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BONE

Adam S. Tenforde, Emily Kraus, and Michael Fredericson

OVERVIEW

Attaining peak bone mass and strength is an important aspect of overall musculoskeletal health in both female and male athletes. Failure to attain peak bone mass during childhood and adolescence may result in an increased risk for bone stress injuries (BSI) during sports participation and fractures associated with osteoporosis in older adults. In this chapter, we review the biological process of attaining peak bone mass during childhood and adolescence and the influence of sports participation on modulating bone health. Next, we discuss sex-specific clinical syndromes that can impair bone health, including the female athlete triad (Triad). We review sex-specific risk factors for BSI, a common overuse injury in athletes. Finally, we discuss the topic of bone health in older adult athletes.

BONE METABOLISM

Peak Accretion

Childhood and adolescence is a time of growth for the skeleton. Total body bone mineral content (BMC) reaches a plateau on average at ages 18 and 20 in females and males, respectively (1). For both sexes, peak bone mass is reached by the end of the second decade or early third decade of life (1,2). The rate of BMC accrual for both sexes may be greatest in the 4 years surrounding peak height velocity, with approximately 40% of BMC gained in the total body, femur, and lumbar spine during this time (1).

Bone mass is most commonly measured using dual-energy x-ray absorptiometry (DXA), which uses ionizing radiation to measure areal bone mass and determine density and quality of bone expressed as BMC and areal bone mineral density (BMD). Common locations for measurement include the lumbar spine (L1-L4 vertebrae), total body, and proximal femur/hip. In children and adolescents of both sexes, lumbar spine and total body less head (i.e., total body excluding contribution of bone mass from the skull, a non-weight-bearing skeletal site) are locations recommended to measure BMD and content, as the hip is prone to measurement error and variability in skeletal development (3). The DXA values measured for an individual at each site can be standardized to Z-scores and T-scores. In children, men less than 50 years of age, and premenopausal women, Z-scores are recommended to standardize individual results to a reference population standardized to sex, age, and ethnicity normal values (3).

In females who are physically active, including children to premenopausal adults, the American College of Sports Medicine (ACSM) recognizes a BMD or BMC Z-score of less than -1 as low bone mass for age (4). ACSM has not defined a similar criterion in male athletes. The International Society of Clinical Densitometry (ICSD) defines “low bone mass for chronological” age as BMC or areal BMD Z-scores of -2 or less for ages 5 to 19 years in both girls and boys (3). The term osteoporosis in children and adolescence ages 5 to 19 requires both BMD/BMC Z-score of -2 or less with a clinically significant history of fracture defined as one lower extremity long bone fracture, two or more upper extremity long bone fractures, or a vertebral compression fracture (3). Other measures of bone geometry can be derived from DXA measures, including hip structural analysis (HSA) or by using other technologies including peripheral quantitative computed tomography (p-QCT).

Response to Osteogenic Activity

Bone density and geometric properties are influenced by many factors, including extrinsic factors of physical activities that apply stress to the bone. In addition to Wolff’s Law (5), the Muscle-Bone Unit theory (6) in children describes that muscle generates the greatest nontraumatic stress on the bone and influences bone health of growth during childhood and adolescence. Other studies have shown that weight-bearing physical activities increase bone mass accrual in children of both sexes (7,8), demonstrating the importance of ground impact forces in influencing bone density and strength.

Sports-specific loading can be categorized into the types of impact loading characteristics. In a review of the influence of sports participation on bone density and geometry in athletes ages 10 to 30 (9), we observed that sports that include activities that generate high impact and multidirectional impact loading (including jumping and ball sports) resulted in greatest BMD/BMC values and bone geometric properties (10–16). Mechanical loading may better explain osteogenic effects of sports participation for improved bone quality rather than high magnitude muscle forces (15). Site-specific loading characteristics influence bone density, as illustrated in racquet sport athletes who have observed greater BMC in the dominant arm compared to the nondominant arm (14). Furthermore, swimming may result in reduced bone quality compared to sedentary age-matched controls (12) and swimming does not predictably improve bone health with continued participation (17). See Table 12.1 for types of sports and loading characteristics with bone density/geometry comparisons (9).

