Archives of Physical Medicine and Rehabilitation
Volume 90, Issue 7 , Pages 1127-1135, July 2009

A Study of Bone Mineral Density in Adults With Disability

Presented to the American Academy of Physical Medicine and Rehabilitation, September 27, 2007, Boston, MA.

  • Éimear M. Smith, MRCPI

      Affiliations

    • Department of Rehabilitation Medicine, National Rehabilitation Hospital, Dublin, Ireland
    • Corresponding Author InformationReprint requests to Éimear M. Smith, MRCPI, Dept of Rehabilitation Medicine, National Rehabilitation Hospital, Dún Laoghaire, Dublin, Ireland
    • ,
  • Catherine M. Comiskey, PhD

      Affiliations

    • School of Nursing and Midwifery, Trinity College, Dublin, Ireland
    • ,
  • Áine M. Carroll, MRCP

      Affiliations

    • Department of Rehabilitation Medicine, National Rehabilitation Hospital, Dublin, Ireland

Article Outline

Abstract 

Smith ÉM, Comiskey CM, Carroll ÁM. A study of bone mineral density in adults with disability.

Objectives

To examine prevalence of low bone mineral density (BMD) among adults with disability, using World Health Organization diagnostic categories.

Design

Cross-sectional study.

Setting

National Rehabilitation Hospital, Dublin, Ireland.

Participants

Patients (N=255; 178 men, 77 women) who were disabled for at least 3 months because of acquired brain injury, spinal cord injury, other neurologic condition, or lower-limb amputation.

Interventions

None.

Main Outcome Measures

Laboratory investigations including intact parathyroid hormone, 25-hydroxyvitamin D (25-OHD), and sex hormones; and BMD of lumbar spine and at least 1 hip, measured by dual-energy x-ray absorptiometry and expressed as T scores and z scores.

Results

Mean age ± SD of participants was 48.7±15.6 years. Vitamin D deficiency, 25-OHD level 50nmol/L or less, occurred in 154 (62.9%); insufficiency, a level between 51 and 72nmol/L, occurred in 36 (14.7%). Based on T scores, 108 participants (42.4%) had osteopenia, and 60 (23.5%) had osteoporosis. A z score of −1 or less but more than −2 occurred in 76 (29.8%); a further 52 (20.4%) had a z score of −2 or less. On multiple linear regression analysis, ambulatory status and duration of disability were independent predictors of BMD at neck of femur (β=.152, P=.007; β=−.191, P=.001, respectively) and total proximal femur (β=.170, P=.001; β=−.216, P<.001, respectively).

Conclusions

Osteopenia and osteoporosis are very common in adults with disability participating in rehabilitation, compared with the general young adult population. Duration since onset of disability and mobility status are independent predictors of BMD at the hip. Bone health monitoring should form part of the long-term follow-up in adults with newly acquired disabilities.

Key Words: Bone density, Disabled persons, Osteoporosis, Rehabilitation

List of Abbreviations: ANOVA, analysis of variance, BMD, bone mineral density, DXA, dual-energy x-ray absorptiometry, iPTH, intact parathyroid hormone, ISCD, International Society for Clinical Densitometry, QC, quality control, SCI, spinal cord injury, 25-OHD, 25-hydroxyvitamin D, WHO, World Health Organization

 

THE NATIONAL REHABILITATION Hospital, Dublin, Ireland, is a 120-bed unit providing multidisciplinary inpatient and outpatient rehabilitation for adults with neurologic conditions including SCI and acquired brain injury, as well as limb amputation. Despite the wide variation in the nature of disability, our patients would appear to have some common risk factors for osteoporotic fractures,1, 2 either dependent on or independent of BMD, including periods of immobilization, vitamin D deficiency,3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13 hypogonadism,14 high risk of falling, or reported high rates of falls.15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27 Morbidity as a result of fractures has been reported to be higher among those with disability than for the able-bodied population, including longer acute hospital stay, deterioration in mobility, less likelihood of home discharge, and increased mortality.28, 29, 30, 31, 32, 33, 34, 35, 36

