From the Department of Neurology, Kurume (Japan) University Medical
Center (Y.S., H.K., M.K.); the Department of Neurosurgery, Ohshima Hospital,
Saga, Japan (Y.O.); the Department of Internal Medicine, Futase Social
Insurance Hospital, Iizuka, Japan (T.A.); and the First Department of Internal
Medicine, Kurume (Japan) University School of Medicine (K.O.).
Correspondence to Dr Yoshihiro Sato, Department of Neurology, Kurume University Medical Center, 155–1 Kokubumachi, Kurume 839-0863, Japan. E-mail y-sato{at}ktarn.or.jp
Methods—Sera were collected from 51 patients from the early group
and 93 patients from the long-term group. All patients had hemiplegia.
Sera were assayed for pyridinoline cross-linked carboxy-terminal
telopeptide of type I collagen (ICTP; a bone resorption marker) and
bone Gla protein (a bone formation marker). The z score
of BMD was determined in both second metacarpals.
Results—Serum ICTP concentrations (ng/mL) were higher in the
early group (15.4±4.1) than in the long-term group (6.7±4.4). Bone
Gla protein was normal or low in both groups. Multiple regression
analysis identified Barthel Index, degree of hemiplegia, and
illness duration as independent determinants of ICTP in the early
group, whereas Barthel Index, degree of hemiplegia, and serum calcium
were determinants of ICTP in the long-term group. There were
statistically significant correlations between the z
score of the hemiplegic side and age, Barthel Index, degree of
hemiplegia, illness duration, 25-hydroxyvitamin D (25-OHD), and ICTP in
the early group and between the z score and degree of
hemiplegia and 25-OHD level in the long-term group.
Conclusions—The pathogenesis of reduced BMD differed between the
early and long-term stroke groups. These results suggest that in the
early group, increased bone resorption caused by immobilization was
responsible for osteopenia on the hemiplegic side, whereas the degree
of hemiplegia and 25-OHD level were the determinants of osteopenia in
the long-term group.
The immobilization-induced osteoporosis observed in poliomyelitis or
spinal cord injury has an effect on bone modeling and remodeling
through an increased activation of remodeling loci leading to increased
osteoclastic bone resorption as evidenced by increased urinary calcium
excretion4 and a decrease of the osteoblastic
stimulus.5 There is a potential for recovery
during the active early phase of immobilization osteoporosis that may
disappear in the subsequent late inactive
phase.4 5 After 12 months, excretion of urinary
calcium indicating net bone resorption returns to
normal6 or remains
elevated.4 On the other hand, from 4% to 15% of
hip fractures occur as a late complication of stroke, with
To prevent hip fracture, the goal of this study was to determine the
bone turnover and bone mass in hemiplegic patients at different phases
of recovery from stroke. We examined the differences in biochemical
indices of bone metabolism and turnover and the changes in
bone density between patients in an earlier recovery period (<1 year,
early group) and those in a later recovery stage (illness duration
between 1 and 2 years, long-term group).
Stroke patients with illness duration between 1 and 2 years after onset
were defined as the long-term group and were selected by detailed
examination of case notes of patients with hemiplegia to match patients
of <1-year duration with respect to age, sex, severity of hemiplegia,
and Barthel Index (BI).11 The exclusion criteria
of the early group also were used in the long-term group. Ninety-three
patients with hemiplegia caused by stroke constituted the long-term
group. As the day the patient first had hemiplegia was defined as the
onset of stroke, the duration of illness was defined as the duration of
both hemiplegia and stroke in the two groups. Community-dwelling
age-matched volunteers (15 men and 17 women) served as healthy control
subjects.
In addition to BI, clinical severity of the hemiplegia was evaluated
with Brunstrom's staging classification,12 in
which a score of 1 is defined as complete paralysis of the finger, arm,
or leg, and a score of 6 represents normal strength.
With the use of a computed x-ray densitometer (CXD; Teijin
Limited),13 BMD of the second metacarpal was
measured in both hands. The CXD method measures bone density at the
middle of the second metacarpal by using a radiograph of the hand and
an aluminum step wedge as a standard (20 steps, 1 mm/step). The
computer compares the gradations of the aluminum step wedge as the
thickness of an aluminum equivalent (mm Al) with corresponding x-ray
absorption. Thus the estimated BMD is a relative scale. A total of 754
individuals, 245 men and 509 women, 50 to 90 years of age (matched for
age and sex) served as control subjects. The standard deviation (SD)
for the normal control subjects in each sex and age group was used to
calculate the z score. Because the normal values of each
individual index vary according to sex and age; we used only the
z score, which is unrelated to sex or age, to assess
patients' bone changes.