Jumping programs have been shown to increase BMC in both sexes when performed in early childhood. Gunter and colleagues studied a population of 205 boys and girls of average age 8.6 years old. Schools were randomly assigned to be the control or intervention school. In the intervention school, children performed a jumping program during a physical education program three times per week for 7 months consisting of 100 box jumps. At 7 months, the intervention group had 7.3% to 8.4% greater BMC values than the control group at all sites tested. The benefits of the jumping program reduced over time but remained greater in the intervention group than the control group 3 years after discontinuation of the jumping intervention (18). A subset of children who participated in the larger study (18) were followed for changes of hip BMC over 8 years, and children who participated in the jumping intervention maintained 1.4% greater hip BMC than the control group (19). These findings suggest early jumping activities may be a strategy to optimize future skeletal health in adulthood (20).

Ball sports are a form of high impact, multidirectional loading resulting in high ground reactions forces, similar to jumping. High impact and multidirectional impact sports, including ball sports, appear to confer greatest BMD and bone geometric properties, whereas running does not predictably increase BMD (13). Participation in ball sports has been observed to reduce risk for future fracture in the military and in runners when performed during childhood, particularly in males (21–23). Studies have not shown consistent benefits in fracture reduction in female athletes, and this finding may be explained by triad risk factors that may reduce or potentially eliminate these benefits (22,24,25).

The observation that participating in high impact loading activities including jumping and ball sports during childhood results in improved bone mineral characteristics during later life is supportive of the concept for a critical period to encourage physical activity during early puberty (26). However, discontinuation of sports activities may result in bone loss during adulthood for both former male and female athletes (27–29), suggesting that maintaining impact-loading activities is important to maintain the full benefits of prior sports participation in bone health.

TABLE 12.1: Loading, Bone Density, and Bone Geometry Patterns of Different Types of Sports, Divided by Loading Patterns

CLINICAL SYNDROMES

The Female Athlete Triad

The triad is defined as the interrelationship of energy availability, menstrual function, and BMD (30). The condition is considered a spectrum disorder (4) ranging from optimal health to disease for each component:

Low energy availability (defined as the difference of energy intake to estimated energy expenditure standardized to fat-free mass) is considered the primary contributor to the triad and is more common in endurance athletes and in the female sex (31). Both athletes and non-athletes may have one or more component of the triad, although having all three components of the triad is less common (32–34). The effects of the triad appear summative, as female athletes with greater number of triad risk factors are at increased risk for low bone density and BSI (4,23,35,36). Since menstrual status may modulate differences in bone density and geometric properties (37), identification of at-risk female athletes is critical as delayed or “catch-up” bone mass accrual is not ensured (38). The 2014 Female Athlete Triad Coalition Consensus Statement on Treatment and Return to Play of the Female Athlete Triad provides guidelines for cumulative risk assessment of triad in female athletes (30). The Risk Factor Scoring and Medical Risk Stratification are included in Figure 12.1. This is an important advancement in providing evidence-based recommendations and best practices for female athletes with the triad. This information is a powerful tool to assist sports medicine professionals in determining clearance and return to play for female athletes. Additionally, the Female Athlete Triad Coalition provides online resources that are helpful for athletes, physicians, and other sports medicine professionals (www.femaleathletetriad.org). Screening questions for the triad have also been published and are important to include in preparticipation examinations (Figure 12.2) (30).

FIGURE 12.1: Female athlete triad: Cumulative risk assessment.

BMD, bone mineral density; BMI, body mass index; DE, disordered eating; EA, energy availability; ED, eating disorder; EW, expected weight.

Source: From Ref. (30). De Souza MJ, Nattiv A, Joy E, et al. Female Athlete Triad Coalition Consensus Statement on Treatment and Return to Play of the Female Athlete Triad: 1st International Conference held in San Francisco, May 2012, and 2nd International Conference held in Indianapolis, May 2013. Br J Sports Med. 2014;48(4):289. Used with permission from BMJ Publishing Group Ltd.

FIGURE 12.2: Triad consensus panel screening questions.

Note: The Triad Consensus Panel recommends asking these screening questions at the time of the sport pre-participation evaluation.

