| | Osteoporosis in Adults With Meningomyelocele: An Unrecognized Problem at Rehabilitation ClinicsPresented in part to the VIII Congress of Nordic Medical Society of Paraplegia, September 4−7, 2003, Helsinki, Finland. Accepted 1 November 2005. Abstract Valtonen KM, Goksör L-Å, Jonsson O, Mellström D, Alaranta HT, Viikari-Juntura ER. Osteoporosis in adults with meningomyelocele: an unrecognized problem at rehabilitation clinics. ObjectivesTo assess the prevalence of osteoporosis and osteopenia in adults with meningomyelocele and to explore whether neurologic level, ambulatory status, and other medical problems are associated with bone mineral density (BMD). DesignA cross-sectional study, including a self-administered questionnaire and clinical assessment. SettingOutpatient referral clinic in Sweden. ParticipantsTwenty-one adults (mean age, 30y) with meningomyelocele admitted to the Young Adult Teams in Göteborg and Bo̊ras, Sweden. InterventionsNot applicable. Main Outcome MeasuresBMD in the lumbar spine and hip and forearm measured with dual x-ray absorptiometry. ResultsSeven (33%) subjects had osteoporosis in at least 1 of the measured sites. Three patients had osteopenia and 2 had osteoporosis in the lumbar spine. Among the 15 subjects whose BMD of the hip region could be reliably measured, 7 (47%) had osteoporosis in the femoral neck or trochanteric region of the hip. Subjects with other medical problems commonly occurring in meningomyelocele had lower BMD in the femoral neck and trochanteric region of the hip than subjects without such factors. Ambulation alone showed only a tendency to be associated with BMD of the femoral neck, whereas the effect of other medical risk factors on BMD of the femoral neck was stronger among the nonambulators than the ambulators. ConclusionsOur results show that osteoporosis is a medical problem to be considered when treating and rehabilitating patients with meningomyelocele.
MENINGOMYELOCELE IS A CONGENITAL malformation of the neural tube in which the spinal cord and nerve roots herniate through a defect in the vertebral arches. The condition results in varying sensory and motor deficits below the affected neurologic level of the lesion, which most often is located in the lumbosacral region. In addition to muscle weakness and sensory loss, associated problems include impaired bladder and bowel control, and hydrocephalus, the latter being seen in more than 80% of meningomyelocele cases.1, 2 The functional ability and ambulatory status of these patients can vary considerably, depending mainly on the neurologic level of the injury. Studies have shown that only about 30% to 50% of people with meningomyelocele are functional ambulators and 30% to 40% rely mainly or entirely on a wheelchair for mobility.1, 3 Furthermore, some studies4 have shown deterioration of the neurologic level of the injury and walking ability in adolescents and young adults.
Osteoporosis is a disease characterized by reduction of total bone mass and microarchitectural deterioration of bone tissue. These changes are associated with an increased rate of fractures. Risk factors for osteoporosis include age, female sex, parental history of hip fracture, and physical inactivity.5 It can be assumed that patients with meningomyelocele are at potential risk to develop osteoporosis at a younger age because of impaired walking ability and subsequent low physical loading of the lower limbs. Furthermore, because of neurogenic bladder dysfunction, these patients are more prone to develop renal failure, which is a known risk factor for osteoporosis.5 Urinary diversion surgery, in which part of the ileum is resected to form a reservoir, is a common method for treating neurogenic bladder, which may cause acidosis and osteoporosis.6 Epilepsy is also fairly common in this patient group and medication for epilepsy can increase the risk for osteoporosis.7
Although several studies have shown that people with meningomyelocele are prone to pathologic fractures, studies of bone mineral density (BMD) in meningomyelocele are almost nonexistent.8, 9 Healing of osteoporotic fractures may take time. Considering the effects of prolonged immobilization on independence in daily activities and quality of life, there should be no disagreement that all efforts are necessary to prevent these fractures. Furthermore, 1 osteoporotic fracture may lead to a vicious cycle of immobilization, decreased bone density, and repeated fractures.