On the day of bone evaluation, a fasting blood sample was obtained in
the 51 patients from the early group, 93 long-term patients, and 32
healthy control subjects. The samples were analyzed for ionized
calcium, parathyroid hormone (intact PTH, 1 to 84), intact bone Gla
protein (BGP, a bone formation marker),14
pyridinoline cross-linked carboxy-terminal telopeptide of type I
collagen (ICTP, a bone resorption marker),15
25-hydroxyvitamin D (25-OHD),1, 25-dihydroxyvitamin D (1,
25-[OH]2D), and creatinine, as
previously described.2 3 Because in our previous
study of the older, convalescent-stage stroke patients, serum ICTP
concentration was low or normal,3 we used serum
ICTP as a bone resorption marker. On the basis of previously reported
data, serum 25-OHD concentration was defined as deficient when <10
ng/mL, insufficient when 10 to 20 ng/mL, and sufficient when >20
ng/mL.
All patients and volunteers were informed of the nature of the study
before witnessed consent from each participant. The protocol of the
study was approved by the Local Ethics Committee.
Data are presented as mean±SD. Unpaired t tests
(continuous variables) were used to assess the significance of
differences between the early and long-term groups. Categorical data
group differences were tested by x2
analyses. One-way analysis of variance and Fisher's
protected least significant difference were used to assess differences
between the two stroke groups and the control subjects. To separate the
influence of illness duration on the z scores of the
hemiplegic and intact sides in the early group, bilateral measurement
of z scores was performed in subgroups with duration of
illness of <6 months and illness duration >6 months. The measurements
were analyzed by repeated-measures analysis of
variance. Spearman's rank correlation coefficients were calculated to
determine the relation between the z score of BMD or ICTP
and each variable. Multiple regression analysis was used to
estimate the independent effects of predictor variables on the
z score of BMD for both sides and ICTP in each stroke group.
Values of P<0.05 were considered statistically
significant.
Serum Biochemical Indices and Bone Changes
Parathyroid Hormone Concentrations and Serum Levels of
25-OHD
Relations Between BMD or ICTP and Each Variable
When analyzed together in the two stroke groups, serum ionized
calcium concentrations correlated positively with ICTP
(r=0.322, P<0.0001) and negatively with BI score
(r=-0.400, P<0.0001), PTH
(r=-0.314, P=0.0002) and 1,
25-[OH]2D (r=-0.243,
P=0.0035). These results imply that immobilization-induced
hypercalcemia inhibits secondary hyperparathyroidism in hypovitaminosis
D and renal synthesis of 1, 25-[OH]2D.
Multiple Regression Analysis
In a second multiple regression analysis, age, BI, degree
of hemiplegia, calcium, and 25-OHD were selected as independent
variables and ICTP as the dependent variable. In the early
group, a significant correlation was observed between ICTP and BI,
illness duration, and degree of finger and leg paralysis. In the
long-term group, BI, degree of finger paralysis, and calcium were
related significantly to ICTP (Table 5
However, little is known about changes of bone metabolism
in immobilized stroke patients. Although our previous study
of elderly patients with long-standing hemiplegic stroke indicated that
long-standing immobilization can cause hypovitaminosis D without
compensatory hyperparathyroidism and induce normal or low skeletal
turnover,3 bone metabolism in the
early stage of stroke recovery had not been examined.
This study demonstrated that accelerated bone metabolism
with increased bone resorption occurs in patients with poststroke
hemiplegia within 1 year, as evidenced by the high serum concentrations
of ICTP and normal or low BGP. Multiple factors may be accountable for
the increased bone resorption and uncoupled high bone turnover.
Immobilization as the result of hemiplegia in the early group may be
the major cause of increased bone resorption, because physical activity
as assessed by BI and the degree of hemiplegia in the finger and leg
were independent determinants of ICTP in the early group. The illness
duration was also a determinant of ICTP in the early group, indicating
that a high rate of bone resorption may occur after early recovery from
a stroke. On the other hand, BI, degree of finger paralysis, and
calcium were the independent determinants of ICTP in the long-term
group. This result implies that a weak uncoupled state persists for >1
year after a stroke. Compensatory hyperparathyroidism in vitamin D
deficiency may not account for the high ICTP level in the early group,
because immobilization-induced hypercalcemia inhibits PTH secretion.
Consequently, PTH did not correlate with the z score of
either the hemiplegic or intact side. The hypercalcemia in the early
group compared with the long-term group resulting in severe inhibition
of 1, 25-[OH]2D production may explain
the discrepancy between the two stroke groups. Normal or low BGP may be
caused by a severe 1, 25-[OH]2D deficiency
resulting from hypercalcemia-induced inhibition of its
production; 1, 25-[OH]2D is needed to
enhance the synthesis of osteoblast-derived BGP and of matrix BGP.
