INTRODUCTION

Over the last 2 decades, it has become more apparent that some male athletes may experience a Triad-like syndrome, similar to the Female Athlete Triad. Scientific experiments and clinical research have helped guide clinicians toward better ways of assessing, diagnosing, and treating this Triad-like syndrome in the male athlete, now termed the Male Athlete Triad. The Male Athlete Triad is illustrated by Figure 1, and also described in depth in The Male Athlete Triad: A Consensus Statement from the Female and Male Athlete Triad Coalition Part 1: Definition and Scientific Basis. As in the female athlete, the key etiologic factor in the Male Athlete Triad is energy deficiency/low energy availability (EA), which may result in impaired reproductive and bone health. The Female and Male Athlete Triad Coalition Consensus Statement Part II: Diagnosis, Treatment, and Return-to-Play, demonstrates ways in which the science of the Male Athlete Triad translates into clinical practice. We present the latest clinical research to support current models of assessment, diagnosis, and management for male adolescent and young adult athletes.

Figure 1.:

Model of the Male Athlete Triad. The unidirectional arrows from energetic Status/EA toward bone health and the HPG axis indicate the causal role of EA on both bone health and HPG axis function. Similarly, the unidirectional arrow from HPG toward bone health indicates the causal effect of reproductive hormones on bone health. Furthermore, the bidirectional arrows along each continuum of severity represent the “reversibility” of the condition, such that an individual can improve or worsen over time. The line showing reversal of bone health outcomes is dashed with a question mark because the reversal of bone mineral density is less known, and more research is needed. Notably, with the Male Athlete Triad, the subclinical and clinical sequelae present at lower EA levels than what is often required for the development of health consequences in exercising women. EA, energy availability; HPG axis, hypothalamic–pituitary–gonadal axis.

As mentioned in the first article, the Female and Male Athlete Triad Coalition convened national and international expert panelists for a Roundtable on the Male Athlete Triad, in conjunction with the 64th Annual Meeting of the American College of Sports Medicine (ACSM) in Denver, Colorado, in May of 2017. Recommendations were set forth based on evidence-based data, as well as expert opinion. Similar to the Male Athlete Triad Part I: Definition and Scientific Basis, an evidence-based taxonomy has been used to grade the summary statements throughout the various sections of this article. Invited Roundtable expert panelists and selected attendees participated in reviewing the evidence statements for the Male Athlete Triad Consensus Statements. The evidence grading taxonomy chosen has been used by the ACSM position stands and by the Agency for Healthcare Research and Quality.1,2 The specific evidence scoring criteria are as follows:

Evidence level A: consistent pattern of findings on the basis of substantial data from randomized controlled trials (RCTs) and/or observational studies.

Evidence level B: strong evidence from RCTs and/or observational studies but with some inconsistent results from the overall conclusion.

Evidence level C: evidence from a smaller number of observational and/or uncontrolled or nonrandomized trials which is generally suggestive of an overall conclusion.

Evidence level D: insufficient evidence for categories A–C; panel consensus judgment.

SCREENING FOR THE MALE ATHLETE TRIAD Who Should be Screened?

At-risk groups for developing one or more components of the Male Athlete Triad include adolescent and young adult male athletes in sports that emphasize a lean physique (lean-sport athletes), especially endurance and weight-class athletes. Most studies to date that have identified one or more components of the Male Athlete Triad have been in adolescent3,4 and young adult long distance runners,5–7 cyclists,8–11 and jockeys.12–14 However, there is a lack of clinical studies that assess one or more components of the Male Athlete Triad in other lean-sport athletes, as well as in non–lean-sport athletes. Future studies are needed to assess the risk of the Male Athlete Triad among male athletes in other sports, as well as among military recruits.

Evidence level B: male adolescent and young adult lean-sport athletes, especially endurance and weight-class athletes, are at risk for developing one or more components of the Male Athlete Triad.

When Should Screening be Performed?