In nondisabled children, BMD increases with age until it peaks in early adulthood. This has been shown to be true also in children with meningomyelocele.8, 9 However, it has been reported that BMD in children and young adults with meningomyelocele falls 1 to 2 standard deviations (SDs) below that of the normative population.8, 10 Previous data also suggest that both neurologic level and ambulatory status affect BMD in children with meningomyelocele.9 Comparisons between meningomyelocele children with bladder augmentation and never-augmented meningomyelocele children have shown no significant difference in BMD.10, 11
Our purpose in this study was to assess the prevalence of osteoporosis and osteopenia in adults with meningomyelocele. Moreover, we wanted to explore whether BMD and osteoporosis are associated with neurologic level, ambulatory status, and medical problems associated with meningomyelocele, such as urinary diversion, renal insufficiency, and medication for epilepsy. We also explored whether ambulatory status is associated with BMD in the forearm. Our hypothesis was that ambulators and subjects with better motor capacity in the lower extremities would show higher BMD in the hip and lumbar spine when compared with nonambulators and subjects with less motor capacity in the lower extremities.
Methods  Clinical Assessment A physician (KMV, ERV-J) and a physical therapist examined all subjects on the day BMD was measured. We followed the American Spinal Injury Association’s (ASIA) International Standards for Neurological Classification of Spinal Cord Injury to determine the neurologic level of the injury.12 The ASIA classification is not a standard method for assessing the neurologic level in meningomyelocele, but it was successfully used in a study of men with meningomyelocele.13 The motor score, which was used to characterize the neurologic level of the injury, was assessed separately for the upper (0−50) and lower (0−50) extremities to make up variables suitable for testing our hypotheses. The median of the lower-extremity motor score was used to categorize the subjects into 2 groups for analyses: subjects with full motor capacity in the upper extremities (upper-extremity motor score of 50), and subjects with impairments in upper-extremity motor function (upper-extremity motor score <50). We classified the present ambulatory status into 4 categories according to Hoffer et al.14 Community ambulators walked with or without aids and never used a wheelchair. Household ambulators walked inside, but used a wheelchair on longer ambulations. Nonfunctional ambulators walked only in therapy situations, and nonambulators used a wheelchair for all ambulations. For statistical analyses, we further classified the subjects into 2 categories, ambulators (community and household ambulators) and nonambulators (nonfunctional ambulators and nonambulators). We also considered the subjects’ history of ambulation by assessing their ambulatory status according to Hoffer14 at the age of 10 years. Only 5 had a changed ambulatory category since the age of 10 and therefore we used the current ambulatory status in our analyses. The other medical risk factors for osteoporosis that we considered in our analyses were urinary diversion surgery, in which part of the ileum had been resected to serve as a urinary reservoir, renal insufficiency based on chrome ethylenedinitrilo tetraacetic acid (EDTA) clearance value, use of antiepileptic drugs, and oral cortisone treatment for more than 3 months. We included also 1 subject with Down syndrome in addition to meningomyelocele in the group of subjects with medical risk factors, because osteoporosis has been shown to be associated with this disease.15 Information about previous fractures and medications was obtained from the questionnaire. We did short interviews with the subjects to complete the data received from the questionnaire. Bladder regime, urinary diversion operations, and chrome EDTA clearance values were obtained from the medical files, with the patients’ approval. To assess bone mineral metabolism, as well as renal function, venous blood samples were obtained for analyses of the levels of osteocalcin, parathyroid hormone (PTH), 25-hydroxyvitamin D (25[OH]D3), total calcium, ionized calcium, standard bicarbonate, cystatin C, and bone-specific alkaline phosphatase. Serum calcium, ionized calcium, and standard bicarbonate were assessed with standard methods. Serum osteocalcin was assessed by radioimmunoassay, PTH with immunochemiluminometry, and cystatin C with turbidimetry. Blood samples were obtained from 16 subjects. Measurement of BMD BMD was measured with dual-energy x-ray absorptiometry.a Bone density of the lumbar spine