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(Stroke. 1996;27:2183-2187.)
© 1996 American Heart Association, Inc.

Articles

Vitamin D Deficiency and Osteopenia in the Hemiplegic Limbs of Stroke Patients

Yoshihiro Sato, MD; Hiroshi Maruoka, MD; Kotaro Oizumi, MD Munetsugu Kikuyama, PhD

the Department of Neurology, Futase Social Insurance Hospital, Iizuka (Y.S., H.M.); the First Department of Internal Medicine, Kurume University School of Medicine, Kurume (K.O.); and the Diagnostic Equipment Department, Teijin Limited, Tokyo (M.K.), Japan.

Correspondence to Yoshihiro Sato, MD, Department of Neurology, Futase Social Insurance Hospital, 1243-1 Ikawa, Iizuka 820, Japan. E-mail y-sato@kurume.ktarn.or.jp.

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Background and Purpose Little is known about bone changes in hemiplegic stroke patients. We evaluated the vitamin D status and bone changes on the hemiplegic and intact sides of stroke patients.

Methods Sera were collected from 87 hemiplegic stroke patients (42 outpatients and 45 inpatients) and from 28 control subjects. The sera were assayed for 25-hydroxyvitamin D (25-OHD). Bone density was measured bilaterally from radiographs of the hands. Diet and sunlight exposure were assessed for all subjects.

Results Serum 25-OHD concentrations were lower in patients (9.1±4.9 ng/mL for outpatients, 5.9±4.1 ng/mL for inpatients) than in control subjects (21.6±3.1 ng/mL). The difference in serum 25-OHD between the two patient groups also was statistically significant. The patients' microdensitometric scores for osteopenia were higher on the hemiplegic side than on the nonhemiplegic side. The microdensitometric scores and their side-to-side differences in patients correlated negatively with the serum 25-OHD concentration and positively with the degree of paralysis. Dietary intake of vitamin D was below the recommended level in 72% of the patients, and 89% of the patients were considered sunlight-deprived.

Conclusions Bone mass was reduced significantly on the hemiplegic side in the stroke patients, which might increase the risk of hip fracture. Vitamin D deficiency and disuse are the probable causes of osteopenia in this population. The hypovitaminosis D might be corrected readily by routine use of vitamin D supplements.

Key Words: complications • hemiplegia • osteoporosis • vitamin D deficiency

	Introduction

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From 4% to 15% of hip fractures occur as a late complication of stroke, with at least 79% occurring on the hemiplegic side.^{1 2 3 4 5} This has been ascribed to disuse osteoporosis on the hemiplegic side and gait instability in hemiplegic patients.⁶ However, the pathogenesis of the bone abnormalities in hemiplegic limbs has not been fully determined.^{7 8} We previously examined the MD indices in the second metacarpal bone of hemiplegic limbs and demonstrated a decrease in bone mass on the hemiplegic side compared with the contralateral side, according to the degree of the palsy.⁹ In the present study, we examined the role of vitamin D in these events.

	Subjects and Methods

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From November 1995 through January 1996 (the winter season in Japan), 118 patients with hemiplegia of more than 1 month in duration due to stroke were seen at the Futase Social Insurance Hospital, where the patient population consists of the neurologically disabled. Of these, 31 patients were excluded because of associated shoulder-hand syndrome (n=12), multiple strokes (n=3), or immobility that precluded radiography of the hands (n=16). Thus, 87 patients were enrolled in this study (42 outpatients and 45 inpatients). The outpatients had been out of the hospital for 2 years or more. A diagnosis of stroke was made on the basis of clinical evaluation, as well as CT, in both the acute and chronic phases. The strokes were classified according to the Classification of Cerebrovascular Diseases III of the National Institute of Neurological Disorders and Stroke.¹⁰ No patients received physical therapy for at least 2 months before the study. Fifteen patients had diabetes mellitus, which is known to result in osteopenia. None of the patients had received any drugs known to alter bone metabolism, such as corticosteroids, thyroxine, anticonvulsants, or vitamin D. None of the patients had a history of hip fracture.

In addition to the BI,¹¹ the clinical severity of the hemiplegia was evaluated using the long-term score of the Scandinavian Stroke Scale,¹² in which a score of 1 is defined as paralysis of the hand, arm, or leg and a score of 4 for the hand and a score of 5 for the upper or lower limb represent normal strength.