Early identification and monitoring of athletes at risk for the Male Athlete Triad are key to preventing the more serious outcomes associated with the Triad. Screening should begin in middle school or high school and should continue through college to identify at-risk athletes, so their bone health can be optimized during the critical years of peak bone accrual. Data indicate that men reach their peak bone mass in the third decade of life, with most of their bone mass accrued by the end of the second decade.15–17 At-risk athletes should be screened for the Male Athlete Triad at the time of their preparticipation physical examinations (PPEs), especially because the primary objective of the PPE is to screen for conditions that may be life-threatening, disabling, or predispose to injury or illness.18 The International Olympic Committee (IOC) also recommends a periodic health evaluation (PHE) for elite athletes, stating that the purpose is to provide a comprehensive assessment of the athlete's current health status and risk of future injury or disease.19 Screening for the Male Athlete Triad at the PPE/PHE is particularly important in male adolescent and young adult athletes who participate in sports at higher risk for the Male Athlete Triad, such as endurance or weight-class sports. In addition to screening at the PPE and/or PHE, screening can occur when the male athlete presents with any one of the Male Athlete Triad medical conditions (Figure 4).

How Should Clinicians Screen for the Male Athlete Triad?

The PPE monograph and the PHE both recommend screening questions relevant to the Male Athlete Triad.18,19 However, there is a paucity of screening tools specific to the Male Athlete Triad, and ideally the tool(s) should be practical for use in a clinical setting. The Female Athlete Triad Coalition Consensus Statement recommended specific screening questions for the Female Athlete Triad in 2014.20,21 A similar list of suggested screening questions for use at the time of the PPE in athletes at risk for the Male Athlete Triad can be found in Table 1. Further validation of these questions is needed, and it should not be assumed that questions designed for females can be used for males.

TABLE 1. - Recommended Screening Questions for the Male Athlete Triad Recommended Screening Questions for the Male Athlete Triad 1. Do you worry about your weight?
2. Are you trying or has anyone recommended that you lose or gain weight?
3. Are you on a special diet, or do you avoid certain types of foods or food groups?
4. Have you ever had an eating disorder?
5. Have you ever had a stress fracture?
6. Have you ever been told that you have low bone density or osteoporosis?
7. Have you ever been diagnosed with low testosterone levels?*
8. Do you have low libido (sex drive)?*
9. Do you have morning erections?*
10. Do you need to shave your facial hair less frequently?*

*Recommend inclusion only on preparticipation physical examinations for postpubertal athletes.

In addition to screening questions for the Female Athlete Triad, the Female Athlete Triad Cumulative Risk Assessment tool has been effectively used to assess Female Athlete Triad–related risk factors.20,21 Kraus et al 22 demonstrated that a modified Female Athlete Triad Cumulative Risk Assessment, which included low EA, low body mass index (BMI), low bone mineral density (BMD), and history of prior stress fracture, was associated with prospective bone stress injury (BSI) in male athletes. A similar Male Athlete Triad Cumulative Risk Assessment tool, presented in Figure 2, provides another method of screening the at-risk male athlete.

Figure 2.: The Male Athlete Triad Cumulative Risk Assessment tool. The Male Athlete Triad Cumulative Risk Assessment Tool provides an evidence-based risk stratification tool which may be used to guide an athlete's clearance for sport (Figure 3). It has been adapted from the Female Athlete Triad Cumulative Risk Assessment tool,20,21 with the menstrual history questions removed. *Some dietary restriction as evidenced by self-report or energy deficiency/low EA on diet logs or validated surveys. In adolescents, absolute BMI cut-offs should not be used, and clinicians should rely on age-adjusted and gender-adjusted BMI percentiles (**% median BMI, CDC BMI-for-age growth charts, or BMI Z-scores) or † % change in weight in the past 12 months. ***Weight-bearing sport; ‡high-risk skeletal sites associated with low BMD and delay in return-to-play include stress reaction/fracture of trabecular sites (femoral neck, sacrum, and pelvis). BMI, body mass index; BMD, bone mineral density; CDC, Center for Disease Control; DE, disordered eating; EA, energy availability; ED, eating disorder.

Athletes should also be screened for the Male Athlete Triad any time they present to the medical team with conditions associated with the Triad (Figure 4). A new diagnosis of a BSI may be the initial presenting symptom in a patient with the Male Athlete Triad and should prompt thorough screening for other components of the Triad. Additional conditions that warrant screening for the Male Athlete Triad include decreased libido, the absence of morning erections, decreased frequency of shaving facial hair, a decrease in weight, decreased performance, fatigue, unexpected changes in mood, or recurrent injuries and illnesses. Because athletes with unintentional energy deficiency/low EA may not be actively attempting to restrict their intake or lose weight, they may not screen positive on the Male Athlete Triad screening questions suggested in Table 1. It is therefore very important to consider energy deficiency/low EA in the differential diagnosis when athletes present with related medical concerns.

