Site-Specific Bone Mineral Density Is Unaltered ... - Injury from Birth

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paralympic athletes with cerebral palsy: preliminary findings. .... who compete at the level of the Paralympic. Games. There is evidence of lower BMD and FFSTM.
Authors: Phoebe Runciman, PhD Ross Tucker, PhD Suzanne Ferreira, PhD Yumna Albertus-Kajee, PhD Lisa Micklesfield, PhD Wayne Derman, MBChB, PhD

Cerebral Palsy

ORIGINAL RESEARCH ARTICLE

Affiliations: From the Division for Exercise Science and Sports Medicine, University of Cape Town, South Africa (PR, YA-K, LM, WD); Department of Sport Science, Stellenbosch University, Stellenbosch, South Africa (SF); International Olympic Committee Research Centre, Cape Town, South Africa (WD); MRC/Wits Developmental Pathways for Health Research Unit, Department of Paediatrics, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa (LM); Division of Orthopaedic Surgery, Institute of Sport and Exercise Medicine, Stellenbosch University, Stellenbosch, South Africa (PR, WD); and Department of Medicine, University of the Free State, Bloemfontein, South Africa (RT).

Correspondence: All correspondence and requests for reprints should be addressed to: Phoebe Runciman, PhD, Institute of Sport and Exercise Medicine, Stellenbosch University, Stellenbosch, South Africa.

Site-Specific Bone Mineral Density Is Unaltered Despite Differences in Fat-Free Soft Tissue Mass Between Affected and Nonaffected Sides in Hemiplegic Paralympic Athletes with Cerebral Palsy Preliminary Findings ABSTRACT Runciman P, Tucker R, Ferreira S, Albertus-Kajee Y, Micklesfield L, Derman W: Site-specific bone mineral density is unaltered despite differences in fat-free soft tissue mass between affected and nonaffected sides in hemiplegic paralympic athletes with cerebral palsy: preliminary findings. Am J Phys Med Rehabil 2016;00:00Y00.

Objective: This study investigated bone mineral density (BMD, g/cm2), fat

Disclosures:

mass (FM, kg), and fat-free soft tissue mass (FFSTM, kg) in Paralympic athletes with cerebral palsy (CP) using dual-energy x-ray absorptiometry.

Financial disclosure statements have been obtained, and no conflicts of interest have been reported by the authors or by any individuals in control of the content of this article.

Methods: Bone mineral density, BMD Z scores (standard deviations), FM, and FFSTM were measured for the whole body and at the lumbar spine, femoral neck, and total hip sites on both nonaffected and affected sides of 6 athletes with hemiplegic CP. Results: There were no differences between nonaffected and affected sides

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with respect to site-specific BMD and BMD Z scores and FM. Fat-free soft tissue mass was significantly lower on the affected side in both upper and lower limbs (15% lower; P G 0.05).

Conclusion: The present study is the first to describe similar BMD between sides, symmetry in FM, and asymmetry in FFSTM in Paralympic athletes with CP. These findings have important consequences for rehabilitation, as they indicate the potential for positive physiological adaptation as a result of exercise training over long periods of time. Key Words:

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Disability, Body Composition, Athletic, Elite, Muscle, Rehabilitation

