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.
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
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.
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.
Other Impairment Categories
Our review did not identify literature related to BMD in athletes with spina bifida, limb deficiency, short stature, or visual impairment.
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.
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.
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.
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:Copyright © 2019 Wolters Kluwer Health, Inc. All rights reserved.
adaptive sports; adaptive athlete; Paralympics; bone health; bone mineral density; energy availability; micronutrient availability