When screening identifies athletes at risk for the Male Athlete Triad during their PPE or another medical visit, a more thorough assessment is warranted and should include a detailed medical history and physical examination.

Evidence level C: it is recommended that clinicians screen the at-risk male athlete with targeted screening questions and risk assessment tools. Further research is needed to validate a best practice screening questionnaire for the Male Athlete Triad.

DIAGNOSIS OF THE MALE ATHLETE TRIAD How is the Male Athlete Triad Diagnosed?

Each of the 3 inter-related conditions of the Male Athlete Triad can occur on a spectrum, ranging from optimal health to the clinically relevant outcomes of energy deficiency/low EA with or without disordered eating or eating disorder, functional hypogonadotropic hypogonadism, and osteoporosis or low BMD with or without BSI (Figure 1). Furthermore, athletes may not present with all 3 components of the Triad at the same time, but identification of any one of the 3 components should prompt a thorough assessment for the others.

The accurate diagnosis of the Male Athlete Triad is best accomplished by a multidisciplinary medical team composed of a team physician, a sports dietitian, and a mental health professional (if disordered eating or a clinical eating disorder is present). Additional members of the team may include a certified athletic trainer, parents (of athletes <18 years old), medical consultants, and specialists, such as an endocrinologist, depending on the circumstances and the resources available.20,21,23,24 The multidisciplinary team not only assists with diagnosis, but, as will be discussed later, also helps with treatment and clearance decisions for athletes with the Male Athlete Triad. Team members should communicate frequently with one another and provide consistent information to the athlete because inconsistency can result in a lack of trust and confidence from the athlete.25

A thorough history should be performed, including a review of current symptoms and behaviors, medical history, medication history, family history, and psychosocial factors.

Current symptoms and behaviors: the athlete's dietary behaviors should be explored in detail, including any dietary restrictions, changes in weight or weight cycling, current weight goals, and behaviors intended to control weight, such as purging or compulsive exercise. Athletes should be asked about recent illnesses or injuries and performance. If the athlete has undergone puberty, it is important to screen for symptoms of hypogonadism such as sexual dysfunction, decreased frequency of shaving facial hair, or decreased libido. Although questionnaires are available to identify symptoms of hypogonadism in males, these are generally limited by poor specificity or were developed for use in older men and have not been validated in athletes.26,27 The International Society for Sexual Medicine, the International Society for the Study of the Aging Male, the Endocrine Society, and the American Urological Association do not recommend the use of a specific screening questionnaire to identify hypogonadism or testosterone (T) deficiency in the general population.28–33 Medical history: this should include a detailed assessment of any prior physician-diagnosed BSI or fractures. In addition, it should include a thorough assessment of the athlete's mental health diagnoses, including any history of depression, anxiety, bipolar disorder, obsessive compulsive disorder, or prior eating disorder. Occurrence of known endocrine disorders, such as hypothyroidism, hyperprolactinemia, and hypogonadism, should be included in this assessment. Medication history: the healthcare team should note any medications which might affect long-term bone health, such as glucocorticoids. In addition, athletes should be screened for medications that might affect libido, such as selective serotonin reuptake inhibitors, medications, and substances, that may cause elevations in prolactin and thus impact the hypothalamic–pituitary–gonadal (HPG) axis (antipsychotics, antidepressants, metoclopramide, domperidone, verapamil, cocaine, opiates, and possibly marijuana)34 and medications that may reduce appetite and cause weight loss (such as medications for attention deficit/hyperactivity disorder and topiramate). Family history: athletes should be asked about a family history of eating disorders, endocrine disorders, osteoporosis, or fragility fractures. Psychosocial factors: it can be helpful to elicit any history of critical comments, regarding body weight or size, or social pressures from coaches, parents, or teammates, because these may be influencing disordered eating behaviors and the maintenance of energy deficiency/low EA. Athletes should be screened for illicit drug use because this might also affect libido.