Body Composition in Athletes with Cerebral Palsy

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umerous developmental disorders, including cerebral palsy (CP), have been associated with abnormal growth and physical development, owing to damage to one or more physiological systems at a young age. Individuals with CP are characterized as having limb asymmetry, shorter stature, lighter body mass, and lower levels of bone mineral content and density than able-bodied controls.1,2 Van den Berg-Emons (1998) measured basic body composition using 4-site skinfold measurements in 20 adolescents with CP, aged 7 to 13 years. Whole body fat percentage was 18% higher in the CP group than the control group (mean [SD], 21.8 [6.1] kg vs. 17.9 [5.0] kg), despite similar muscle mass between the groups.3 Chad et al2 compared 17 ambulant and nonambulant individuals with CP (7.6Y13.8 years) to 894 able-bodied individuals in a pediatric database using dual-energy x-ray absorptiometry (DXA) total body scans. Bone mineral content (BMC, a measure used in pediatric populations) and density (BMD) were calculated at the proximal femur, femoral neck (FN), and in the total body, whereas fat mass (FM) and fat-free soft tissue mass (FFSTM, total mass minus fat and bone mass) were calculated in the total body. Bone mineral content Z scores, which represent age- and sex-matched normative values, were found to be 1.8 standard deviations (SDs) lower in the total body scan and 3.2 SDs lower in the FN site of individuals with CP, compared to the control group. Bone mineral content and BMD were both lower in nonambulant children than ambulant children with CP. Furthermore, although FM was similar between CP and control groups, FFSTM was 2 SDs below the control group, which is in agreement with the reductions in BMC and BMD.2 Recent studies on individuals with CP have investigated the contribution of non-nutritional factors in the body composition of these individuals, disputing previous research that attributed low BMD in children with CP to vitamin D deficiency.2,4Y6 These studies focused on the functional weightbearing bones of the hip, which contain mostly cortical bone, which responds to mechanical loading. It was proposed that the lower BMC, BMD, and FFSTM reported in these individuals with CP were the result of low volumes of ambulation, and subsequent lower bone and muscle loading in these patients. Both ambulant and nonambulant CP groups, however, presented with at least 1 SD lower BMD and BMC compared to the control database.2 The effect of mechanical loading on BMD in cortical bone is well established. Research conducted on astronauts returning from long-term space

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travel has definitively correlated the lack of mechanical loading to significant losses in BMD.7 When investigating the effect of unilateral loading on BMD in athletic individuals, research has shown that BMC and BMD are significantly increased in the dominant arm of squash and tennis players, compared to nondominant and control group arms.8,9 This increase was not related to isokinetic concentric strength of surrounding muscles but rather the high levels of loading over long periods of time required by volleyball and racquet sports.8 In these studies, high BMD was negatively correlated to starting age of high-level training, indicating the younger the athletes started training (prepubescent vs. postpubescent), the higher the dominant arm BMD. This has been equated to a 22% higher humeral BMD in the dominant arm (prepubescent starting age) compared to only 9% higher humeral BMD in individuals starting the sport at a postpubescent age.9 It would therefore be intriguing to investigate BMD, FFSTM, and FM in elite hemiplegic athletes with CP who compete at the level of the Paralympic Games. There is evidence of lower BMD and FFSTM in individuals with CP, independent of levels of ambulation. Furthermore, high levels of BMD have been associated with high levels of weight bearing involved in continued exercise participation in ablebodied individuals. Therefore, studying a group of elite athletes with CP who have undergone high levels of intensive athletic training over many years may further our understanding of the complex interaction between weight bearing, exercise, and CP. To our knowledge, BMD and body composition of athletes with CP using DXA has not been described previously. We therefore aimed to describe BMD, FM, and FFSTM in 6 elite male Paralympic athletes with hemiplegic CP.

METHODS Participants Six male elite Paralympic athletes with CP were recruited for the study (CP group; 5 with spastic hemiplegic CP and one with athetoid hemiplegic CP). Ethnic distribution was 4 white ancestry, one mixed ancestry, and one black ancestry. All participants were track sprinters with hemiplegic CP, as diagnosed by a physician. They all competed in track athletics at national and international Paralympic levels. The athletes have specialized in track and field athletics for 4 to 12 years and participate in elite level training, ranging from 6 to 20 hours per week. Four of the participants were classified as

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T37 and 2 athletes as T38 athletes, in accordance with the criteria established by the Cerebral Palsy International Sport and Recreation Association and International Paralympic Committee for Paralympic competition. T37 athletes are classified as having true ambulant spastic hemiplegia and present with distinctive hemiplegic limitations, with a fully functional nonaffected side. T38 athletes are distinguished by limitations in running activities in any limb distribution, as a result of hypertonia, ataxia, or athetosis.10,11 Both T38 and T37 athletes fall into levels I to II on the Gross Motor Function Classification System.12 Each participant provided written informed consent before the study. The study was approved by the University"s Research and Human Ethics Committee (Ref: 156/2011).