Fortunately, fracture risk can now be accurately assessed, with a view to fracture prevention. BMD measurement using DXA at any specific site is the single best predictor of fracture at that site, with the hip representing the site with greatest predictive power.37, 38 In calculating fracture risk based on BMD, actual BMD measurements (g/cm2) are expressed as relative values, T score, and z score, with the T score representing a comparison with the young adult reference mean and z score a comparison with the age-matched mean. According to WHO criteria, a T score of less than or equal to 1 SD below the young adult mean is normative, a T score greater than 1 but less than 2.5 SD below the young adult mean is osteopenia, and a T score of 2.5 SD or more below the young adult mean is classified as osteoporosis. Every SD in BMD below the age-matched mean correlates to an approximate doubling of fracture risk, a relationship best proven in postmenopausal women and men over 50 years of age.1, 37, 39, 40

Two previous cross-sectional studies of inpatients in rehabilitation facilities, with a mean age of 60 years or more, found high rates of low BMD (T score <−1), 65.5% to 68% among female subjects and 73.3% to 85% among male subjects.41, 42 A study of 429 community-dwelling women with a range of disabilities found that 30.5% had osteopenia and 22.6% had osteoporosis, based on peripheral DXA measurement of the calcaneus; prevalence of low BMD was higher in groups with neurologic disorders than musculoskeletal disorders.43

There have been previous studies examining low BMD in adults who have developed various disabilities. However, in the spinal cord–injured population, few of these adhered to WHO recommendations for diagnosis and classification, while most of the work to date in the stroke population has been based on the elderly (≥65y of age). There have been no studies to our knowledge examining bone loss in adults with traumatic brain injury, nor have there been any studies that have categorized BMD of lower-limb amputees according to WHO criteria.

The objective of this study was to measure the prevalence of low BMD, based on WHO diagnostic categories, in adults with disability participating in rehabilitation at our institution, and to investigate for factors that affect and predict BMD in this population, with a longer-term aim of developing guidelines for referral for DXA assessment.

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Methods 

This was a cross-sectional study of patients who were admitted to the National Rehabilitation Hospital, Dublin, Ireland, between August 2006 and March 2007. All patients had been diagnosed with an acquired brain injury, SCI, other neurologic condition, or lower-limb amputation. Patients were eligible to participate if disabled for at least 3 months and aged 16 years or over. The 3-month period chosen was a practical one: by then, patients were expected to be medically stable and able to make an informed decision about participation in the study. In addition, ambulatory status is usually re-established at 3 months. Exclusion criteria were a diagnosis of osteopenia or osteoporosis prior to onset of disability and any acute illness that could have prevented DXA scanning. Ethical approval for the study was obtained from the ethics committee of the National Rehabilitation Hospital. Written patient information was provided and written consent was obtained from all participants or their next-of-kin.

Study participants completed a questionnaire seeking information about demographics, nature of disability and time since onset, history of fractures since onset, and risk factors for osteoporosis. Body mass was recorded. Ambulatory ability was classified as one of “unable to walk at all,” “able to walk indoors only, either with or without a walking aid,” or “able to walk out of doors, with or without a walking aid.” Female subjects were questioned regarding menstrual history and menopausal status. Previous glucocorticoid steroid use was classified as long-term, repetitive, short-term, or never. Any medical conditions the patient had that were known to be associated with low BMD were recorded. Cigarette smoking was calculated as pack-year history. Alcohol consumption was classified as none, low to moderate, or high; low to moderate included all female subjects consuming less than or equal to 14 units a week and all male subjects consuming less than or equal to 21 units a week; high was anything in excess of these figures.

Serum samples were reserved from each patient and the following assays measured: total alkaline phosphatase, corrected serum calcium, iPTH, 25-OHD, follicle-stimulating hormone, luteinizing hormone, and testosterone (male patients only) or estradiol and progesterone (female patients only).