in the L1-4 vertebrae was obtained for 19 patients. We could not measure the lumbar spine of 2 subjects who had prior surgical treatment of scoliosis with Harrington rods. To check the reliability of the BMD measurement of the lumbar spine, a radiologist (L-ÅG) assessed the existence of vertebral arch defects in each one of L1-4 vertebrae. For this purpose, we used plain radiographs from earlier renography examinations and lumbar spine examinations (eg, for scoliosis). The radiologist then measured the width of the vertebral arch defect in millimeters. Because a defect in the L1 vertebra was rare, this level was used in the analyses. Furthermore, the values for the L1 vertebra showed high correlation with the total lumbar spine (Spearman ρ=.76, P=.002). The subjects with defects in all vertebrae were excluded from the analyses of the lumbar spine. BMD of the left hip was measured in 19 subjects and of the right hip in 13 subjects. Because of technical problems in positioning the subjects, 1 subject could only be measured on the right side and the hips of 1 subject could not be measured at all. The radiologist who checked the reliability of the BMD measurement of the lumbar spine also determined deformities of the hips from the graphs obtained during the absorptiometry. Subjects with hip deformities in both hips were excluded from the analyses of the BMD of the hip. In the analyses, we mainly used values of the left hip, but for those whose right hip was less deformed than the left hip, we used the BMD value of the right hip. The BMD of the forearm was included in the study protocol from the fifth subject onward and this measurement was obtained for 13 patients. Four subjects could not be measured in the forearm because of technical problems in the positioning of the subjects. We used the World Health Organization’s (WHO) diagnostic criteria for osteoporosis, which establishes a diagnosis of osteoporosis when the T score for BMD falls −2.5 SDs or more below that for the young adult mean of the reference population. When the value for BMD falls between −1.0 and −2.5 SDs below the young adult mean, the bone is defined as osteopenic. A North American reference population provided by the manufacturer was used. The study was approved by the Ethics Committee of Göteborg University. Analysis of Results The results are given as T scores for BMD at the measured locations. A T score is the number of SDs the BMD value is above or below that of the young adult mean of the reference population. A z score is the number of SDs the BMD value is above or below that of the age-matched mean of the reference population. We looked at both T and z scores, but because our study population was relatively young, there were no major differences between the T score and z score. Furthermore, using the T score is consistent with WHO’s diagnostic criteria. We applied a logistic regression model to assess risk of osteoporosis in at least 1 of the measured sites. Because of the limited number of subjects, only univariate models could be calculated. Other analyses were made using absolute BMD values (in g/cm2) as a continuous variable as the outcome. We used general linear models (analysis of variance) to study the effects of ambulatory status and medical risk factors on BMD. The interaction between ambulatory status and medical risk factors was included into the models. The models were fitted using the SPSS statistical software.b Statistical significance was defined as P less than .05. Results Subject Characteristics Patient characteristics are shown in table 2. According to the ASIA classification, the neurologic level was cervical in 1, cervicothoracic in 1, thoracic in 4, thoracolumbar in 3, and lumbar in 11 patients. Ten subjects had complete injury (ASIA Impairment Scale [AIS] grade A). After dichotomization of the study group by ambulatory status, there were 8 ambulators and 13 nonambulators. Seventeen subjects had hydrocephalus and 4 had epilepsy. One subject had used oral cortisone treatment for more than 3 months. Eight of 21 subjects had a history of at least 1 fracture, with the frequency ranging from 1 to 4 fractures. The majority of these fractures were in the lower extremities, with only 1 in the upper extremity. At follow-up, 2 patients micturated by normal voiding or straining. Eleven subjects performed clean intermittent catheterization (CIC) of their natural bladder via urethra and 2 via suprapubic vesicostomy. One patient performed CIC via urethra of a bladder augmented by ileocystoplasty. Another patient had a permanent suprapubic catheter. Three patients were diverted via a Bricker conduit and 1 via a continent cutaneous ileal reservoir (Kock reservoir). Based on