Independent determinants of the z score of the
hemiplegic side were age, BI, degree of finger paralysis, illness
duration, calcium, 25-OHD, and ICTP in the early group, whereas degree
of finger paralysis and 25-OHD were determinants of the hemiplegic
z score in the long-term group. The fact that the
z score of the hemiplegic side in the two stroke groups did
not differ significantly indicates that a great deal of bone loss
occurs within 1 year. The reason for the heavy loss of bone may be
explained by the fact that seven independent determinants affected the
z score of the hemiplegic side in the early group, whereas
only two of them influenced the hemiplegic z score in the
long-term group. These differences between the two stroke groups are
important in skeletal management of stroke patients with different
illness durations. In addition to age, physical inactivity as the
result of immobilization and paralysis may be the primary cause of the
decreased hemiplegic z score. Illness duration, calcium,
25-OHD, and ICTP in the early group may be influenced by physical
activity. In the nondisabled population of age ranging from 70 to 95
years, bone remodeling may almost reach an equilibrium, resulting in a
steady rate of bone loss.19 It is noteworthy that
the older stroke patients in the early group showed higher skeletal
turnover and that age was a determinant of the z score of
both sides.
A comparison was not made between metacarpal BMD determined by CXD and
femoral neck BMD measurements performed by dual-energy x-ray
absorptiometry in disabled stroke patients. In the present study,
however, we found a positive correlation between Brunstrom's stage in
the leg and the observed BMD in the finger. Also, the degree of leg
paralysis correlated with ICTP in the early group. Our previous study
demonstrated that the degree of BMD reduction in the second metacarpal
of the hemiplegic side, as determined by the CXD method used in the
present study, correlated with the risk of hip fractures on that
side.20 Reduction in the second metacarpal BMD in
stroke patients, therefore, may reflect a decrease in hip BMD.
Although a longitudinal study would have been desirable to assess
continuous changes of bone and biochemical parameters that
occur during the early stages of a hemiplegic stroke, the present
cross-sectional study demonstrated significant differences in BMD and
in biochemical indices between the two stroke groups. During the early
recovery period after a stroke, especially within the first year, a
clinical trial of agents inhibiting bone resorption such as
bisphosphonate21 or
calcitonin22 is needed to assess whether they can
decrease bone resorption and prevent further bone loss.
Received December 30, 1997;
revision received April 24, 1998;
accepted April 24, 1998.
2.
Sato Y, Maruoka H, Oizumi K, Kikuyama M. Vitamin D
deficiency and osteopenia in the hemiplegic limbs of stroke patients.
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© 1998 American Heart Association, Inc.
Original Contributions
Increased Bone Resorption During the First Year After Stroke
Abstract
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Background and Purpose—Significant
bone mineral density (BMD) reduction occurs in stroke patients on the
hemiplegic side compared with the intact side. To elucidate the
pathogenesis of hip fractures in this population, we measured serum
markers of bone metabolism and BMD in the stroke patients
within 1 year (early group) and between 1 and 2 years after onset of
hemiplegia (long-term group).
Key Words: bone density • hemiplegia • metabolism • osteoporosis
Introduction
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Previously we
demonstrated that disuse as the result of paralysis and vitamin D
deficiency caused by malnutrition, sunlight deprivation,
and immobilization-induced hypercalcemia can cause reduced bone mineral
density (BMD) on the hemiplegic side compared with the contralateral
side in elderly patients over a period of 4 years after a
stroke.1 2 3 Because long-standing immobilization
can cause hypovitaminosis D and induce normal or low skeletal turnover
in poststroke patients, immobilization may be a major cause of this
osteopenia.3 
79%
occurring on the hemiplegic side.7 8 9 10
Subjects and Methods
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Hemiplegic patients <1 year after a stroke were eligible for
this study. Patients included individuals of either sex, 65 years of
age or older, who had been examined in one of three hospitals (Kurume
University Medical Center, Ohshima Hospital, and Futase Social
Insurance Hospital) from June 1997 to November 1997. Patients were
excluded if they had received any drug known to alter bone
metabolism such as corticosteroids,
thyroxine, anticonvulsants, estrogen, or vitamin D before and after the
onset of stroke. Other reasons for exclusion included multiple strokes,
severe physical immobility (bedridden), or severe renal (>1.5 mg/dL of
creatinine) or hepatic insufficiency. Fifty-one physically
mobile patients were enrolled in the early group.
Results
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Characteristics of Study Subjects
Descriptive characteristics of the patient population are shown in
Table 1
. No differences were observed
between the two stroke groups in terms of age, sex, BI score, degree of
hemiplegia, or type of stroke. The duration of illness was
significantly shorter in the early group than in the long-term group.