While our laboratory recommended that vitamin D deficiency be based on a value less than or equal to 25nmol/L, and insufficiency, a level between 26 and 52nmol/L, we have chosen to base our classification on the recent, more stringent recommendation that a value of less than 50nmol/L represents deficiency, and up to 72nmol/L, insufficiency.44

BMD was measured using DXA with the Hologic Discovery A,a and all scans were performed by the same operator. In all cases, WHO categories were applied to T score results. The z scores were classified as less than 1 SD below or greater than the mean (within normative range), greater than or equal to 1 but less than 2 SD below the mean, and greater than or equal to 2 SD below the mean.

All patients had densitometry measurements at the lumbar spine and 1 hip, as well as lateral vertebral assessment, except where the latter was precluded by the patient's inability to elevate the arms above the head. In addition, patients with hemiparesis and patients with lower-limb amputation had both hips examined, unless precluded by hip prosthesis. Lumbar vertebrae numbers 1 to 4 inclusive were used to calculate the total lumbar BMD and to categorize according to WHO criteria. A vertebra was excluded from the analysis if its T score was more than 1 SD greater or less than that of the adjacent vertebra. At the hip, neck of femur, greater trochanter, intertrochanteric area, and total proximal femur were measured, although only neck of femur or total proximal femur were used for diagnostic purposes. Lateral vertebral morphometry was performed to eliminate false-negative results because of vertebral fracture.

In the case of 1 patient with acquired brain injury caused by anoxic encephalopathy, only hip BMD was assessed because the patient became restless and the full range of investigations was not possible. Five of the patients who had hemiparesis had DXA assessment of the sound hip only because of a metal prosthesis on the paretic side. Among 6 patients with amputation, only the sound hip was examined because of metal prostheses on the amputated side, or in 1 of those cases, hip disarticulation.

Forearm examination was used for diagnostic purposes in 10 cases in which either lumbar spine or hip could not be measured. At the forearm, BMD measures were taken of the ultra-distal radius, mid-radius, proximal one third, and total radius; only proximal one third was used in assigning a diagnostic category. Patients requiring forearm assessment were as follows: 2 patients with amputation had bilateral total hip replacements, precluding BMD measurement at that site; 1 patient with amputation had had metal fixation to the lumbar spine as a result of a previous injury to the spinal column; in 6 participants with SCI, lumbar spine BMD measures could not be obtained because of metal fixation from the spinal injury; in 1 patient with SCI, hip examination was not possible because of difficulty positioning, secondary to contractures.

Daily QC was performed by scanning a phantom spine, a humanlike spine segment made of calcium hydroxyapatite, enclosed in a block of water-stimulant epoxy. Each daily QC result was compared with 10 separate measurements taken at the time of the system's installation and provided the basis for continuous self-calibration by the system.

As is the recommendation of the ISCD, the operator carried out short-term precision error assessment by measuring hip and lumbar spine BMD of 30 patients twice and entering results into the ISCD calculator. The following precision results were obtained: total hip, 1.4%; femoral neck, 1.7%; and lumbar spine, 1.1%, all within the accepted range.45, 46

Statistical analysis of the data were performed using SPSS version 13.b Descriptive statistics are presented as mean ± SD. Where the data was highly skewed, medians and interquartile ranges are provided. An independent sample t test was used to compare BMD by sex. One-way ANOVA was used to examine the relationships between BMD and each of the following variables: mobility status, use of steroids, other medical conditions, and alcohol consumption. Univariate associations employing correlation coefficient were used to measure the association between BMD and each of the following variables: age, duration of disability, vitamin D status, parathyroid hormone, estradiol and testosterone levels, and cigarette smoking. Finally, a multiple linear regression analysis was performed to identify factors that might be predictors of BMD. Significance is expressed as P less than .05 except for the 21 univariate associations employing correlation coefficient, where significance is expressed as P less than .05/21 (.002).