Source: From Ref. (30). De Souza MJ, Nattiv A, Joy E, et al. 2014 Female Athlete Triad Coalition Consensus Statement on Treatment and Return to Play of the Female Athlete Triad: 1st International Conference held in San Francisco, May 2012, and 2nd International Conference held in Indianapolis, May 2013. Br J Sports Med. 2014;48(4):289. Used with permission from BMJ Publishing Group Ltd.

The concept of a parallel process of the triad in males has been proposed (39,40). Analogous to the female athlete triad, males may have impaired nutrition and lower sex hormones including testosterone, both of which may negatively influence BMD (40). Our understanding of a similar process in male athletes and health consequences are limited, as research characterizing the female athlete triad is based on greater than two decades of research.

Other Nutrition Considerations: Calcium and Vitamin D

In addition to adequate energy availability, other aspects of nutrition are important to ensure optimal bone mass accrual and prevention of BSI. The Institute of Medicine (IOM) guidelines in 2010 recommend calcium intake of 1,300 mg daily and vitamin D of 600 IU daily for both sexes ages 9 to 18 years old to optimize bone health (41). Table 12.2 is a summary of the recommended daily intake values based on age and sex. Research on target calcium and vitamin D intake for BSI prevention has been primarily performed in young adult female runners and military. Lappe et al. (2008) performed a randomized double-blind, placebo controlled trial in female U.S. Navy recruits; the experimental group supplemented with 2,000 mg of calcium and 800 IU of vitamin D daily benefited from one-fifth reduction in stress fractures compared to the control group over 8 weeks of basic training (42). In a population of competitive female runners ages 18 to 26, Nieves and colleagues demonstrated that higher intake of skim milk, dairy, and calcium reduced risk for stress fracture (43). Additionally, investigators reported that each cup of skim milk per day consumed was associated with 62% reduction in development of a stress fracture (43). A subset analysis within this population (43) found that female runners with daily calcium intake of 800 mg or less were six times more likely to develop a stress fracture compared to those with 1,500 mg or greater daily calcium intake, suggesting that calcium intakes of 1,500 mg daily may be most effective for prevention of BSI in young athletes (44). In a separate investigation, females ages 9 to 15 who consume greater vitamin D were found to have lower rates of stress fracture when performing high levels of high impact activity (45). A report in male military recruits average age 18 found that lower calcium and vitamin D intake values were associated with prospective development of stress fractures during a 4-month course of basic training (46). In summary, meeting intake values for calcium and vitamin D recommended by the IOM is essential during stages of growth and development.

Bone Stress Injuries

BSI represent the failure of bone to withstand submaximal repetitive loading, falling on a spectrum from stress reaction to stress fracture to complete fracture (47). These are a common form of overuse injury in athletes of both sexes. Most research investigations describe incidence of stress fracture injuries in their populations studied. Stress fractures are common and represent up to 20% of injuries seen in sports medicine clinics (48). Both sexes appear more susceptible to BSI at younger ages (49,50). Stress fractures are more common in childhood and adolescent females who participate in greater hours of running, dance/gymnastics, and basketball (51). Other studies have demonstrated that cross-country runners and track and field athletes of both sexes are commonly affected with stress fractures (52,53). High school female athletes are more likely to sustain a stress fracture than males (52), consistent with an earlier review that concluded stress fractures are more common in female athletes and military personnel than males (54).

Sex-specific risk factors for development of BSI have been identified, including the female athlete triad. All female athletes should be screened for risk factors of the triad during preparticipation physical examinations, including completing a full menstrual history (age of menarche, history of menstrual irregularities). It is important to ask about use of oral contraceptive medications or other hormonal therapy, as withdrawal bleeding is not equivalent to eumenorrhea as hormonal therapy does not address the underlying causes of menstrual dysfunction (4). In female high school runners, prior fracture, BMI less than 19 kg/m², late menarche (menarche at age 15 and older), and prior participation in dance and gymnastics were each independent risk factors for prospective development of a stress fracture injury (23). Additionally, these risk factors were cumulative, with female runners possessing three of these four risk factors at 40% risk of sustaining a prospective stress fracture during the study (23). Similarly, male runners with history of fracture were more likely to develop a stress fracture (23). A history of fracture has been recognized as a risk factor for future stress fracture in young adult female runners (49). Recently a multicenter investigation of active young women demonstrated the following independent risk factors associated with developing a BSI: participation in 12 hours or more of exercise, BMI less than 21 kg/m², and BMD Z-scores below -1 (35). Morphological qualities have been suggested to increase risk for BSI in female track and field athletes. Risk factors include less lean mass in the lower limbs, leg length discrepancy, and decreased calf circumference in females; however, this relationship was not observed in men (55).

