDb: − 1.0 to − 2.0
Osteoporosis: − 2.0 or lower
As part of the 2007 Female Athlete Triad Position Stand, the ACSM identifies a criteria for low BMD of a Z-score between − 1.0 and − 2.0 (Table 1). The need for this extra criteria above those provided by the ISCD is justified by the fact that athletic populations typically have higher BMD than non-athletes, and thus a Z-score of less than − 1.0 is likely worthy of further investigation .
Prevalence of Low Bone Density
In a comprehensive review of the prevalence of the triad conditions (low energy availability, menstrual disturbances and low BMD), of the 755 athletes included, a weighted average of 21.6% of the women demonstrated a Z-score of − 1 to − 2, with a further 5.9% of the women with a Z-score of less than − 2 . Since this review took place, further study by Tenforde et al.  examined the effects of sport participation on total body and lumbar spine BMD in 239 female athletes and showed that swimming and diving (24%), synchronized swimming (45%) and cross country (19%) were particularly prone to low BMD (Z-score less than − 1). While the volume of literature in males is considerably lower, there are studies that have illustrated similar results. For example, in a study of 51 male adolescent runners, 23.5% of the subjects exhibited a lumbar spine BMD Z-score of less than − 1 compared to 5.6% of non-runner controls . In a study of 50 competitive male cyclists, BMD of less than − 1 in the lumbar spine was demonstrated in 44% of the subjects .
Thus, it appears that a substantial proportion of athletes that may be prone to RED-S exhibit reduced BMD, and in particular athletes in sports emphasizing leanness, such as endurance sports, as well as sports that do not require substantial weight bearing, such as swimming and cycling are particularly prone. It is also important to note the sites at which low BMD tends to occur, which appears to be the lumbar spine specifically, as opposed to the total body average.
Role of Energy Availability in Low BMD
Energy availability (EA) is defined as energy intake (kcal) minus exercise energy expenditure (kcal), divided by FFM (kg). Thus, EA is essentially the amount of kilocalories the body’s lean mass has access to, after exercise, to support bodily functions. The female athlete triad specifically refers to 3 inter-related components: (1) low energy availability with or without disordered eating, (2) menstrual dysfunction and (3) low bone mineral density , with low EA identified as the direct cause of menstrual dysfunction and the subsequent deleterious effects on bone density . These clear direct effects of low EA on menstrual dysfunction were eloquently illustrated in a study that controlled EA over the course of 5 days in tightly controlled conditions, prescribing either 10, 20, 30 or 45 kcal/kg FFM per day. At EA lower than 30 kcal/kg FFM per day, the endocrine disruptions were clear, showing luteinizing hormone (LH) pulse frequency decrease and the amplitude of the pulse increase . Thus, there is little doubt regarding the role that low EA plays in the development of the triad.
In males, such a direct cause and effect pertaining to EA and low testosterone has not been clearly identified, with the absence of the equivalent study controlling EA and measuring LH pulsatility that was conducted in females . At present, conclusions can only be drawn from studies observing subjects with exercise associated low testosterone that have also reported EA. For example, in a study comparing long-distance runners with sedentary controls, the runners had significantly lower testosterone as well as EA, notably below the 30 kcal/kg FFM per day threshold (runners: 27.2 ± 12.7 vs. controls: 45.4 ± 18.2 kcal/kg FFM per day) . However, there were no differences in LH pulse frequency or amplitude. In a study of competitive road cyclists who demonstrated a mean testosterone in the lower end of the reference range, 28% were identified as exhibiting low EA . In addition, the combined effect of training and chronic low EA resulted in a significantly lower testosterone concentration, compared with those cyclists with adequate EA . However, it should be noted that the large variance in EA documented in the exercise associated low testosterone literature suggests that some individuals must have adequate EA despite the reduced testosterone .
While the cause and effect relationship between low EA and reduced sex hormone concentrations has not been demonstrated as clearly in males as it has been in females, ensuring adequate EA is clearly essential in all athletic populations and if low EA is identified, it should be corrected, with the typical target of 45 kcal/kg FFM per day suggested for females  also suggested for males . If the low EA has occurred inadvertently, or without the presence of disordered eating, then nutritional education is sufficient . However, if the low EA is caused by disordered eating, referral to a physician and sports dietician is necessary, and in the case of an eating disorder, a mental health practitioner , as the reversal of low EA will not be possible without psychological treatment . It is also worth noting that if EA is low, micronutrient content may also be low, and thus the athlete should be screened for adequate calcium and vitamin D levels, which should be corrected if low .