A comprehensive physical examination should be performed by the physician and should specifically seek to identify any signs of gonadal abnormalities or eating disorders. If a genitourinary examination is performed, a chaperone should be present.35 For the purpose of the targeted PPE in the male athlete, the purpose of the genitourinary examination is primarily to ensure that both testicles are in the scrotal sacs, and, for educating and teaching, the testicular examination to screen for testicular cancer. Findings suggestive of hypogonadism can also be assessed at this time if suspected by history and may include a lower than expected testicular volume depending on the time of onset and severity of hypogonadism. Hypogonadism before genital maturity may lead to an underdeveloped phallus and sparse pubic hair.

A low BMI, defined as BMI <18.5 in adults,36 may suggest energy deficiency/low EA with or without disordered eating. A major change in the Diagnostic and Statistical Manual of Mental Disorders (fifth edition) was to remove the weight criterion for anorexia nervosa (AN), which previously required the patient to be <85% of estimated body weight to meet diagnostic criteria. This was replaced with broader statements which identify changes in an individual's growth trajectory.37 In children and adolescents with disordered eating and eating disorders, absolute BMI is not an optimal method to reflect the nutritional status.38 Preferred methods for BMI calculation in adolescence include examination of an adolescent's weight in relation to the 50th BMI percentile (also known as the BMI percentile method or percent median BMI),38 use of the Center for Disease Control (CDC) BMI-for-age growth charts,39 or use of BMI Z-scores.40 Amount and rate of weight loss should also be considered in evaluation of energy deficiency/low EA and disordered eating.40

Physical examination findings suggestive of an eating disorder might include bradycardia, orthostatic hypotension, lanugo, dental erosions, swelling of the parotid glands, or calluses on the proximal interphalangeal joints (Russell's sign).20,21

Based on the history and physical examination, if there is a high degree of suspicion for the Male Athlete Triad, additional laboratory and radiological studies may be indicated. Suggested laboratory studies are listed in Table 2. Indications for proceeding with imaging studies, such as a dual-energy x-ray absorptiometry (DXA) scan or pituitary MRI, are reviewed below.

TABLE 2. - Suggested Laboratory Studies for the Evaluation of the Male Athlete Triad Suggested laboratory studies for the evaluation of the Male Athlete Triad*  Complete blood count  Comprehensive metabolic panel  25-OH vitamin D  Total and free testosterone†  Thyroid stimulating hormone  Free T4  Total ± free triiodothyronine (T3) Follow-up studies to consider if testosterone levels are low or fall in the gray zone* (8-12 nmol/L)  Luteinizing hormone  Follicle-stimulating hormone  Prolactin  Iron studies, including ferritin  Erythrocyte sedimentation rate and C-reactive protein

*Additional studies may also be indicated, depending on the patient presentation.

†Total testosterone should be routinely ordered. Free testosterone is helpful if total testosterone is low or in the gray zone (8-12 nmol/L). In addition, free testosterone may be considered in conditions expected to alter sex hormone–binding globulin levels, such as thyroid disease, HIV, use of anticonvulsants or glucocorticoids, liver disease, or diabetes.26,30,34

Evidence level C: male athletes are diagnosed with the Male Athlete Triad if they have one or more components along the spectrums of the Male Athlete Triad. The diagnosis includes a thorough history and physical and is best accomplished by a multidisciplinary healthcare team.

How is Energy Deficiency Identified?

Unfortunately, it can be very challenging to determine accurate EA values, particularly because the calculation is dependent on self-reported measures of dietary energy intake (EI), exercise energy expenditure (EEE), and body composition.20,21,41 As stated in the Male Athlete Triad: A Consensus Statement from the Female and Male Athlete Triad Coalition: Part I Definition and Scientific Basis, we recommend that EA is best suited to assessment in laboratory settings where the measurements can be carefully executed. However, although the limitations of these measures are understood, clinicians and sports dietitians may find that explaining the concept of EA and performing example calculations may be useful when the goal is to encourage the athlete to increase energy intake. Such conversations can take the focus off of body weight and provide examples of how the relative contributions of EI and EEE can be manipulated according to the individual's needs and unique circumstances. Consultation with a sports dietitian is highly recommended to quantify energetic status, especially if nutritional deficiencies are suspected.42 Although there are inherent limitations that are well defined in the literature regarding assessment of EI,43,44 EI may be estimated by using dietary logs, 24-hour food recalls, and food-frequency questionnaires.45 EEE may be estimated by using heart rate monitors and accelerometers or by web-based calculators, various phone-based applications, or by using the Physical Activity Compendium.46,47 Fat free mass (FFM)48 may be calculated based on the weight of the athlete in kilograms, as well as the percent body fat, which may be estimated by DXA, air displacement plethysmography, skin-fold measurements, Bod Pod, or bioelectrical impedance.49,50 Discussing patterns of food intake and behaviors with the athlete, and estimating their EA at the time that the athlete is being assessed for any one of the components of the Male Athlete Triad, can serve as an opportunity for the provider to educate and give immediate feedback to the athlete regarding suspected energy deficiency/low EA and under-fueling, as well as the possible relationship to their presenting complaint.