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Results 

Demographic and Clinical Details 

There were 255 participants in total, 178 men and 77 women. Mean participant age was 48.7±15.6 years. Mean male age was 47.9±14.8 years, and mean female age was 50.5±17.3 years. There were 112 cases of acquired brain injury, either traumatic or nontraumatic; 75 cases of SCI; 52 cases of lower-limb amputation; and 16 other, including 4 cases of multiple sclerosis, 5 cases of critical care neuropathy, 5 cases of Guillain-Barré syndrome, 1 case of hereditary spastic paraparesis, and 1 case of sensorimotor polyneuropathy associated with Churg-Strauss syndrome. All except 2 patients were white, 1 of black and 1 of Asian origin. Duration of disability had a median value of 7 months and an interquartile range of 14.6. Mean body mass was 76.4±17.1kg. Eighty-five patients (33.3%) were unable to walk at all, 65 (25.5%) were indoor walkers only, and 105 (41.2%) could walk outdoors. Sixteen (6.3%) had sustained a fragility fracture since onset of disability, of whom 10 were female.

Nine patients (3.5%) were on long-term steroids, and 16 (6.3%) had had repetitive courses. Apart from steroid use, 65 patients (25.5%) had a medical condition associated with low BMD, for example rheumatoid arthritis, or phenytoin use for management of epilepsy. Nine female subjects (11.7%) had a prior history of amenorrhea. Thirty female subjects (39%) were premenopausal, 5 (6.5%) perimenopausal, and 42 (54.5%) postmenopausal; among the postmenopausal women, average duration since menopause was 17.1±10.3 years. One hundred sixty-four of the 255 participants had smoked during their lives. Median cigarette pack-year history was 8, and interquartile range was 30. Twenty-eight patients (11%) did not consume alcohol, 179 (70.2%) were light to moderate consumers, and 47 (18.4%) were heavy consumers.

Laboratory Results 

In table 1, mean biochemistry and endocrinology values are displayed. Vitamin D results were available on 245 patients. Based on our chosen classification as outlined,44 154 patients (62.9%) had deficient levels of vitamin D, 36 (14.7%) had insufficient levels, and 55 (22.5%) were within the normative range. Among those with vitamin D deficiency, 3 patients had levels of parathyroid hormone and alkaline phosphatase above the normative range. A further 5 had elevated levels of parathyroid hormone only. In 20 (11.3%) of the 177 male participants, serum testosterone level was below the normative range of 8 to 30nmol/L. Laboratory results confirmed hypogonadism in the 42 female participants who reported that they were postmenopausal and in none of the premenopausal group.

Table 1. Mean Laboratory Biochemistry and Endocrinology Values in All Subjects
All (N=255)Men (n=177)Women (n=78)
Corrected serum calcium (mmol/L)2.32±0.12.32±0.12.33±0.1
25-OHD (nmol/L)50±34.3247.31±31.7456.34±39.26
iPTH (ng/L)33.44±19.0731.97±16.8436.9±23.23
Alkaline phosphatase (U/L)91.04±33.1791.38±32.0290.3±35.86
FSH (mIU/mL)17.66±26.357.06±6.8641.22±36.55
LH (mIU/mL)10.15±12.785.42±5.520.64±17.33
Testosterone (nmol/L)—15.03±5.83—
Estradiol (pmol/L)——161±171.3
Progesterone (nmol/L)——2.44±3.34

NOTE. Values are mean ± SD.

Abbreviations: FSH, follicle stimulating hormone; LH, luteinizing hormone.

BMD Results 

Forearm BMD values were normative in the 10 cases in which this site was used in diagnosis. In these 10 cases, 1 other site was also analyzed for diagnostic purposes. BMD at the lumbar spine, neck of femur, and total proximal femur are displayed in table 2, for all study participants, men, women, the 3 groups based on ambulatory ability, and the 3 main disability subgroups.