TABLE 12.2: Summary of the Recommended Daily Intake Values

MRI is commonly used to grade the severity of BSI. Nattiv et al. (56), Fredericson et al. (57), and Arendt et al. (58) have all proposed grading systems that use MRI to determine severity of BSI on a scale of one to four. To summarize in all three grading systems, the higher grade BSI demonstrate abnormal signal on T2 and T1 (grade 3), with grade 4 defined as evidence of a fracture line. Higher MRI grade BSI, lower BMD values, and trabecular sites (pubic bone, sacrum, and femoral neck) are common risk factors for longer healing time in collegiate track and field athletes of both sexes (56). Additionally, female athletes with oligomenorrhea (commonly defined as menstrual periods greater than 35 days apart) or amenorrhea were more likely to have higher MRI grade BSI (56).

The location of BSI is important for risk factor assessment and clinical management. Injuries in the pelvis, proximal femur, anterior tibia, patella, tarsal navicular, base of fifth metatarsal, great toe sesamoids, talus, and medial malleolus are considered high risk BSI due to multiple factors including increased biomechanical stress, limited vascular supply, and/or potential consequences if healing is not achieved (59). Growth plate injuries are also important to consider in the skeletally immature athletes (60).

For both sexes, management of BSI includes activity modification guided by the athlete being pain-free, which is important to ensure that the bone(s) affected do not continue to be loaded to promote healing. In high-risk fracture locations or if pain persists despite activity modification, initial use of crutches may be required. Walking boots are prescribed to ensure pain-free ambulation for most BSI in the foot and ankle. Athletes of both sexes may usually participate in non-weight-bearing activities, including deep water running, after the initial phase of injury recovery as long as these activities can be performed pain-free.

For an athlete who presents with one or more BSI, it is important to screen for and address risk factors for injury. In both sexes, BMI should be calculated as BMI below 17.5 kg/m², which has been suggested as a marker for low energy availability (30) and has been associated with low BMD values in young runners of both sexes (61). Additionally, both female and male athletes should be screened for eating disorders or disordered eating, dietary intake patterns including foods containing calcium and vitamin D, fracture history, personal history of other medical conditions contributing to impaired bone health (including thyroid disease, rheumatologic disease, other inflammatory conditions, food allergies, and malabsorption), and family history of osteoporosis or bone disease. Medications that contribute to impaired bone health include oral steroids, proton pump inhibitors, antidepressants, and anti-epileptic medications. In female athletes who have a positive screen for triad risk factors include menstrual dysfunction, referral to a specialist in the triad can be valuable in aiding a full endocrine workup. Treatment of the triad is patient-centered and may require a multidisciplinary team including sports physician, dietician, coach, athletic trainer, family, and a mental health specialist, if there are comorbid conditions including eating disorders.

Evidence-based guidelines for evaluation and management of male athletes with impaired bone health have not been clearly defined in this population. In our review (40) we outline our current practice in male athletes who sustain high-risk BSI. This includes obtaining a DXA and completing a nutrition evaluation and endocrine workup. Referral to a sports dietician is prudent in male athletes who participate in sports, emphasizing leanness or weight control behaviors. Currently, there are no clear guidelines on the endocrine workup for male athletes who present with BSI or concerns for impaired bone health, although workup may include assessing for vitamin D deficiency, thyroid dysfunction, and low sex steroid hormones including testosterone.

THE AGING ATHLETE

As adults reach older ages and are encouraged to remain active into their later years of life, maintaining optimal bone health is critical to reduce risk for health issues including fragility fractures and overuse BSI as seen in younger athletes. This section addresses bone health in the aging athlete, including hormonal changes affecting bone loss, BMD changes, and the role of exercise in optimizing bone health.