the age-specific chrome-EDTA clearance reference values, 3 subjects showed renal insufficiency. Laboratory Assessment The 25(OH)D3 levels as a whole were on the lower end of the reference range and 1 subject was below the lower reference value. In 1 subject, 25(OH)D3 was increased due to oral vitamin D supplementation. Total serum calcium and ionized calcium levels, as well as standard bicarbonate and cystatin C levels, were within the reference range in all subjects. Eight subjects showed high osteocalcin values that were most often explained by the young age of the subject. In 1 case, high osteocalcin value was associated with high bone-specific alkaline phosphatase and high PTH. Two other subjects showed high PTH values as the sole finding and the subject with low vitamin D level also showed an increased bone-specific alkaline phosphatase value. Prevalence of Osteoporotic Values The T scores for BMD in the measured locations are shown in figure 1. Because the L1 vertebra was nearly always free of bone defect, we report the BMD of the L1 vertebra instead of that of the lower vertebrae or the total lumbar spine. After the exclusion of the 6 subjects with bone defect in the L1 vertebra, the bone density of the lumbar spine was osteopenic in 3 of 14 (21%) subjects and osteoporotic in 2 (14%) subjects. After the exclusion of 5 subjects with hip deformities, 9 (60%) subjects had osteopenia and none had osteoporosis in the total hip, but when the BMD in the femoral neck and trochanteric region of the hip was scrutinized, 7 (47%) subjects could be considered to have osteoporosis in either site. The bone density of the forearm was nearly always within normative limits and only 3 (23%) patients showed osteopenia and no one had osteoporosis. Seven of the total of 21 (33%) subjects had osteoporosis in at least 1 of the measured sites. Potential Risk Factors for Osteoporosis Sex, chronologic age, body mass index (BMI), lower-extremity motor score, upper-extremity motor score, or ambulatory status had no effect on the risk for osteoporosis in at least 1 of the measured sites. Odds ratio for all medical risk factors combined was 9.60 (confidence interval, 0.88−105.17). The risk of osteoporosis in at least 1 of the measured sites did not differ between those with and without previous fractures. The absolute values of BMD according to ambulatory status and other medical risk factors for osteoporosis are shown in figure 2. When the effect of ambulatory status on BMD was studied without considering the possible effect of other medical risk factors, the ambulators showed higher BMD values in the forearm than did the nonambulators (F=5.2, P=.043). A similar tendency was seen in the femoral neck, but this difference was not statistically significant (F=3.3, P=.094). Ambulatory status alone had no effect on BMD in the trochanteric region of the hip, total hip, or lumbar spine. Twelve subjects had 1 or more medical risk factors for osteoporosis (urinary diversion with ileum resection, renal insufficiency, medication for epilepsy, oral corticosteroid treatment, diagnosis of Down syndrome). Among 13 nonambulators, 7 had at least 1 other medical risk factor for osteoporosis and among 8 ambulators, 5 had at least 1 other medical risk factor. When both ambulatory status and other medical risk factors for osteoporosis were studied in the same model, ambulatory status alone no longer had an effect on BMD (table 3). The presence of other medical risk factors, in contrast, had a significant effect on the BMD of the femoral neck and trochanteric region of the hip so that subjects with at least 1 other medical risk factor showed lower BMD at these locations than did the others. A similar tendency was seen in the BMD of the total hip, but this difference was not statistically significant. The presence of other medical risk factors had no effect on the BMD of the L1 vertebra or the forearm (see fig 2, table 3). The effect of medical risk factors on BMD of the femoral neck, trochanteric region of the hip, and total hip seemed to be stronger in nonambulators than in ambulators (see fig 2). This interaction was statistically significant for the femoral neck, but not for the total hip or trochanteric region of the hip. No such interaction was seen in the BMD values for the L1 vertebra or the forearm (see table 3). Discussion Our results indicate that osteopenia and osteoporosis are more common among adults with meningomyelocele than in the normative population. Given our original hypothesis that this is mainly due to physical inactivity, it was somewhat surprising that there was only a trend for lower BMD at femoral neck among nonambulators compared with ambulators. On the contrary, the