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Bone Health in Adaptive Sports Athletes

Blauwet, Cheri A., MD*,†; Borgstrom, Haylee E., MD, MS*; Tenforde, Adam S., MD*

Sports Medicine and Arthroscopy Review: June 2019 - Volume 27 - Issue 2 - p 60–66
doi: 10.1097/JSA.0000000000000235
Review Articles
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Adaptive sports athletes represent a growing population within the athletic community worldwide. Given potential cardiometabolic and psychosocial benefits of adaptive sports participation, the impact on bone health and injury risk in adaptive athletes is of increasing clinical interest. Impaired bone health as a result of low energy availability has been well described in able-bodied athletic women and, more recently, men as part of the female athlete triad and Relative Energy Deficiency in Sport (RED-S). However, the applicability of these models to adaptive athletes remains unclear given altered physiology and biomechanics compared with able-bodied counterparts. Thus, a literature review was completed to characterize the influence of adaptive sports participation and associated risk factors for impaired bone health in this unique population. To date, limited investigations demonstrate a consistent, positive effect of sports participation on bone health. Risk factors for impaired bone health include low energy availability and micronutrient deficiency.

*Kelley Adaptive Sports Research Institute

Department of Physical Medicine and Rehabilitation, Spaulding Rehabilitation Hospital, Harvard Medical School, Boston, MA

Disclosure: The authors declare no conflict of interest.

Reprints: Cheri A. Blauwet, MD, Department of Physical Medicine and Rehabilitation, Kelley Adaptive Sports Research Institute, Spaulding Rehabilitation Hospital/Brigham and Women’s Hospital, Harvard Medical School, 300 1st Avenue, Charlestown, MA 02129

In recent years, adaptive sports have grown in participation and overall public interest. The Paralympic movement has gained considerable international recognition for its premier elite athletic events.1 Most recently, the Rio 2016 Summer Paralympic Games featured over 4300 athletes from 160 countries competing across 22 sports,2 and the Pyeong Chang 20183 Winter Games featured over 550 athletes from 49 countries competing across 6 sports. The increase in elite adaptive sports participation reflects the growing interest and expansion of sporting opportunities for athletes with disabilities worldwide.4 Along with the known cardiometabolic health benefits, participation in adaptive sports has been shown to improve mental health, community engagement, employment, pain reduction, and life satisfaction.5,6

In the light of these benefits, bone health and injury risk within this athletic community is a topic of growing clinical interest.7 Healthy skeletal metabolism is characterized by a complex interplay of metabolic, endocrine, and biomechanical factors that act in concert to maintain bone mass and architecture.8 Individuals with disabilities often experience impaired bone density and quality due to immobility, reduced weight-bearing, and other neuroendocrine-related factors, as well as sport-specific behaviors in adaptive athletes.

Concerns with regard to impaired bone health have traditionally been described in able-bodied female athletes. The female athlete triad was initially proposed in 1993, linking disordered eating to the development of amenorrhea and osteoporosis.9 The Triad is currently defined as the interrelationship of energy availability (EA), menstrual function, and bone mineral density (BMD)10 existing on a spectrum of health to disease.11–13 Low EA is the underlying etiology of the Triad. The effects of low EA may similarly affect male athletes, including low BMD and suppressed testosterone.14 Recognizing the influence of low EA on health and performance in both female and male athletes, the International Olympic Committee (IOC) proposed a revised framework termed Relative Energy Deficiency in Sport (RED-S).15 The 2018 IOC Update on RED-S emphasizes the importance of low EA in athletes with disabilities and calls for greater research to understand the unique health concerns of this population.16

Given the paucity of literature related to impaired bone health specific to adaptive sports athletes, prevention and treatment strategies are often extrapolated from current standards of care and evidence-based practice within the able-bodied athletic population. However, injury and illness may have more profound functional implications for adaptive athletes.17,18 The aim of this article is to review the current literature with regard to the influence of sports participation and associated risk factors for impaired bone health in athletes with disabilities.