Application of Heavy Strength Training
As previously mentioned, the ACSM recommends a BMD Z-score of < − 1, as opposed to < − 2, as a threshold that warrants further investigation in the case of the triad . This is due to the fact that athletes in weight bearing sports typically demonstrate a higher bone density than non-athletes . In the case of low BMD in either the triad, or highly active men with reduced testosterone, weight bearing exercise is obviously an insufficient stimulus for bone density development and therefore further intervention is necessary.
As osteoporosis is a significant public health concern, it has been much more studied in older, frail populations than athletic populations. In these older populations, many randomized controlled trials as well as systematic reviews and meta-analyses (for a comprehensive list see ) have been conducted investigating various forms of exercise, such as aerobic activity and strength training in the prevention of osteoporosis. In summary of this vast area of research, it is suggested that aerobic training is able to limit the reduction of BMD, particularly if it is of high intensity and speed . However, in comparison to strength training, it is suggested that progressive resistance training for the lower limbs is superior to aerobic activity for developing BMD .
It is of course essential to note that athletic populations are quite different to older, frail populations. While it has been specifically noted that high impact, multidirectional sport athletes have higher BMD than non-athletes, it has been suggested by Exercise and Sport Science Australia that it is not practical to create exercise guidelines for osteoporosis prevention or management based on technically and physically challenging sports . Of course, while this seems reasonable in the case of high-risk individuals, these types of activities are not unreasonable for athletes with low BMD. In fact, even in the case of high-risk individuals, some studies have suggested that high intensity, progressive resistance and impact exercise does not pose a significant risk even to post-menopausal women with low bone mass when closely supervised, despite a common misconception to the contrary . Thus, strength training certainly appears to be an appropriate intervention in RED-S populations.
Although there is a lack of randomized controlled trials, systematic reviews and meta-analyses on osteoporosis in athletes, there is still evidence that resistance training would be beneficial in these populations for developing BMD. For example, in a cross-sectional study comparing male runners who regularly perform resistance training to those that do not, the resistance training group demonstrated significantly greater bone density for all analyses, including total body, femoral neck, greater femoral trochanter, total femur and lumbar spine . Furthermore, in a study of factors associated with bone density in competitive cyclists, it was noted that participation in weight training is associated with a higher BMD of the lumbar spine, hip, femoral neck and femoral trochanter . While these studies cannot infer cause and effect, combined with the extensive literature supporting the superiority of strength training to aerobic exercise at enhancing bone density in older, osteoporotic populations, resistance training certainly appears to be an appropriate and likely effective intervention in RED-S athletes.
Prescription of Heavy Strength Training
In terms of how strength training is prescribed to develop BMD, it has been recommended that the intensity be high to very high [3, 49]. That is, at a load of at least 80–85% of an individual’s 1-repetition maximum (1-RM), which will lead to a repetition range, depending on the exercise, of approximately 5–10. As the lumbar spine is particularly prone to low BMD in athletic populations, exercises that load the lumbar spine and the muscles attached to the hip and spine are important as bone development is highly site specific . Thus, exercises such as the barbell back squat, deadlift, lunges and overhead press should be utilized [3, 5, 49]. It is also worth noting that the loads lifted may not need to be heavy at the onset of a strength training program, as after 40 weeks of resistance exercise, two groups of older men and women utilizing either 40% or 80% 1RM were able to improve BMD, with no differences between groups .
Again, these recommendations have been developed with older, frail populations in mind. With the importance of high loads on the spine and hip, and the apparent benefits of high impact and high velocity movements enhancing muscle power, Olympic weightlifting movements and their derivatives meet these criteria and are more likely to be appropriate in RED-S populations than the older populations osteoporosis exercise prescription had in mind. In fact, assessments of bone density in competitive weightlifters have demonstrated higher BMD in elite junior weightlifters (mean age 17 years old) compared to age-matched controls , as well as similar results in older nationally and internationally ranked weightlifters (mean age 33 years old) . In fact, even long after retirement from weightlifting, men aged 50–64 years that had been retired from weightlifting for an average of 27 years continued to demonstrate higher BMD than age matched controls .
Although the benefits of increased BMD may last many years, the process of increasing BMD with strength training can also take at minimum several months if not years. In a study including 19 cyclists, 10 of whom demonstrated a BMD Z-score of < − 1 despite all reporting to participate in heavy resistance exercise . However, no specific information on the intensity or frequency of the lifting was given, therefore these subjects may have been training at levels below the recommendations for developing BMD. The authors also noted that the subjects in their studies may have only been performing strength training during the off-season of 2–4 months, which may be an insufficient time period to develop BMD.
Race Performance Benefits
While an improved BMD and a potentially reduced risk of stress reaction or fracture may be appealing to endurance athletes, evidence that heavy strength training is beneficial to race performance is much more likely to lead to it being incorporated into an athletes regular exercise program.