presence of other medical risk factors was an independent risk factor for lower BMD at the femoral neck and trochanteric region of the hip. Furthermore, interactions between ambulatory status and medical risk factors indicated that the effects of medical risk factors were stronger among nonambulators than among ambulators. In previous studies of children with meningomyelocele, stronger associations have been found between ambulatory status and BMD.8, 9 Rosenstein et al9 found that both neurologic level and ambulatory status had a significant effect on bone density at the distal radius, tibia, and first metatarsal in children with meningomyelocele. We found no significant correlation between the neurologic level and BMD. This suggests that the actual loading of the lower extremities is a predictor of BMD rather than the potential for ambulation in the form of neurologic level of injury or motor score of the lower extremities. This concept, however, is not fully supported by our results since the effect of ambulation turned out to be weaker than we had expected. The fact that there was no difference in the BMD in the lumbar spine between the ambulators and nonambulators is in line with the findings of previous studies among subjects with traumatic spinal cord injury (SCI). It has been shown that there is a clear dissociation of BMD between the lumbar spine and the hip after an acute phase of paraplegia.16 Our results suggest that besides low degree or lack of loading of the extremities, osteoporosis can be caused by neurogenic and metabolic mechanisms in this patient group. Lower BMD values in the forearm reported in some previous studies could be explained with such mechanisms.8 On the other hand, subjects with meningomyelocele load the upper extremities through the use of crutches or wheelchair, the effect of which could be an increase in BMD. In our study, bone density in the forearm was almost always within normative limits and only few patients had osteopenia and none had osteoporosis. In accord with previous studies, we found that BMD tended to be lower in the forearm among the nonambulators than among the ambulators. A previous study10 found that subjects with bladder augmentation are prone to develop metabolic acidosis. Quan et al8 found that subjects with meningomyelocele may have hypercalciuria related to immobilization. In our study, all subjects showed normative standard bicarbonate and serum calcium values. Because hypercalciuria is closely related to ambulatory status and therefore cannot be studied reliably as an independent predictor for osteoporosis in this patient group, we decided not to collect 24-hour urine samples.8 In nondisabled subjects, a low BMI is a known risk factor for osteoporosis.5 In our study, however, there was no association between BMI and BMD. This is probably because in subjects with meningomyelocele, overweight is a common problem and most often a consequence of impairments in functioning.17 In our study, those with higher BMI were more often nonambulators and the effect of BMI on BMD could therefore not be studied independently of ambulation. Moreover, the assessment of BMI can be unreliable in subjects with meningomyelocele because of altered proportions in body dimensions and eventual contractures in the lower extremities. Impairments in ambulation and functioning may cause subjects with meningomyelocele to spend more time inside and become even more easily institutionalized. This may result in diminished exposure to sunshine, which in turn may lead to reduced production of vitamin D in the body and disturbance of calcium metabolism. In our study population, nearly all subjects showed vitamin D levels that were in the lower end of the reference range. Treatment with both calcium and vitamin D has been shown to be cost effective in able-bodied adults.18 Although there are no studies of the effect of supplementary calcium and vitamin D on BMD in people with meningomyelocele, we suggest adding them to the medication of subjects with meningomyelocele and osteoporosis. On the other hand, constipation is a frequent problem in these patients and supplementary calcium may worsen it. This must be considered and laxatives should be added into treatment when necessary. There are no studies concerning the treatment of osteoporosis in this patient group. However, previous studies have shown promising results of bisphosphonates in the treatment of osteoporosis in patients with traumatic SCI or cerebral palsy.19, 20, 21 Presumably, similar effects could be seen in patients with meningomyelocele. Calcitonin has been shown to be more effective in the prevention of vertebral fractures than in the prevention of hip fractures in