Dual Energy X-Ray Absorptiometry (DXA) Scan Participants" height (m) and weight (kg) was recorded on a calibrated scale (Seca, Model 708, Germany) and body mass index (BMI, kg/m2) was calculated. Both height and weight were measured while the participant was wearing minimal clothing, and without shoes. Bone mineral density as well as FM and FFSTM were measured using dual-energy x-ray absorptiometry (DXA; Hologic Discovery-W software version 13.4.1, Hologic Bedford Inc., Bedford, MA).

Bone Mineral Density (BMD) Whole body (WB), lumbar spine (LS), FN, and total hip (TH) BMDs were measured and expressed as g/cm2. Bone mineral density Z scores, which represent a participant"s comparison to age- and sex-matched controls in the DXA reference database of age and sex controls, were calculated by the DXA software and expressed as SDs away from the control database. One measurement was given for WB

and LS, whereas bilateral measurements were given for FN and TH for nonaffected and affected sides.

FM and FFSTM Total fat mass (FM) and FFSTM (total body mass minus fat mass and bone mass) were measured for individual upper limb (arm) and lower limb (leg) as well as unilateral appendicular limb distributions and expressed as kilograms (kg). Measurements were given for nonaffected and affected sides in the aforementioned groupings of limbs.

Statistics All data were analyzed using statistical software (Statistica 12, Statsoft Inc. Tulsa, Oklahoma). As this was a descriptive study of one group of athletes (N = 6), statistical analyses were not performed on whole body total values (height, weight, BMI, WB BMD, LS BMD, WB BMD Z score, and LS BMD Z score). Paired t tests were performed to compare differences in FN BMD, TH BMD, FN BMD Z score, TH BMD Z score, upper limb FM, lower limb FM, appendicular limb FM, upper limb FFSTM, lower limb FFSTM, and appendicular limb FFSTM between nonaffected and affected sides. Significance was accepted at P G 0.05.

RESULTS Participants Table 1 presents descriptive characteristics of 6 athletes with CP with regard to class and level of competition, diagnosis, resting spasticity level, hemiplegic involved side, and current 100-m performance time in seconds (s) as a general overview of the current sample.

Age and Body Composition Table 2 presents data for body composition, BMD, BMD Z score, FM, and FFSTM. Mean (SD) age

TABLE 1 International Paralympic Committee competition classification, level of competition, diagnosis, resting Ashworth Scale spasticity level, involved side, and current 100-m sprint time of 6 participants with CP

Participant IPC Class Level of Competition 1 2 3 4 5 6 Mean (SD)

T 37 T 38 T 37 T 37 T 37 T 38 V

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Paralympic Paralympic Paralympic National Paralympic Paralympic

100-m Resting Spasticity Involved Side Time (s)

Diagnosis Hypertonic hemiplegia Hypertonic hemiplegia Hypertonic hemiplegia Hypertonic hemiplegia Hypertonic hemiplegia Athetoid hemiplegia V

1Y2 1Y2 1Y2 1Y2 1Y2 V

Right Left Right Right Right Left V

11.54 11.29 12.21 12.49 12.6 11.21 11.9 (0.9)

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TABLE 2 Descriptive data of body composition, BMD, BMD age-matched Z scores (BMD Z score), FM, and FFSTM of 6 Paralympic athletes with CP Total Age, years Body composition Height, m Weight, kg BMI, kg/m2 Bone mineral density Whole body BMD, g/cm2 Lumbar spine BMD, g/cm2 Femoral neck BMD, g/cm2 Total hip BMD, g/cm2 Whole body BMD Z score Lumbar spine BMD Z score Femoral neck BMD Z score Total hip BMD Z score Fat mass Upper limb FM, kg Lower limb FM, kg Appendicular FM, kg Fat-free soft tissue mass Upper limb FFSTM, kg Lower limb FFSTM, kg Appendicular FFSTM, kg

Nonaffected

Affected

0.979 (0.080) 1.092 (0.087)

0.932 (0.124) 1.053 (0.124)

0.400 (0.626) 0.417 (0.567)

0.050 (0.909) 0.133 (0.809)

0.42 (0.11) 1.46 (0.46) 1.89 (0.56)

0.46 (0.14) 1.58 (0.51) 2.04 (0.65)

3.60 (0.39) 10.34 (0.82) 13.94 (1.18)