Given the challenges of accurately measuring EA, there are several proxies that may be used which are reliant on physiological adaptations to energy deficiency. Thus, the term ‟energy deficiency” as determined by objective measures of metabolic compensation such as resting metabolic rate (RMR) and metabolic hormone changes, in addition to documenting changes in anthropometrics, is likely valuable conceptually and, in practice, if these measures can be obtained. As mentioned above, in adults, energy deficiency/low EA may be indicated by low body weight, as defined by BMI <18.5.36 In children and adolescents, percent median BMI,38 BMI percentiles using CDC BMI-for-age growth charts,39 or BMI Z-scores40 can be calculated, as well as amount and rate of weight loss and/or change of growth trajectory.39,40 A stable body weight, however, does not ensure normal EA, because an athlete may reach a state of energy balance while at a low EA state because of suppression of normal physiologic and metabolic functions.20,21 Such adaptations to chronic low EA may be suggested by low triiodothyronine (T3) levels (free and total) and a reduced RMR that can be compared with predicted values in calculations of ratios of measured RMR/predicted RMR (mRMR/pRMR).51–57 Ratios of mRMR/pRMR are stable over time and can be used for serial assessments57 to predict low T3 and amenorrhea in exercising women.52 Depending on the data available (ie, weight, FFM, and lean body mass), several prediction equations are available for use to calculate ratios of mRMR/pRMR, and it is important to note that specific cut-off values indicative of metabolic suppression secondary to energy deficiency are unique to each prediction equation in women.52 Specifically, ratios indicative of energy deficiency in exercising women include 0.94 for use with the DXA prediction equation,58 0.92 for the 1991 Cunningham prediction equation,59 and 0.90 for the Harris–Benedict60 and 1980 Cunningham61 prediction equations. In addition, measured RMR was conducted under well-controlled laboratory conditions that included following strict pretest guidelines such as refraining from exercise, caffeine, medications, or alcohol in the prior 24 hours and a 12 hours overnight fast; the efficacy and utility of field-based measures of RMR to calculate ratios of mRMR/pRMR must still be tested. Similarly, the ability of mRMR/pRMR ratios to identify energy deficiency in exercising men has yet to be examined, and much work is needed to identify appropriate cut-off values specific to exercising men.

As previously stated, disordered eating behaviors and eating disorders may contribute to the development of a chronic energy deficiency/low EA. Therefore, identifying behaviors which contribute to undereating may be beneficial in identifying those at risk for energy deficiency. Several screening tools exist62–64 and have been used in the Female Athlete Triad literature to identify disordered eating and as proxy indicators of energy deficiency/low EA51,55,56,65,66; however, few tools exist that have been appropriately validated in men. Because disordered eating behaviors may manifest differently in men and women, tools and criteria specific to male athletes must be developed and tested. The Eating Pathology Symptom Inventory is a validated tool appropriate for use in both men and women and, interestingly, has a muscularity scale.67,68 Notably, this tool also has a scale to assess dietary restriction. An additional option is the EDE-Q, which also includes a dietary restraint subscale, and has male-specific cut-off values.69

Evidence level B: although measurement of energy deficiency or low EA is best quantified in laboratory settings, several proxies can be used clinically when estimating energetic status. These include objective measures of metabolic compensation, hormone changes, anthropometrics, and/or energy prediction equations.