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METHODOLOGY

In June 2018, a literature review was performed using PubMed and Google Scholar for athletes with 6 major impairment categories: spinal cord injury (SCI), spina bifida, central neurological injury [cerebral palsy (CP) or acquired brain injury], amputee or limb deficiency, short stature or achondroplasia, and visual impairment or blindness (Table 1). These impairment categories were selected given their direct relation to eligible impairment types for elite adaptive sports competition, as described by the International Paralympic Committee (IPC).7,19,20 References were screened utilizing the following inclusion criteria: written in English; relevance to 1 of 6 major impairment categories in an athletic population; and relevance to bone health, energy or micronutrient availability, and menstrual function. This screening process yielded 13 original articles and 2 review articles specific to adaptive sports athletes (Table 2).7,21–34

TABLE 1

TABLE 1

TABLE 2

TABLE 2

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DEFINITIONS

Bone Mineral Density

BMD is a clinical measure used to define bone health. The International Society for Clinical Densitometry describes age-matched Z-score ≤−2.0 as “below the expected range for age” in premenopausal women and men younger than 50.35 In contrast, “low BMD” is defined by the American College of Sports Medicine for female athletes in weight-bearing sports as BMD or bone mineral content Z-scores between −1.0 and −2.0 with other risk factors for impaired bone health.10 Similar criteria have been proposed for male athletes.36 Appropriate thresholds for defining low BMD in adaptive athletes is currently unknown.

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Energy Availability

EA is defined as the difference in energy intake and energy expenditure standardized to fat-free mass per day (kcal/FFM/d).37 Thus, EA can be affected by changes in nutrition, exercise status, and impairment-specific changes in FFM. Adequate EA in healthy active female individuals is defined as ≥45 kcal/kg FFM/d and low EA as ≤30 kg FFM/d.12,38 EA thresholds have not been well described for male or adaptive athletes.16

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RESULTS

Effects of Sport Participation by Impairment Category on BMD

Spinal Cord Injury

To date, the largest body of literature on bone health in adaptive sports is focused on the SCI population. A recent longitudinal study found that 8 months of regular wheelchair rugby training resulted in significantly increased bone mineral content, bone area, and lean mass in the arms of tetraplegic male athletes, as well as reduced total body fat. Authors concluded that regular wheelchair rugby training produces a favorable metabolic profile in athletes with SCI.21 Predictably, no similar findings were noted in the lower extremities, which were not subjected to increased loading during sport.

Two cross-sectional studies investigating BMD in athletes with SCI were identified. An investigation of male wheelchair athletes found that BMD was negatively correlated with time since injury, but that faster return to sport following SCI was associated with higher BMD for total body, trunk, and lower extremity independent of age and sport.22 These findings suggest that timely return to sport may attenuate known decreases in BMD below the level of injury. This study also reported that BMD in the legs of wheelchair athletes was 23% lower than able-bodied athlete controls.22 Another study found that elite paraplegic male wheelchair basketball players had increased BMD in the distal radius compared with sedentary paraplegic controls.23 BMD was similarly decreased below the level of injury in both groups.23

Collectively, these studies suggest positive effects on bone health in adaptive athletes with SCI, including higher BMD in the upper extremities and potential attenuation of bone loss in the lower extremities. Despite this, it is important to note that individuals with SCI commonly experience persistent, and often profound, deficits in lower extremity BMD due to reduced skeletal loading. These changes often lead to osteoporosis and increased fracture risk, particularly in women.39–41 It is unknown how these training-mediated improvements in bone health modify injury rates in adaptive athletes with SCI. In addition, it remains unclear if and how these improvements may be sustained over time among individuals with SCI.

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Central Neurological Injury

A single cross-sectional study investigating bone health in 6 male Paralympic sprinters with hemiplegic CP demonstrated no measurable differences in BMD or BMD Z-scores between affected and unaffected sides, despite a15% reduction in FFM on the affected side.24 These suggest that Paralympic-level exercise training for athletes with CP results in positive physiological adaptations, including preserved BMD in the affected side over time.