Table 2. BMD of Total Lumbar Spine, Neck of Femur, and Total Proximal Femur in All Study Participants, Men, Women, Each of the 3 Mobility Groups, and Each of the Main Disability Subgroups
BMD (g/cm2)
Total Lumbar SpineNeck of FemurTotal Proximal Femur
All study participants (N=255)1.002±0.1740.771±0.1590.911±0.183
Men (n=177)1.036±0.1750.802±0.1590.959±0.178
Women (n=78)0.925±0.1460.695±0.1310.797±0.139
Nonwalkers (n=85)1.000±0.1880.739±0.1720.861±0.200
Indoor walkers (n=65)1.015±0.1920.735±0.1340.891±0.161
Outdoor walkers (n=105)0.996±0.1530.816±0.1500.962±0.168
Spinal cord–injured (n=75)1.056±0.1720.792±0.1650.916±0.188
Acquired brain-injured (n=112)0.974±0.1640.779±0.1600.923±0.179
Lower-limb amputees (n=52)0.994±0.2010.724±0.1410.897±0.190

NOTE. Values are mean ± SD.

When the BMD of all study participants was classified based on T scores, 108 (42.4%) had osteopenia and 60 (23.5%) had osteoporosis; in 4 cases, a T score was not supplied because patients were too young. When BMD was classified based on z scores, 76 (29.8%) were greater than or equal to 1 SD but less than 2 SD below the mean, and a further 52 (20.4%) were greater than or equal to 2 SD below the mean; in 1 case, z score was not supplied because the patient was too old. In table 3, each classification is applied to the results from the lumbar spine, hip, and either site.

Table 3. Classification of Bone Mineral Density Results of All Study Participants
Based on T ScoresBased on z Scores
Lumbar SpineHip⁎Any Site Lumbar SpineHip⁎Any Site
Normative149(58.4)96(37.6)83(32.5)Normative170(66.7)146(57.3)126(49.4)
Osteopenia65(25.5)104(40.8)108(42.4)z score ≤−1 and >−249(19.2)67(26.3)76(29.8)
Osteoporosis32(12.5)48(18.8)60(23.5)z score ≤−230(11.8)39(15.3)52(20.4)
Not available†9(3.5)7(2.7)4(1.6)Not available†6(2.4)3(1.2)1(0.4)

NOTE. Values are n (%).

⁎Worst neck of femur or total proximal femur reading considered, including values at the paretic or amputated limb in relevant patients.

†Reasons for nonavailability include metal fixation of the spine, hip prostheses in situ, and age too young or too old for T score and z score classification, respectively.

Of the 20 male subjects whose testosterone levels fell below the normative range, 11 had osteopenia and 3 had osteoporosis. Of the 42 postmenopausal female participants, 20 had osteopenia and 16 had osteoporosis.

Variables Associated With Low BMD 

Independent sample t test was used to compare BMD between sexes; female subjects had significantly lower BMD at the lumbar spine (t244=4.78; P<.001), neck of femur (t249=5.13; P<.001), and total proximal femur (t249=7.01; P<.001) than male subjects.

There was no significant difference in BMD of the lumbar spine regardless of mobility status when examined using ANOVA. However, neck of femur BMD (F2,250=8.14; P<.001) and total proximal femur BMD (F2,250=7.18; P=.001) varied significantly according to mobility status. The results of the post hoc analysis are displayed in an error bar plot in Fig 1, Fig 2. Cross-tabulation and chi-square analysis also found a significant relationship between ambulatory ability and diagnostic category at the hip, with outdoor walkers accounting for most patients with normative BMD and the minority with osteoporosis.

  • View full-size image.
  • Fig 1. 

    Error bar plot showing the effect of ambulatory ability on neck of femur BMD. Abbreviation: CI, confidence interval. *Significantly lower than outdoor walking group.

Results from correlation testing are displayed in table 4. P values reported in table 4 are a result of 3 times 7, or 21, individually computed correlations. In order to reduce the probability of a type 1 error, the P value of .05 has been divided by 21 to obtain a more rigid test of significance, giving a P value of .002 as significant. No correlation was found between vitamin D levels and BMD, although there was a significant negative correlation between iPTH levels and BMD at the hip. Duration of disability was also significantly negatively correlated with hip BMD.