How is Hypogonadotropic Hypogonadism Diagnosed?

tHypogonadism is defined as low testosterone (T) levels and/or defects in spermatogenesis in the presence of symptoms attributed to low T.26,30 Rather than using a questionnaire, most guidelines recommend assessing for symptoms or consequences of hypogonadism, such as low libido, erectile dysfunction, infertility, decreased shaving of facial hair, gynecomastia, low trauma fractures or reduced BMD, reduced muscle mass and strength, decreased energy and motivation, depressed mood, poor concentration, sleep disturbance, or diminished physical performance.26–28,30,34,70,71 If symptoms are identified, or the patient has additional Triad risk factors, a fasting, morning (7 am-11 am) total T level should be assessed.26,34,71 Abnormal T levels should be repeated for confirmation28,30,34,71; please refer to The Male Athlete Triad: A Consensus Statement from the Female and Male Athlete Triad Coalition Part 1: Definition and Scientific Basis for guidance on normal total T values. If hypogonadism is identified, further work-up is indicated to understand the cause. Male athletes with functional hypogonadotropic hypogonadism (secondary hypogonadism not associated with organic or structural pathology) generally have low T levels with low or inappropriately normal luteinizing hormone and follicle stimulating hormone levels.30,34,71,72 It is important to rule out other potential causes of hypogonadism, including genetic causes, drug use (see Medication History), or supplement use (such as anabolic steroids). Depending on the experience of the practitioner, it may be helpful to consult an endocrinologist for further guidance. A pituitary magnetic resonance imaging (MRI) is indicated in specific situations, such as when patients have hyperprolactinemia (that is not medication induced), symptoms of a possible mass effect, multiple pituitary hormone deficiencies, or severely low total T levels (<150 ng/dL or <5.2 nmol/L in a fully pubertal or adult male).30,34,71

Evidence level A: male athletes with symptoms of hypogonadism, or additional Triad-risk factors, should have a morning fasting T level drawn to assess for hypogonadism. If abnormal T levels are identified, these should be repeated for confirmation.

How is Low Bone Mineral Density and Osteoporosis Diagnosed in the Male Athlete?

The International Society for Clinical Densitometry (ISCD) definition for osteoporosis in adolescents and children up to age 19 years requires the presence of both a clinically significant fracture history and low bone mineral content (BMC) or BMD.73,74 In the absence of vertebral compression fractures, a clinically significant fracture history includes one or more of the following: 2 or more long bone fractures by age 10 years or 3 or more long bone fractures at any age up to age 19 years.74 Low BMC or BMD is defined as a BMC or areal BMD Z-score of ≤−2.0, adjusted for age, gender, and body size.73,74 Occurrence of vertebral compression or crush fractures in the absence of local disease or high-energy trauma is consistent with a diagnosis of osteoporosis, regardless of BMD.

In men less than 50 years of age, according to the ISCD, a BMD Z-score ≤−2.0 is considered “below the expected range for age” and a Z-score above −2.0 is “within expected range for age.” Osteoporosis cannot be diagnosed in men younger than 50 years of age on the basis of BMD alone. A BMD Z-score ≤−2.0 plus secondary causes of osteoporosis is required for diagnosis.75

Given that repetitive mechanical loading or high impact stress in athletes should provide a beneficial stimulus to bone health, the ACSM has proposed that for the female athlete, a Z-score of <−1.0 (at any weight-bearing site) should be used as a threshold for low BMD in athletes engaged in weight-bearing sports, especially in those with additional risk factors for the Female Athlete Triad.23 Similarly, it is the recommendation of the Female and Male Athlete Triad Coalition Consensus Statement that a Z-score of <−1.0 be used as a threshold for low BMD in the male athlete participating in weight-bearing sports because of concern for an increased susceptibility to a BSI or complete fracture, especially if the athlete has additional risk factors for the Male Athlete Triad. The threshold of concern is therefore lowered for the male athlete in a weight-bearing sport compared with the ISCD criteria for low BMD. However, in the general population and in female and male athletes participating in non–weight-bearing sports, we recommend that the current ISCD recommended value of a Z-score ≤−2.0 should be used for the threshold to categorize low BMD below the expected value for age.

When is a Dual-Energy x-Ray Absorptiometry Indicated in the Male Athlete?