Reductions in BMD and increased fracture risk are well-documented in the non-athlete CP population and are predicted by ambulatory status, Gross Motor Function Classification System level, and nutritional status.42–44 A Subtype of CP has also been shown to affect BMD in nonathletes with lower Z-scores at the femur in adults with spastic CP compared with those with dyskinetic CP.43 Long-term use of anticonvulsants in this population has also been found to reduce BMD.44 Given multifactorial contributions to impaired bone health in those with CP, preservation of BMD in the affected limbs of Paralympic sprinters with primarily spastic CP appears to be a clinically important finding,24 though overall evidence remains limited.

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Other Impairment Categories

Our review did not identify literature related to BMD in athletes with spina bifida, limb deficiency, short stature, or visual impairment.

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Additional Risk Factors for Impaired Bone Health

Energy and Micronutrient Availability

In both the RED-S and Triad, low EA is the underlying etiology resulting in impaired BMD.10,13,15,16 To date, there are no studies evaluating the relationship between EA and bone health in adaptive sports athletes. Current literature investigating EA in athletes with disabilities is primarily focused on the SCI population who have 25% to 70% reduction in energy expenditure compared with able-bodied athletes.25 Male and female elite wheelchair athletes with SCI and spina bifida appear to meet total energy requirements based on dietary intake,26–28 though there is a suggestion that intake may be insufficient in some athletes.29 An increase in disordered eating behaviors has been reported for both female and male athletes with SCI.30 In addition, reduced EA, as defined by criteria for able-bodied athletes, has been demonstrated in male and female Paralympic sprinters with visual impairment, hemiplegic CP, and distal upper limb deficiency with mean EA of 36 to 39 kcal/kg FFM/d.31 Over 80% of athletes in this study did not meet adequate EA of ≥45 kcal/kg FFM/d.31

Furthermore, all identified studies examining micronutrient availability in adaptive athletes revealed considerable and consistent deficiencies, specifically in several micronutrients necessary for maintaining adequate bone health. Vitamin D insufficiency or deficiency was common among SCI, spina bifida, and limb-deficient athletes, both male and female, ranging from 55% to >95%,26–29,32,33 in addition to inadequate calcium and magnesium intake.26–29 Of note, up to 70% of wheelchair athletes did not use vitamin supplements or did so on an irregular basis.28,33 A longitudinal, interventional study supplemented 20 elite male wheelchair athletes with known vitamin D insufficiency/deficiency with 6000 IU vitamin D3 daily for 12 weeks and reported that all participants increased serum 25(OH)D to optimal levels defined as100 to 220 nmol/L, or 40 to 88 ng/ml.34 Given the potential for both macronutrient and micronutrient deficiencies, adaptive athletes may be at increased risk for impaired bone health.

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Reproductive Hormonal Dysfunction

To date, there are no studies examining the influence of menstrual health, estradiol levels, or testosterone levels on bone health in athletes with any of the specified impairment categories.

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DISCUSSION

Our review of the literature identified limited studies describing bone health in the adaptive sport population. Similar to able-bodied athletes, limited investigations demonstrate a consistent and positive effect of sports participation on bone health, likely resulting from increased weight-bearing and biomechanical demands specific to the site of loading as demonstrated in athletes with hemiplegic CP and SCI.22,24 It follows that the same concept should hold true for other populations with limited weight-bearing or reduced BMD as a result of impairment, such as individuals with spina bifida,45 limb deficiency,46 achondroplasia,47 and visual impairment.48 These populations require further investigation to characterize bone health. In addition, further studies are needed to better understand sport-specific effects. There is evidence that high-volume functional electrical stimulation cycling can improve lower extremity BMD in chronic SCI,49 while cycling and swimming have been shown to have neutral to negative effects on BMD in able-bodied athletes.50–52 No studies to date describe consequences of sports-related injury associated with impaired bone health in adaptive sport.

Although no studies were identified directly evaluating low EA and bone health in adaptive athletes, optimizing nutrition is important for all athletes. Athletes with visual impairment, CP, and limb deficiency have all been found to meet criteria for reduced EA in training settings, regardless of sex.31 Although it is likely that visually impaired and distal upper extremity amputee sprinters have similar EA needs compared with able-bodied athletes, literature in nonathletes with disabilities suggests this is likely not the case for athletes with SCI,25 spina bifida,53 CP,54 and more proximal or lower extremity limb deficiency.55 Given extreme variations in energy expenditure compared with the general population, impairment-specific and even disability-specific recommendations for optimal EA are necessary for adaptive athletes to prevent energy deficiency, a cornerstone of the Triad and RED-S that may translate to impaired bone health.