osteoporosis.22 Therefore, it may not be the first treatment option in this patient group, in which dissociated osteoporosis is commonly seen. A recombinant human parathyroid hormone teriparatide has been shown clinically to improve BMD in postmenopausal women and men.23 There are no studies concerning the effects of teriparatide in people with functional impairments. In animal studies, however, there have been promising results in preventing immobilization-related bone loss.24 Hydrochlorothiazide has been shown to increase BMD in nonmeningomyelocele patients with hypercalciuria.25 Because immobilization-related hypercalciuria is commonly seen in nonambulatory patients with meningomyelocele, hydrochlorothiazide could be a potential treatment option for osteoporosis in this patient group. In 1 study, use of hydrochlorothiazide for 1 year did not affect BMD, but it reduced urinary calcium excretion in nonambulatory children with meningomyelocele.26 The effect of standing on bone density is not clear.27, 28 Previous studies have shown promising results of regular functional electric stimulation–assisted training, but this is often nearly impossible to carry out in daily life.29 The prevention of fractures should be among the major goals in the rehabilitation of people with meningomyelocele. The assessment of BMD is worthwhile in patients with risk factors for osteoporosis, because low BMD is a known risk factor for fractures.5 The fact that we did not find an association between BMD and history of fractures was probably attributable to our small sample size and the retrospective nature of the information concerning fractures. The assessment of BMD in subjects with meningomyelocele can be problematic. Some feel uncomfortable lying on their back and for some it is impossible to straighten their legs because of contractures. There may also be difficulties in assessing bone density because of deformed hips, heterotopic ossification, sclerotic vertebrae, and sequelae of operations. Most of these changes cause overestimation of bone density. Overestimation may also result from subjects being overweight, which is frequently the case in subjects with meningomyelocele.17 On the other hand, the defect in itself can cause underestimation of BMD because there is lack of bone in the vertebral arch. The measurement of BMD in the heel with quantitative ultrasound would not solve the problem because the heels of these patients are also often deformed. Our study population was fairly small, so few results could be ascertained with statistical significance. The low participation rate could have been because our subjects had already had numerous contacts with various health professionals. Some might not want to know whether they have osteoporosis, and that can be seen as one of their coping strategies. One could also claim that the number of functional impairments and the prevalence of other comorbidities were higher among the nonparticipants than among the participants. If so, BMD may be even lower in meningomyelocele than our results suggest. However, our study population was very representative of the source population with regard to age, sex, and ambulatory status and the results therefore have generalizability with regard to other Young Adult Team patient populations. Conclusions To our knowledge, this is the first study on bone density in adults with meningomyelocele. Our results show that osteoporosis is a medical problem that must be considered when treating and rehabilitating patients with meningomyelocele. More studies, especially longitudinal studies, are needed to learn about the prognosis of osteopenia and osteoporosis in subjects with meningomyelocele and about the effect of different treatment regimens.
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Acknowledgments We acknowledge Ingrid Berglind Nordh, RPT, for carrying out the muscle testing. We thank Marie-Louise Lindqvist, RN, for carrying out the bone density measurements. We are indebted to Ragnhild Björklund, MD, for her valuable contribution in the recruitment of patients for this study. Lauren Lissner Östlund, PhD, is acknowledged for valuable comments on the article. References 1.
1
Hunt GM
, Oakeshott P
.
Outcome in people with spina bifida at age 35
(prospective community based cohort study)
.
BMJ
. 2003;326:1365–1366
.
2.
2
Tomlinson P
, Sugarman D
.
Complications with shunts in adults with spina bifida
.
BMJ
. 1995;311:286–287
.
3.
3
McDonnell GV
, McCann JP
.
Issues of medical management in adults with spina bifida
.
Childs Nerv Syst
. 2000;16:222–227
.
MEDLINE |
CrossRef
4.
4
Bartonek Å
, Saraste H
, Samuelsson L
, Skoog M
.
Ambulation in patients with myelomeningocele
(a 12-year follow-up)
.