Table 4. Correlations Between BMD and Each of Duration of Disability, Age, Body Mass, 25-OHD, iPTH, Estradiol, and Testosterone Levels
Duration of DisabilityAgeBody Mass25-OHDiPTHEstradiol (Female Subjects)Testosterone (Male Subjects)
RPRPRPRPRPRPRP
Total lumbar spine BMD (g/cm2)−.087.174.023.722.404<.001−.053.417−.192.003.164.164−.015.849
Neck of femur BMD (g/cm2)−.247<.001−.183.004.470<.001−.042.513−.255<.001.128.279−.093.229
Total proximal femur BMD (g/cm2)−.271<.001−.022.735.549<.001−.111.085−.213.001.041.728−.164.033

NOTE. P values reported in table 3 are a result of 3 by 7 or 21 individually computed correlations. In order to reduce the probability of a type 1 error, we have divided the P value of .05 by 21 to obtain a more rigid test of significance. Hence, a P value of .05/21 equal to .002 is significant.

To examine further the relationship between vitamin D, BMD, and mobility status, we performed an ANOVA to look for any association between mobility status and vitamin D level; none was found.

One-way ANOVA showed that use of long-term or repetitive courses of steroids had a significant effect on BMD and T score of the total proximal femur, but post hoc analysis could not be performed because the group size was too small. ANOVA also showed a significant effect of related medical conditions on BMD total hip, T score total hip, z score neck of femur, and z score total hip; again, post hoc analysis was not performed because the groups were too small. One-way ANOVA followed by post hoc analysis found that neck of femur BMD, T score, and z score, and total proximal femur BMD, T score, and z score were significantly greater among low to moderate consumers of alcohol than high consumers or nonconsumers; there was no significant difference between high consumers and nonconsumers. Lumbar spine BMD was significantly greater in low to moderate consumers than nonconsumers, but no different from heavy consumers; again, there was no difference between heavy consumers and nonconsumers. We did not find any significant correlation between cigarette smoking and BMD at any site.

The results of the multiple linear regression analysis on lumbar spine and hip BMD are shown in table 5. The object of the regression was to identify factors that might be predictors of BMD. For ease of comparison of the effects of the 6 independent predictors, we have provided the raw and the standardized beta values. The null hypothesis in each of the multiple linear regressions is that each beta is 0; the difference between the null hypothesis value and the true value of a model parameter is the effect size. Within table 5, it can be seen that sex, body mass, duration of disability, and ambulatory status independently predict BMD at the neck of femur and total proximal femur in this study population; the most powerful predictor, body mass, also acts as an independent predictor of lumbar spine BMD.

Table 5. Multiple Linear Regression Analysis of Bone Mineral Density Measurements and Each of Sex, Age, Duration of Disability, Body Mass, Ambulatory Status, and Nature of Disability
BMD Sites MeasuredLinear Regression P
SexAgeDuration of DisabilityBody MassAmbulatory StatusNature of Disability
bbbbbb
ββββββ
PPPPPP
Total lumbar spine BMD (g/cm2)−.058.000.000.003−.011.023
−.134−.006−.068.310−.052.097
.064.935.294<.001.416.170
Neck of femur BMD (g/cm2)−.046−.002.000.004.028.002
−.126−.163−.191.397.152.009
.046.007.001<.001.007.890
Total proximal femur BMD (g/cm2)−.084.000.000.005.036.001
−.200.010−.216.433.170.004
.001.858<.001<.001.001.949

NOTE: This table shows both unstandardized (b) and standardized (β) beta values from the multiple regression and the associated P value.