In terms of physiology, endurance performance is classically influenced by 3 main parameters: VO2max, running economy, and fractional utilization, which refers to the percentage of VO2max that can be sustained for greater than ~ 3000 m . Particularly in runners with high mileage, it is likely that VO2max is nearing its upper limit, which is evident by the lack of variability in this measure in highly trained distance runners . Where variability is much greater, however, is in running economy, where 65% of the variation in 10 k race performance can be explained , suggesting that this may be a key area for development once a high VO2max has been established.
Running economy is the energy cost of sustaining a given submaximal running velocity , which has been recently suggested to be ideally measured as aerobic energy expenditure . Thus, if before a training regimen an athlete has an energy expenditure of 17 kcal/min at a 6 min/mile pace, and following the training now demonstrates an energy expenditure of 16 kcal/min at the same 6 min/mile pace, their running economy has improved. Due to the wealth of research in the area of strength training and its effects on running economy, a recent meta-analysis of 24 studies was conducted and demonstrated that in general, a strength training intervention lasting 6–20 weeks, added to the training program of a distance runner appears to enhance RE by 2–8% .
Incorporating Heavy Strength Training
Of the 24 studies included in the meta-analysis by Blagrove et al. , the overwhelming majority added strength training to the current running regimen. However, in the condition of RED-S, where energy availability may already be low, it is important that the inclusion of strength training is not added to the current training program, but rather substituted for some of the high energy utilizing endurance exercise . While this approach to the inclusion of strength training in endurance athletes is rare, it has been studied [44, 48].
In a study of 23 men with a mean VO2max of 59 ± 1 mL/min/kg, 11 continued their regular running training while the remaining 12 reduced their weekly running distance by 42% and incorporated 2 speed endurance and 2 heavy resistance training (80–90% 1RM) workouts for 8 weeks . In this short period, strength improved substantially in the intervention group, with a 12% improvement in 1RM squat (113–126 kg), 18% improvement in 1RM leg press (231–271 kg) and a 22% improvement in 5RM deadlift (100–122 kg), with no changes seen in the control. This large strength development corresponded with significant improvements in 10 km (44 min 11 s–42 min 20 s) and 1500 m (5 min 27 s–5 min 10 s) time trial performances, as well as distance covered in the Yo–Yo IR2 test (491–705 m) for the strength training intervention group, while no significant differences were seen in the control group. The improvement in aerobic performance was potentially due to the improved running economy seen at a running speed of 12 km/h, which significantly improved in the strength trained group (by 3.1%) and did not improve significantly in the control. All of these performance improvements in the strength trained group occurred without any changes in VO2max in either group, suggesting there were no deleterious effects of the large reduction in training volume on VO2max, at least over the course of 8 weeks.
Similar results were also seen in a study of 16 male endurance runners (VO2max 59.6 ± 5.6 mL/min/kg), where 9 men were assigned to a speed endurance and strength training group, which reduced their weekly running training volume by over 50% (from 62.7 to 26.4 km/week). These men were compared to a control group that were instructed to not change their running training (43.6–36.6 km/week). Again, very large strength gains were seen in the strength training group, with improvements in 4RM squat (87–156 kg), deadlift (75–111 kg) and leg press (173–365 kg). No strength changes were noted in the control group. The strength training group saw statistically significant improvements in 400 m (4.8%) and Yo Yo IR2 (18.5%), whereas the control group saw no changes. In addition, maximal aerobic speed, time to exhaustion and peak blood lactate during an incremental treadmill test all improved significantly, with no changes in the control group. On this occasion, 10 km time trial performance did not improve in either of the 2 groups, and neither group saw any changes in VO2max.
In terms of the effects of strength training on endurance athletes, there is a substantial window of opportunity for strength enhancement. Developing strength appears to significantly improve either running economy, or induce muscular adaptations related to anaerobic capacity. These adaptations led to measurable changes in running performance that running training without strength training was unable to produce. In these aforementioned studies, strength training alone cannot be isolated as the reason for the adaptations, as both interventions also included speed endurance training which could have been responsible. However, it is clear that resistance training can be performed at enough volume and intensity to considerably improve strength and do so concurrently with improvements in running performance without any negative effects on VO2max, even when strength training replaces considerable amounts of running.
In the case of an individual showing symptoms of RED-S, Exercise Hypogonadal Male Condition or the Female Athlete Triad, heavy strength training could form an important part of the training regimen. Heavy strength training specifically should include high relative loads of 80% 1 RM or greater and exercises that load the areas prone to low bone mineral density, including the lower spine and the hip. Explosive exercises with high loads such as Olympic weightlifting and its derivatives may also be beneficial. This form of resistance exercise can help to increase bone mineral density as well as enhance running economy and anaerobic capacity, even when it is used in the context of reduced endurance exercise volume.
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Conflict of interest
The author declares no conflict of interest
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