J Pediatr Orthop
. 1999;19:202–206
.
MEDLINE |
CrossRef
5.
5
Kanis JA
.
Diagnosis of osteoporosis and assessment of fracture risk
.
Lancet
. 2002;359:1929–1936
.
Abstract | Full Text |
Full-Text PDF (114 KB)
|
CrossRef
6.
6
Abes M
, Sarihan H
, Madenci E
.
Evaluation of bone mineral density with dual x-ray absorptiometry for osteoporosis in children with bladder augmentation
.
J Pediatr Surg
. 2003;38:230–232
.
Abstract | Full Text |
Full-Text PDF (108 KB)
|
CrossRef
7.
7
Farhat G
, Yamout B
, Mikati MA
, Demirjian S
, Sawaya R
, El-Hajj Fuleihan G
.
Effect of antiepileptic drugs on bone density in ambulatory patients
.
Neurology
. 2002;58:1348–1353
.
MEDLINE 8.
8
Quan A
, Adams R
, Ekmark E
, Baum M
.
Bone mineral density in children with myelomeningocele
.
Pediatrics
. 1998;102:E34
.
9.
9
Rosenstein BD
, Greene WB
, Herrington RT
, Blum AS
.
Bone density in myelomeningocele
(the effects of ambulatory status and other factors)
.
Dev Med Child Neurol
. 1987;29:486–494
.
MEDLINE 10.
10
Koch MO
, McDougal WS
, Hall MC
, Hill DE
, Braren HV
, Donofrio MN
.
Long-term metabolic effects of urinary diversion
(a comparison of myelomeningocele patients managed by clean intermittent catheterization and urinary diversion)
.
J Urol
. 1992;147:1343–1347
.
MEDLINE 11.
11
Mingin GC
, Nguyen HT
, Mathias RS
, Shepherd JA
, Glidden D
, Baskin LS
.
Growth and metabolic consequences of bladder augmentation in children with myelomeningocele and bladder exstrophy
.
Pediatrics
. 2002;110:1193–1198
.
12.
12
Maynard FM
, Bracken MB
, Creasey G
, et al.
American Spinal Injury Association
International Standards for Neurological and Functional Classification of Spinal Cord Injury
.
Spinal Cord
. 1997;35:266–274
.
MEDLINE 13.
13
Hultling C
, Levi R
, Amark SP
, Sjöblom P
.
Semen retrieval and analysis in men with myelomeningocele
.
Dev Med Child Neurol
. 2000;42:681–684
.
MEDLINE |
CrossRef
14.
14
Hoffer MM
, Feiwell E
, Perry R
, Perry J
, Bonnett C
.
Functional ambulation in patients with myelomeningocele
.
J Bone Joint Surg Am
. 1973;55:137–148
.
MEDLINE 15.
15
Lazner F
, Gowen M
, Pavasovic D
, Kola I
.
Osteopetrosis and osteoporosis
(two sides of the same coin)
.
Hum Mol Genet
. 1999;8:1839–1846
.
MEDLINE |
CrossRef
16.
16
Kannisto M
, Alaranta H
, Merikanto J
, Kröger H
, Kärkkäinen J
.
Bone mineral status after pediatric spinal cord injury
.
Spinal Cord
. 1998;36:641–646
.
MEDLINE 17.
17
Fiore P
, Picco P
, Castagnola E
, et al.
Nutritional survey of children and adolescents with myelomeningocele (MMC)
(overweight associated with reduced energy intake)
.
Eur J Pediatr Surg
. 1998;8(Suppl 1):34–36
.
CrossRef
18.
18
Boonen S
, Rizzoli R
, Meunier PJ
, et al.
The need for clinical guidance in the use of calcium and vitamin D in the management of osteoporosis
(a consensus report)
.
Osteoporos Int
. 2004;15:511–519
.
19.
19
Henderson RC
, Lark RK
, Kecskemethy HH
, Miller F
, Harcke HT
, Bachrach SJ
.