2.96 (0.44)* 8.81 (0.27)* 11.77 (0.64)*

23.3 (3.8) 1.76 (0.03) 68.59 (2.73) 22.14 (1.40) 1.164 (0.081) 1.117 (0.072) j0.150 (0.547) 0.250 (0.672)

Total scores are provided for variables only available as whole body measurements, and unilateral values are given for variables divided into nonaffected and affected sides. Fat mass and FFSTM are divided by limb, as well as appendicular distributions. *P G 0.05 group effect between nonaffected and affected sides in FFSTM.

for the participants was 23.3 (3.8) years. Mean (SD) height and weight were 1.76 (0.03) m and 68.59 (2.73) kg. Mean (SD) BMI was 22.14 (1.40) kg/m2.

BMD and BMD Z Scores There were no differences between WB, LS, FN, and TH BMD or BMD Z scores (Table 1, Fig. 1).

FM and FFSTM There were no differences between affected and nonaffected FM in any limb distribution (Table 1, Fig. 2). Upper limb FFSTM was significantly lower on the affected side compared to the nonaffected side (Table 1, Fig. 2B; 2.96 [0.44] kg vs. 3.60 [0.39] kg; P G 0.05). Lower limb FFSTM was significantly lower on the affected side (8.81 [0.27] kg for affected and 10.34 [0.82] kg for nonaffected; P G 0.01). Appendicular FFSTM was also significantly lower on the affected side compared to the nonaffected side (11.77 [0.64] kg vs. 13.94 [1.18] kg; P G 0.01).

DISCUSSION The present study is the first to describe BMD and body composition in elite Paralympic athletes with CP. Bone mineral density, FM, and FFSTM were measured at whole body sites as well as at unilateral sites on the nonaffected and affected sides.

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The first important finding was that there was no significant difference in FN and TH BMD and BMD Z scores between nonaffected and affected sides in this group of athletes with CP (Table 1, Fig. 1). There was no difference in absolute BMD between the nonaffected and affected sides (Fig. 1A), and although there was a tendency toward differences in BMD Z scores between the nonaffected and affected sides, they did not reach significance (Fig. 1B). Furthermore, although not significantly different, BMD Z scores of the LS, FN, and TH were above that of the age- and sex-matched able-bodied individuals in the control database. Whole body BMD was the only testing site where a lower-than-average Z score was observed. This finding indicates that BMD measures in this group of athletes were closely matched to the able-bodied individuals in the normative database. The second important finding was the difference observed in FFSTM between nonaffected and affected sides, despite similarities in FM between the sides (Table 1, Fig. 2). There were no differences in FM between nonaffected and affected sides in any of the upper limb, lower limb, or appendicular limb distributions (Fig. 2A). It is widely accepted that various physiological systems are impaired in individuals with CP as the result of brain damage at a young age and widespread neuromuscular dysfunction.13 Individuals with CP also present with secondary complications

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FIGURE 1 Bone mineral density (A) and bone mineral density age-matched Z scores (B) for specific locations in the body, including whole body (WB), lumbar spine (LS), FN nonaffected side, FN affected side, TH nonaffected side, and TH affected side. No differences were seen in BMD and BMD Z scores between sides in FN or TH.

due to the initial movement disorder and physical inactivity. Previous research has demonstrated that individuals with CP show significant reductions in functional capacity and exercise performance compared to able-bodied individuals. These deficits have been documented as a 30% to 73%, 15% to 42%, and 27% to 46% reduction in strength, aerobic capacity, and anaerobic capacity, respectively.14Y20,20Y24 These data are similar in magnitude to the 1.8 to 3.2 lower SD BMD Z scores observed in similar samples of individuals with CP.2 These studies, however, were conducted using sedentary children. There has been very little research conducted on adults with CP, and even less on adults with CP who undertake regular physical activity. Thus, sedentary behavior has been an influencing factor in the research conducted on the physical capacity of individuals with CP. We have previously shown using exercise trials that adult elite athletes with CP display significantly smaller deficits in exercise performance than the values provided by the literature. These deficits equated to www.ajpmr.com