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Discussion 

There are few other studies that have examined BMD in a patient population with a range of disabilities. Based on T scores, the number of patients who we found to have low BMD (65.9% at any site) is similar to that in previous studies,41, 42 but far in excess of the quoted rates of 15% with osteopenia and 0.6% with osteoporosis among young healthy women.1 At the lumbar spine and total proximal femur, in excess of 30% and 40%, respectively, had z scores of −1 or less, which probably reflects the influence of disability on their bone status. Considering the mean age of our patients, 48.7 years, and the fact that only 35 (13.7%) of the 255 were over 65 years of age, the frequency of low BMD is a cause for concern. While the relationship between T score and fracture risk is not as well established in younger people, if low BMD is not addressed, these people will enter the later stages of their lives with osteopenia and osteoporosis already established, at which point their fracture risk is likely to increase significantly.

A very high number of our patients had insufficient (14.7%) or deficient (62.9%) levels of 25-OHD. Such findings are not unique. Fifty-three patients participating in inpatient rehabilitation for a range of reasons had a 33.9% prevalence rate of vitamin D insufficiency and a 49.1% rate of deficiency, using the same ranges as we have used.42 Even when using less rigorous ranges, between 70% and 98% of elderly patients with stroke were found to have low levels of vitamin D, lack of sunlight exposure, and immobilization-induced hypercalcemia cited as the likely reasons, although it was also possible that deficiency predated stroke.6, 7, 8, 11, 47 Among patients with multiple sclerosis, 46% to 69.3% were found to have vitamin D levels below the normative range.48, 49, 50 It is worth noting that in our patients, vitamin D measurements were obtained on 206 (84.1%) during the winter months, with the remaining 39 (15.9%) having been taken during the summer months. The seasonal variation in 25-OHD levels is well established in the northern hemisphere.51 In our study, there were 8 patients with low BMD whose vitamin D deficiency was associated with elevated levels of iPTH; in 3 of these cases, alkaline phosphatase levels were also above the normative range; it is valid to suggest that osteomalacia may have contributed to low bone mass in these cases, although as a histologic diagnosis, it was not possible for us to confirm this.51 Failure to attribute a precise proportion of cases of low BMD to osteomalacia may be a valid criticism of this study; 2 previous studies of patients with disability have also referred to the difficulty of confirming osteomalacia without histology where biochemistry is suggestive,47, 49 while other similar studies fail to refer to this diagnostic dilemma at all.6, 7, 8, 42, 48

There was no correlation between BMD and 25-OHD levels; however, a weak but significant negative correlation was found between iPTH levels and BMD at the neck of femur and total proximal femur. This correlation may be explained by the seasonal variation in vitamin D affecting iPTH levels, although there were only 8 patients with iPTH levels above the normative range. Previous studies of elderly patients with stroke found a significant correlation between BMD and vitamin D levels,6, 8, 9, 10, 11, 12, 47, 52, 53 although no such relationship occurred in the multiple sclerosis population.48, 49, 50, 54 The absence of any relationship between vitamin D levels and mobility status may suggest that seasonal variation in vitamin D levels affected all patients equally, not just those who could not walk outdoors.

The independent predictive value of age and body mass on BMD is well established. However, specifically relevant to the disabled population was our finding that ambulatory status and duration of disability were also independent predictors of hip BMD. Patients' ambulatory ability was found to be significantly associated with and an independent predictor of BMD at neck of femur and total proximal femur but not at the lumbar spine. In previous studies of elderly patients with stroke, the relationship between BMD and the recovery of walking has also been explored. When a 5-point walking score was used as the assessment tool, patients' walking ability was found to correlate positively and significantly with paretic metatarsal cortical BMD and to be significantly negatively correlated with decline in BMD at the paretic femoral neck, total femur, greater trochanter, and Ward's triangle.55, 56 Those unable to walk had a decline in BMD on both the paretic and nonparetic sides, greater on the paretic side, while those who retained any ambulatory ability only lost bone mass on the paretic side.57 Timing of walking was also extremely important: even as little as a 2-month delay in return to walking was associated with significantly greater demineralization of the lower limbs, particularly on the paretic side.58, 59 The amount of weight borne through the limb, ground reaction forces, and number of steps taken would appear to be related to the extent of BMD decline at the paretic femoral neck and total proximal femur.58, 60 While we cannot prove causation between walking ability and BMD, we do not think it unreasonable to suggest that rehabilitation, focused on regaining outdoor walking ability, may have important implications for the lower-limb skeletal health of patients with newly acquired disabilities. In addition, there may be a further benefit from regaining walking ability: greater likelihood of an improvement in BMD from bisphosphonate therapy, as was shown in some studies of the spinal cord–injured population.61, 62, 63, 64, 65, 66