It is the recommendation of the Male Athlete Triad Coalition Consensus Statement that a DXA be considered in male athletes who are at various stages of risk for the Male Athlete Triad (Table 3). Male athletes with one or more “high risk” factors, or 2 or more “moderate risk” factors, or athletes who have been taking a medication which may affect their BMD may warrant screening (Table 3). For athletes undergoing monitoring for low BMD, follow-up testing should be obtained when the expected change in BMD equals or exceeds the least significant change.76 In most cases of the Male Athlete Triad, this would be approximately every 1 to 2 years for those athletes who are at risk and/or for monitoring treatment. If low BMD is identified, it is important to rule out other potential causes of low BMD, such as other causes of hypogonadism, severe vitamin D deficiency, medications (such as glucocorticoids), malabsorption syndromes (such as celiac disease and inflammatory bowel disorders), certain systemic diseases, and genetic conditions.

TABLE 3. - Who Should Get a Dual-Energy X-Ray Absorptiometry Scan to Assess Bone Mineral Density (BMD)? Athletes with one or more high risk factors:  Body mass index (BMI) ≤17.5 in adults, OR % median BMI ≤85% in adolescents, OR ≥10% weight loss/month  Two prior bone stress injuries or one prior injury in a high-risk location such as the femoral neck, sacrum, or pelvis  A clinical eating disorder  Prior BMD Z-score ≤−2.0 Athletes with 2 or more moderate risk factors:  BMI 17.5 < 18.5 in adults, OR % median BMI 86%-89% in adolescents, OR 5 < 10% weight loss/month  One prior bone stress injury  Some history of disordered eating behaviors  Prior BMD Z-score between −1.0 and −2.0 in athletes involved in weight-bearing sports* Athletes who have been taking a medication which may affect their BMD may warrant screening

*For athletes in non–weight-bearing sports, a Z-score of −2.0 should be used.

Evidence level C: a DXA scan is recommended in male athletes who are at moderate or high risk for the Male Athlete Triad.

TREATMENT OF THE MALE ATHLETE TRIAD What are the Nonpharmacologic Treatment Recommendations?

Because a chronic energy deficit is the underlying cause of the Male Athlete Triad, treatment for the Triad should emphasize improving the male athlete's energy status, with the goal of eliminating energy deficiency and ensuring that EI meets all energetic requirements (Figure 4). Although energy deficiency can be reversed by increasing EI or decreasing EEE, or a combination of both, initial efforts to optimize energy status should target an increase in EI relative to EEE. This allows for continued sports participation and promotion of behaviors that support typical training and competition. Because of a lower prevalence of disordered eating and clinical eating disorders in male compared with female athletes,77,78 males may be more amenable than females to recommended changes in dietary patterns and EI. However, in cases where male athletes are not able to sufficiently increase EI, a modification of training may be needed, at least temporarily, to reduce EEE.

In addition to increasing EI to meet expenditure needs, it is important that dietary recommendations support sports-specific recommended intake of macronutrients and micronutrients. An overview of the nutrient recommendations for athletes is described in the 2016 ACSM, Academy of Nutrition and Dietetics, and Dietitians of Canada Joint Position Statement: Nutrition and Athletic Performance.79,80 A subset of male athletes may be at risk for underconsuming carbohydrates78,81–83 and should be monitored accordingly. Athletes should also aim to consume at least the recommended daily allowance (RDA) of micronutrients such as calcium, vitamin D, iron, B vitamins, and magnesium.79,80,84–86 Although supplements may help an athlete reach their recommended daily intake, most of these nutrients should be acquired from an athlete's diet whenever possible.

Although the plan for increasing EI will vary based on the individual, the process should be incremental, as more abrupt increases in EI may not be sustained. Current dietary patterns can be assessed and modified with moderate, high-impact changes. EI should be increased gradually, by adding 300 to 500 kcal/d, which is usually well tolerated and can be accomplished by adding 1 to 2 snacks per day or enhancing the energy content of current snacks and meals. For some athletes, especially those with disordered eating/eating disorders, or others who strongly feel that their performance may be negatively affected by increasing their caloric intake, starting on the lower end of this range may be needed. Athletes with energy deficits beyond 500 kcal/d can increase EI by another 300 to 500 kcal/d after maintaining the initial increase, although caution must be used to prevent failure because the EI prescription is too high to favor success. If not already consumed, the introduction of a postexercise snack containing carbohydrate and protein should be prioritized. Other priorities include optimizing intake before exercise, especially if the athlete is skipping meals or exhibiting long periods of fasting during the day, as within-day energy deficits have been associated with suppressed RMR and markers of catabolism in male athletes.87 Packing snacks and meals that can be taken on-the-go and use of portable and shelf-stable energy dense foods (such as trail mix, whole grain crackers, granola bars, shelf-stable milk, dried fruit, or nuts) may be particularly useful. The clinician and sports dietitian may also find it helpful to discuss increasing EI as “optimizing the athlete's fueling” because athletes often have negative connotations associated with increasing calories.