10% lower anaerobic capacity and 6% lower sprint capacity, when compared to able-bodied athletes.25,26 Interestingly, we reported that the affected leg of the CP group produced significantly less power than that of the nonaffected leg during maximal vertical jump testing, whereas the nonaffected leg performed at the same capacity of both legs in the able-bodied control group. We also found that this deficit in power generation negatively affected tasks performed on both legs simultaneously in the CP group. We attributed the overall physiological similarities between athletes with CP and able-bodied athletes to the effect of high-level athletic training over many years, which is required for Paralympic competition. Therefore, the findings of similar BMD, BMD Z scores, and FM in the present study support our previous findings in exercise trials that showed that elite athletes with CP present with similar physiology to able-bodied individuals. These findings may highlight the importance of high levels of exercise training for all individuals with CP. Furthermore, the greater-than-average BMD Z scores Body Composition in Athletes with Cerebral Palsy

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FIGURE 2 Fat mass (FM) (A) and FFSTM (B) for specific locations in the body, including the upper limb nonaffected side, upper limb affected side, lower limb nonaffected side, lower limb affected side, and combined upper and lower limb nonaffected and affected sides, for unilateral FM and FFSTM) distributions. There were no differences between nonaffected and affected with regard to FM. *P G 0.05 difference between nonaffected and affected sides in FFSTM.

in the FN and TH, despite lower WB BMD, may indicate that athletes with CP who have undergone long-term exercise training have higher BMD in cortical bone sites in the body, which respond to load-bearing stress. Similarly, the finding of comparable FM between nonaffected and affected sides provides further evidence for the benefits of long-term athletic training on health parameters in individuals with CP. However, the finding that FFSTM was lower on the affected side in this group of athletes indicates that there may be a ceiling toward which adaptation may occur. That is, although bone and FM may be highly adaptable in individuals with CP, the central inhibition of muscle recruitment, which results in the inability to recruit available motor units in affected muscles, as well as neuromuscular deficits typically observed in CP, may still have a large effect on muscle size, function, and physiology.15,27,28 The combination of these findings has important implications for the involvement of children

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with CP in exercise as a management or rehabilitative tool. As discussed earlier, it has already been established that engaging in physical activity has positive effects on functional performance in children with CP. It has also been established that loading of the bone through physical activity, especially from a young age, increases BMD in weightbearing sites.8 This study of adult athletes with CP has allowed us to investigate a group of individuals that have already been engaging in high levels of physical activity over many years. This allows rehabilitative professionals to understand the possible adaptation of bone, and as a consequence, the adaptation of other physiological systems, due to exercise training. Thus, there may be a significant number of children who have the capacity to participate in high-level exercise training from a young age. This needs to be explored and confirmed with a longitudinal intervention study, exposing individuals with CP to a weight-bearing exercise training program, since we cannot exclude the possibility that

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our group of athletes with CP may have had greater BMD and other measured variables before their exercise training. The present study provided novel insight into the BMD, FM, and FFSTM of elite Paralympic athletes with CP. We acknowledge that limitations of the study include the small sample size, differences in ethnic selection of the sample, lack of a control group, and lack of longitudinal tracking of BMD over time. This study was conducted in a finite group of elite athletes, where no more than 6 athletes were available, which also applies to the combination of 4 white ancestry participants, one mixed ancestry participant, and one black ancestry participant in the sample. However, all participants were males, and comparisons were made between each individual"s nonaffected and affected sides, making differences in ethnicity less important to the conclusions made in the present study. It is suggested that future studies compare athletes" results with regard to ancestry, in a larger sample, to investigate the contribution of race to bone, fat, and muscle properties in these individuals. We did not include a control group but compared our data to an age- and sex-matched control database. Future research is required comparing body composition of a larger sample of athletes with CP to ablebodied athletes, as well as untrained able-bodied/CP individuals, to further understand the findings of the present study and consequently the possibly implications of this research.

CONCLUSION The present study offers the first novel insights into in-depth body composition and BMD of elite Paralympic athletes with CP. Similar BMD and FM between nonaffected and affected sides may indicate that high levels of athletic training over many years may result in physiological adaptation toward ablebodied levels. However, asymmetries in FFSTM and slightly-lower-than-average WB BMD indicates that there may be a limit to the adaptation observed in the present study. The findings of the present study provide further evidence to a growing body of research that indicates that high levels of exercise from a young age may be beneficial to individuals with CP.

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