Duration of disability was found to be significantly negatively correlated with and an independent predictor of BMD at both hip sites but not at the lumbar spine. Such a relationship has been shown previously. Duration since stroke was found to be significantly negatively correlated with BMD at specific sites on the paretic lower limb,52, 55, 67, 68, 69 but not with lumbar spine BMD.70 Among patients with SCI, most studies examining the effect of duration of disability found a significant negative correlation with lower limb BMD,71, 72, 73, 74, 75, 76, 77, 78, 79, 80 while fewer reported no such relationship.81, 82, 83, 84, 85

Nature of disability was not found to be a predictor of BMD at any site, suggesting greater influence from the common features of disability already alluded to, including duration of disability and ambulatory status. In one of the few existing studies of BMD in people with a range of disabilities, an association was found between WHO diagnostic category and type of disability among community-dwelling women; those with neurologic disorders including SCI were more likely to have osteopenia or osteoporosis than those with musculoskeletal disorders.43 However, this cohort included women who had lifelong conditions such as cerebral palsy, suggesting that duration of disability may have confounded this relationship.

Although the expected positive correlation between testosterone or estradiol levels and BMD did not occur, among those subjects with evidence of hypogonadism, most had osteopenia or osteoporosis. However, among those with osteopenia or osteoporosis, most did not have hypogonadism, apart from the postmenopausal female group. Again, this is suggestive of the fact that in this population, other factors such as impaired mobility are more important in determining bone health. Among the participants with traumatic brain injury (n=29), there were just 2 cases of hypogonadism in spite of reported concerns in this patient population.14 Longitudinal assessment of gonadal status and BMD in a larger number of patients with traumatic brain injury may yield further information on this potential relationship.

Given the high prevalence of osteopenia and osteoporosis in younger adults with disability, it would seem prudent to address this early, to prevent fractures later in life. Intervention using physical modalities has been investigated in the spinal cord–injured population but with minimal or no improvements in BMD.75, 82, 85, 86, 87, 88, 89, 90, 91, 92, 93 Some benefit from bisphosphonate treatment has been reported among people with SCI, although these studies contained only small numbers of participants and none reported reduction in fracture rates.61, 62, 63, 64, 65, 66 There are a few studies examining the effect of bisphosphonates on the BMD of elderly patients with stroke, but none were large enough or over a long enough period to allow reliable calculation of fracture reduction rates.94, 95, 96, 97 Consequently, there is need for large multicenter trials to examine the effects of bisphosphonates and strontium ranelate on BMD in younger adults with disabilities, and in particular on fracture rates as they age.

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Conclusions 

In this population of people with disability, there was a higher prevalence of osteopenia and osteoporosis than in the general young adult population. Duration since onset of disability and ambulatory status were the most important disability-specific independent predictors of BMD at the hip. Bone health monitoring should form part of the long-term follow-up in adults with newly acquired disabilities.

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References 

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  • a Hologic Inc, 35 Crosby Dr, Bedford, MA 01730.
  • b SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL 60606.

 Supported by the National Medical Rehabilitation Trust.

 No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated.

PII: S0003-9993(09)00282-2

doi:10.1016/j.apmr.2008.09.578

Archives of Physical Medicine and Rehabilitation
Volume 90, Issue 7 , Pages 1127-1135, July 2009

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