In addition, there is strong evidence to support that, even given adequate energy intake, significant deficiencies are widespread in this population for micronutrients essential to maintaining adequate bone health. Vitamin D insufficiency or deficiency was found in a large majority of male and female SCI, CP, and limb-deficient athletes,26–29,32,33 in addition to inadequate calcium and magnesium intake.26–29 Notably, most adaptive athletes did not regularly use vitamin supplements,28,33 which may exacerbate immobility-related deficits in bone health. Certainly, the combination of reduced EA, micronutrient deficiency, and variable energy expenditure increase risk for impaired bone health.

Low EA may also occur with or without disordered eating.13,15,16 Disordered eating behaviors and overt eating disorders may be present among certain subgroups of adaptive athletes, including men.30,56,57 For some athletes, these behaviors may develop as a result of performance or sport-specific aesthetic concerns or due to a focus on weight control as a means to compensate for disability, increase mobility, and ease caregiver exertion.56,57 This is an important consideration given increasing competitive opportunities for athletes requiring higher levels of support.58

Development of menstrual dysfunction in athletes with chronic impairments has not been investigated, but this may serve as a warning sign of low or reduced EA just as in the able-bodied population. Similar effects of low EA on testosterone in male adaptive sport athletes are important to characterize.

Our review does suggest that sports participation may result in beneficial changes to bone health, but there are limitations. The few studies that do exist investigating adaptive sports populations are limited in sample size and primarily focus on male individuals with SCI. Most studies are cross sectional and do not have a control population of nonathletes with disabilities. Studies on overuse and traumatic bone injuries were not identified. Prospective studies in larger populations of adaptive sports athletes that incorporate both measures of bone quality and other factors, including nutrition and hormonal status, could clarify our understanding of impaired bone health in this population.

Priorities for future research are described in a recent review article studying components of the Triad in individuals with disability.7 Despite limited research in the field, clinicians may extrapolate certain preventative and treatment recommendations for impaired bone health in adaptive sports athletes given currently available evidence (Fig. 1). For athletes with impaired mobility resulting in decreased weight-bearing and higher risk for reduced BMD and fractures, a focused early intervention with intensive loading activities and timely return to sport may help to preserve or attenuate loss of BMD to a certain degree.21–23 In addition, evaluation of vitamin D status should be completed for all adaptive athletes.59 When appropriate, further evaluation with screening DXA and/or metabolic workup can be pursued, similar to that for able-bodied athletes.13,15,16 Dietary interventions and counseling should be individualized59 and focus on adequate EA and calcium, vitamin D, and magnesium intake guidelines, along with consideration for vitamin D supplementation.

FIGURE 1

FIGURE 1

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CONCLUSIONS

Although the foundation of scientific literature in this field is growing, much remains unknown with regard to the effect of sports participation on bone metabolism and risk factors for impaired bone health in adaptive sports athletes. Given increasing participation in community-based athletic programs up through Paralympic-level competition, the sports medicine community would be remiss in not optimizing care for this emerging group of athletes with disabilities. Limitations in mobility, energy and/or micronutrient deficiencies, and reproductive or endocrine dysfunction may all contribute in a multifactorial manner to impaired bone health. Impairment—and even disability—specific guidelines for normative BMD Z-scores and adequate EA are necessary to guide future preventative and treatment interventions tailored to optimizing bone health in adaptive athletes. In addition, increased insight with regard to prevalence, injury risk, and performance effect of impaired skeletal health is needed. Educational efforts must continue to be a priority and will likely be most effective with an integrated, multidisciplinary approach including the athlete, his or her support system, coaching staff, and health care provider team.

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Keywords:

adaptive sports; adaptive athlete; Paralympics; bone health; bone mineral density; energy availability; micronutrient availability

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