Bisphosphonates to treat osteopenia in children with quadriplegic cerebral palsy
(a randomized, placebo-controlled clinical trial)
.
J Pediatr
. 2002;141:644–651
.
Abstract | Full Text |
Full-Text PDF (109 KB)
|
CrossRef
20.
20
Sniger W
, Garshick E
.
Alendronate increases bone density in chronic spinal cord injury
(a case report)
.
Arch Phys Med Rehabil
. 2002;83:139–140
.
Abstract | Full Text |
Full-Text PDF (28 KB)
|
CrossRef
21.
21
Zehnder Y
, Risi S
, Michel D
, et al.
Prevention of bone loss in paraplegics over 2 years with alendronate
.
J Bone Miner Res
. 2004;19:1067–1074
.
MEDLINE |
CrossRef
22.
22
Mehta NM
, Malootian A
, Gilligan JP
.
Calcitonin for osteoporosis and bone pain
.
Curr Pharm Des
. 2003;9:2659–2676
.
MEDLINE |
CrossRef
23.
23
Quattrocchi E
, Kourlas H
.
Teriparatide
(a review)
.
Clin Ther
. 2004;26:841–854
.
MEDLINE |
CrossRef
24.
24
Sakai A
, Sakata T
, Ikeda S
, et al.
Intermittent administration of human parathyroid hormone (1-34) prevents immobilization-related bone loss by regulating bone marrow capacity for bone cells in ddY mice
.
J Bone Miner Res
. 1999;14:1691–1699
.
MEDLINE |
CrossRef
25.
25
Legroux-Gerot I
, Catanzariti L
, Marchandise X
, Duquesnoy B
, Cortet B
.
Bone mineral density changes in hypercalciuretic osteoporotic men treated with thiazide diuretics
.
Joint Bone Spine
. 2004;71:51–55
.
CrossRef
26.
26
Quan A
, Adams R
, Ekmark E
, Baum M
.
Bone mineral density in children with myelomeningocele
(effect of hydrochlorothiazide)
.
Pediatr Nephrol
. 2003;18:929–933
.
CrossRef
27.
27
Caulton JM
, Ward KA
, Alsop CW
, Dunn G
, Adams JE
, Mughal MZ
.
A randomised controlled trial of standing programme on bone mineral density in non-ambulant children with cerebral palsy
.
Arch Dis Child
. 2004;89:131–135
.
CrossRef
28.
28
Kunkel CF
, Scremin AM
, Eisenberg B
, Garcia JF
, Roberts S
, Martinez S
.
Effect of “standing” on spasticity, contracture, and osteoporosis in paralyzed males
.
Arch Phys Med Rehabil
. 1993;74:73–78
.
MEDLINE 29.
29
Belanger M
, Stein RB
, Wheeler GD
, Gordon T
, Leduc B
.
Electrical stimulation
(can it increase muscle strength and reverse osteopenia in spinal cord individuals?)
.
Arch Phys Med Rehabil
. 2000;81:1090–1098
.
Abstract | Full Text |
Full-Text PDF (157 KB)
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a Department of Rehabilitation Medicine, Sahlgrenska Academy, Göteborg University, Göteborg, Sweden b Department of Geriatric Medicine, Sahlgrenska Academy, Göteborg University, Göteborg, Sweden c Department of Rehabilitation Medicine, Sahlgrenska University Hospital, Göteborg, Sweden d Department of Radiology, Sahlgrenska University Hospital, Göteborg, Sweden e Department of Urology, Sahlgrenska University Hospital, Göteborg, Sweden f Käpylä Rehabilitation Centre, Helsinki, Finland  Reprint requests to Kirsi M. Valtonen, MD, Härkävaljakontie 5 B 1, FI-00750 Helsinki, Finland. Reprints are not available from the authors.
No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated. PII: S0003-9993(05)01382-1 doi:10.1016/j.apmr.2005.11.004 © 2006 American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation. Published by Elsevier Inc. All rights reserved. | |
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