Hormonal Changes in the Aging Athlete

Hormonal changes occur with aging in both sexes, which influences bone health. Sex hormones including both estrogen and testosterone play an important role in bone health throughout life, with estrogen the predominant hormone modulating bone loss for both sexes (62). In females, menopause results in a short period of accelerated bone loss followed by slower ongoing bone loss, whereas aging men have a slow steady decline (62). A review by Khosla (2010) concluded that low estrogen levels remain an important topic to address in postmenopausal women to influence bone health (63). Older men with lowest bioavailable estradiol had greatest rate of BMD loss in the total hip (64). While bioavailable testosterone was not directly correlated with differences in bone loss, the combination of low bioavailable testosterone and estrogen with highest sex hormone binding globulin had the fastest rates of BMD loss (64). While low estrogen places males at increased risk for hip fracture, men at greatest risk for fractures have both low estrogen and low testosterone levels (65).

Changes in Bone Mineral Density With Age

Age-related reductions in BMD observed in both sexes is an important determinant for overall bone health. Osteoporosis may be diagnosed in a male 50 years or older or a postmenopausal female with a T-score less than or equal to −2.5 at the lumbar spine, total hip, or femoral neck (3). Ongoing loss of BMD associated with aging may result in a greater proportion of individuals meeting these criteria. In a prospective population-based study, a menopausal status change from premenopausal/early menopausal transition to late menopausal transition was associated with annual reduction in BMD of 0.7% at the femoral neck and 0.9% at the lumbar spine (66). In this population, reaching postmenopausal status was associated with a decline of BMD of 1.7% at the femoral neck and 2.5% at the lumbar spine (66). Furthermore, greatest BMD loss may begin approximately 1 year before to 2 years following the final menstrual period termed transmenopause (67). The transmenopause stage resulted in a majority of the 10.6% lumbar spine and 9.1% femoral neck cumulative BMD loss observed over a 10-year period surrounding the final menstrual period for a multiethnic population (67). In males 65 years or older, rapid bone loss (defined as greater than or equal to 3% BMD loss per year) and osteoporosis were most common with either estrogen or testosterone deficiency (68).

For both sexes, BMD loss is an independent risk factor for fragility fractures, especially in those with osteopenia (BMD T-score between −1 and −2.5)(69). Low hip BMD is a risk factor for nonvertebral fractures including hip fracture in older men (70). Lower lumbar spine BMD is also associated with fractures, although the relationship is less strong (70). In women before menopause, most bone loss is from the axial skeleton with appendicular bone mass relatively preserved (71). Bone loss at the femoral neck site may be seen in females at their perimenopausal transition (72), and BMD loss then accelerates during menopause (73).

Role of Physical Activity and Exercise on Preserving Bone Mass in Older Adults

Physical activity has numerous benefits for both skeletal and overall health. The 2004 ACSM position statement on physical activity and bone health concludes that activities including both weight-bearing and resistance training may be most appropriate for preserving bone health in adults (74). In addition, moderate walking has been observed to repress bone turnover in postmenopausal women with osteopenia or osteoporosis (75). Similarly for men, one prospective study observed both men and women who maintained their running habits over 5 years had lower rates of lumbar spine bone loss than those who reduced running with older age (76).

Physical activity interventions have been primarily performed in women. A meta-analysis on walking as a singular exercise therapy suggested positive influence on femoral neck and not lumbar spine BMD in postmenopausal women (77). In contrast, high-intensity resistance training may result in increases for lumbar spine BMD (78). Mixed loading exercise programs incorporating both low impact activities (such as jogging) and higher impact/magnitude activities including resistance training may reduce postmenopausal bone loss at both the hip and spine (79). In contrast, insufficient evidence currently exists to recommend specific exercises targeting lumbar spine and femoral neck BMD in men (80).

Practical Applications

Given the clear benefits of physical activity on bone health and overall health and well-being in older adults, it is important to encourage continued physical activity with aging. However, the known bone loss associated with the aging process needs to be considered in evaluation and management of sports injuries. Given that bone loss can be anticipated with the aging process, BSI need to be considered more strongly on the differential diagnosis for an older adult who presents with a sports injury. Both addressing the current sports injury and ensuring the athlete has proper assessment of bone health is important for secondary prevention. Understanding the underlying bone health may be helpful in counseling on relative risks for participation in different forms of sporting activity.

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