Evidence level C: optimizing energetic status by increasing EI, reducing EEE, or both, is the first-line treatment for male athletes with one or more components of the Male Athlete Triad.

What are the Recommendations for Calcium and Vitamin D Supplementation?

Given concerns of low BMD in the hypogonadal male athlete, it is important to ensure that athletes are obtaining the RDA of micronutrients such as vitamin D, calcium, and magnesium (Figure 4). When this proves challenging, or if athletes are diagnosed with vitamin D deficiency or insufficiency, supplementation may be necessary. Although data are currently lacking regarding a definitive 25-hydroxy vitamin D (25(OH)D) level below which BMD is compromised, a 25(OH)D level of 20 to 22 ng/mL or higher seems sufficient to avoid deleterious effects on the bone.88,89 Other studies suggest that parathyroid hormone (PTH) levels start to rise and calcium absorption is lower, although still within the normative range, when 25(OH)D levels fall below 30 to 32 ng/ml.90–92 More research is needed on optimal levels of bone building nutrients in athletes, and whether or not an optimal range exists to prevent BSI, decrease injury severity, and/or enhance recovery from BSI. Until more definitive data are available, we suggest maintaining 25(OH)D levels at or above 32 ng/mL, which may require use of supplemental vitamin D. 25(OH)D levels should not exceed the normal range given concerns for hypercalcemia.

Calcium supplementation may also be necessary if athletes are not able to reach the RDA through their diet (1300 mg/d for children and adolescents 9–18 years old, 1000 mg/d for those 19–70 years old, and 1200 mg/d for those >70 years old).86 One study in male adolescent runners demonstrated that receiving <1 serving of calcium-rich food per day was a risk factor for low BMD.3

What is the Role of Pharmacologic Treatment for the Male Athlete Triad?

As in female athletes,20,21 and as discussed above, first-line treatment for the Male Athlete Triad should be nonpharmacological and should focus on optimizing energetic status by increasing EI, reducing EEE, or both (Figure 4). When considering pharmacological therapy in the male athlete, it is important to consider what one is treating and the hormonal status of the athlete. Pharmacological therapy, although rarely needed, may be necessary in some cases to treat low BMD and increased fracture risk, symptoms of hypogonadism, or infertility.

Evidence level D: pharmacologic therapy, although rarely needed, may be necessary to treat low BMD and increased fracture risk, symptoms of hypogonadism, or infertility.

What Therapies May Help Normalize Testosterone Levels in the Hypogonadal Male Athlete? T Replacement Therapy

Although normalizing T levels would be expected to improve BMD, sexual function, and quality of life in the hypogonadal male athlete, hormone replacement is currently fraught with challenges, both because of the limited evidence available and because of restrictions placed around the use of exogenous T in athletes given that this may provide a competitive advantage.

In adolescent and young adult female hyperexercisers/athletes with oligoamenorrhea, good data now exist for physiologic hormone replacement (such as the 17-β estradiol transdermal patch with cyclic oral progestin) as a strategy to improve BMD,93–95 after lifestyle modification has been optimized to address energy deficiency. This form of hormone replacement therapy has also been demonstrated to improve eating behavior,96 verbal memory and executive function in adolescent and young adult oligoamenorrheic athletes,97 and trait anxiety in low-weight amenorrheic girls with AN.98 Of note, adult hypogonadal women with AN have low T levels, which correlate with lower BMD measures.99 However, a RCT of low dose T replacement in women with AN did not demonstrate a beneficial effect on BMD.100

Although some studies suggest that T levels are associated with bone outcomes in male athletes, others suggest that it is estradiol (from aromatization of testosterone) that drives these outcomes.93,101–103 Studies in adult hypogonadal men indicate a beneficial effect of T replacement on bone outcomes,104–106 mostly related to its aromatization to estradiol.107 In healthy adult men, estradiol levels above 10 pg/mL and testosterone levels above 200 ng/dL were n