The mean illness duration of the patients from the early and long-term
groups was 118 and 439 days, respectively. Eighteen (35%) patients in
the early group and 31 (33%) patients in the long-term group were able
to ambulate without assistance, whereas the remaining patients in both
groups could ambulate independently with an assistive device but did
not require help from another person. Hemiplegia affected the dominant
side in 26 (51%) patients in the early group and 45 (48%) patients in
the long-term group. Other than hemiplegia, the following neurologic
deficits were observed in the early and long-term groups:
hemisensory impairment in 26 and 69, homonymous hemianopsia
in 3 and 7, and alternate hemiplegia in 1 and 2 patients, respectively.
Aphasia was observed in 6 and 8 patients, respectively.
View this table:
[in a new window]
Table 1. Clinical Characteristics of Stroke Patients
As previously reported,2 the serum
concentrations of 25-OHD and 1, 25-[OH]2D were
significantly lower in the two stroke groups than in the control
subjects (Table 2). Also, the mean serum
calcium levels were significantly higher in the early group than those
in the long-term group and in the control subjects, indicating
immobilization-induced hypercalcemia. There was no significant change
of PTH and creatinine levels between the three groups. The
serum ICTP concentrations of the early group patients were
significantly higher than those of the long-term group and control
subjects, whereas significant differences of these indices were not
observed between the long-term group and control subjects. BGP was
normal or low in the two stroke groups, although this difference was
not statistically significant. As previously
reported,1 the z score of the
hemiplegic side was significantly lower than on the contralateral side
in the two stroke groups and as compared with the control subjects. The
z score on the hemiplegic side in the two stroke groups did
not differ significantly but was decreased significantly compared with
control subjects.
View this table:
[in a new window]
Table 2. Serum Biochemical Parameters and
z Score of Bone Mineral Density
The mean PTH level was significantly higher in patients with
deficient levels of 25-OHD (n=70, PTH; 49.1±11.5 pg/mL) than in those
with insufficient (n=73, PTH; 29.4±16.1 pg/mL) or sufficient levels of
25-OHD (n=1, PTH; 13 pg/mL) (P<0.0001). This result
indicated vitamin D deficiency with compensatory
hyperparathyroidism.
Spearman's rank correlation coefficients between the z
score of BMD or ICTP and each variable were analyzed
together in both the early and long-term groups (Table 3). There were significant correlations
between the z score of the hemiplegic side and the
patient's age, BI score, degree of hemiplegia in the finger and leg,
illness duration, calcium, 25-OHD, and ICTP, whereas the z
score of the intact side correlated with BI score and 25-OHD. For both
sides, PTH, BGP, and creatinine did not correlate with the
z scores. ICTP correlated with age, BI score, degree of
hemiplegia of not only the finger but the leg, illness duration,
calcium, and 25-OHD.
View this table:
[in a new window]
Table 3. Correlations Between z Score or ICTP and
Each Variable
The results of multiple regression analysis, in
which age, BI, degree of hemiplegia, duration of illness, calcium,
25-OHD, and ICTP were selected as independent variables and the
z score of BMD as the dependent variable, are shown in
Table 4. On both the hemiplegic and
intact sides in the early group, age, degree of finger paralysis, and
25-OHD correlated significantly with the z score, whereas
BI, illness duration, calcium, and ICTP were significantly related to
the z score of the hemiplegic side. In the long-term group,
25-OHD correlated with the z score on both sides, whereas
the degree of finger paralysis was related to the z score of
the hemiplegic side. In the early group, left-right differences of the
z score did not show a significant change between subgroups
with an illness duration <6 months (n=16) and subgroups with an
illness duration >6 months (n=35) (P=0.77, P
value of interaction=0.51). This result suggests that the effect of
illness duration did not differ between the hemiplegic and intact
sides.
View this table:
[in a new window]
Table 4. Multiple Regression Analysis of
z Score With Age, BI, Degree of Hemiplegia, Illness
Duration, Calcium, 25-OHD, and ICTP Selected as Independent
Variables ).
View this table:
[in a new window]
Table 5. Multiple Regression Analysis of Pyridinoline
Cross-Linked Carboxy-Terminal Telopeptide of Type I Collagen With Age,
BI, Degree of Hemiplegia, Illness Duration, Calcium, and 25-OHD
Selected as Independent Variables
Discussion
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Prolonged immobilization in spinal cord injury has long been known
to result in hypercalciuria, hypercalcemia, accelerated bone
resorption, and osteoporosis.4 5 16 17 18
Acknowledgments
This study was supported by grants from the Sumitomo and
Eisai Corporations.
References
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
1.
Sato Y, Maruoka H, Honda Y, Asoh T, Fujimatsu Y,
Oizumi K. Development osteopenia in the hemiplegic finger in patients
with stroke. Eur Neurol. 1996;36:278–283.[Medline]
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-hydroxyvitamin D3 and calcium supplementation.
Stroke. 1997;28:736–739.
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