For the determination of bone changes, plain radiographs of both hands were taken with an aluminum step scale and analyzed with an MD (Teijin Ltd). The optical density at the center of the second metacarpal bone was read according to the method of Inoue et al¹³ (Figure). The bone width (D), bone marrow width (d), cortical width on the radial side (d1), cortical width on the ulnar side (d2), density at the center of the bone marrow (GSmin), peak density on the radial side (GSmax1), and peak density on the ulnar side (GSmax2) were measured. The cross section of the metacarpal bone was assumed to be a circle, and the cortical bone width (d1 and d2) was classified into three grades (3/3, 2/3, and 1/3). The optical densities of d1 and d2 also were graded (1, 1/2, and 0). Nine bone models were prepared by drawing the metacarpal bone pattern according to the above parameters. The measurements were used to determine six indices: (1) the metacarpal index (MCI), (2) the bone marrow width index (d), (3) the center density index (GSmin), (4) the side density index (Gsmax; mean of the GSmax1 and GSmax2), (5) the index corresponding to the mineral content of the bone (GS/D; GS=the integrated value of the density area), and (6) the densitometer pattern index (1 to 9). Each index was plotted against age separately for 388 men and 315 women, for a total of 703 age-matched and sex-matched control subjects aged 30 to 90 years. Among the patients, the changes in the indices were defined as follows: changes of <1 SD from the appropriate regression line for healthy control subjects were defined as a change of 1 point; 1 to 2 SD as 2 points; and >2 SD as 3 points. From the sum of these scores for the six indices, the degree of bone loss was expressed as the MD score. The severity of the bone changes was classified according to the MD score: 0 to 3, normal; 4 to 6, slight change; 7 to 9, moderate change; and 10, severe change. To confirm the similarity of the MD indices on right and left sides in healthy individuals, a total of 28 age-matched volunteers (14 men and 14 women) served as control subjects. Since the normal values of each individual index vary according to the sex and age of the patients, and since the number of patients enrolled in this study was small, we used only the MD scores (which are unrelated to sex or age) to compare the hemiplegic side to the contralateral side (in the patients) and the two sides (in the control subjects).

View larger version (39K): [in this window] [in a new window]   Figure 1. Schematic representation of the MD method. Ranking the bone cortex width (d1+d2) and the bone density, nine bone models (1 through 9) were determined. Each index was ranked by severity with a score of 0, 1, 2, or 3. From the sum of the scores of these six indices, the MD score was calculated. MCI (metacarpal index) is the ratio of the combined thickness of the cortical bone (d1+d2) to the bone width (D). The density index at the center (GSmin) and the side (GSmax; the mean of GSmax1 and GSmax2) also were determined. GS denotes the integrated value of the density area.

The patients and control subjects completed a questionnaire concerning their diet and sunlight exposure. The mean weekly dietary vitamin D intake was calculated for each individual.

On the day of each patient's bone evaluation, a fasting blood sample was obtained. During the same period (November 1995 through January 1996), blood was drawn from the 28 control subjects. The serum samples from the 87 patients and 28 controls were analyzed for 25-OHD and 1,25-[OH]₂D. The serum 25-OHD concentration was determined with a competitive protein-binding assay and that of 1,25-[OH]₂D with a radioreceptor assay using calf thymus receptor (Nichols Institute Diagnostics).

A serum 25-OHD concentration of <10 ng/mL was considered deficient, a concentration of between 10 ng/mL and 20 ng/mL was categorized as insufficient, and a concentration of >20 ng/mL was considered sufficient on the basis of previously reported Japanese data.¹⁴

All patients and volunteers were informed of the nature of the study; consent was obtained from each participant in the presence of a witness. The protocol of the study was approved by the Human Investigation Committee of the Futase Social Insurance Hospital.

All statistical procedures were performed using the Statview 4.11 software package (Abacus Concepts, Inc). Data are presented as the mean±SD. The unpaired t test (continuous variables) was used to assess the significance of the differences between the two patient groups. Group differences of the categorical data were tested by ² analyses. One-way ANOVA and Fisher's protected least-significant difference were used to assess the differences between the two stroke groups and the control subjects. Spearman's rank correlation coefficients were calculated to determine the relationship between the MD score or serum vitamin D concentration and each variable. Values of P<.05 were considered to be statistically significant.

	Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Characteristics of the Study Subjects
The clinical characteristics of the patients and control subjects are listed in Table 1. No differences were observed between the two groups of stroke patients for age, sex, type of stroke, or incidence of diabetes mellitus. The duration of illness for the inpatients was longer than that for the outpatients. The mean length of hospitalization was 560±989 days. The BI score and the degree of hemiplegia for the inpatients were worse than those for the outpatients, and the reduced mobility of these patients prevented them from venturing outdoors.

View this table: [in this window] [in a new window]   Table 1. Clinical Characteristics of Study Subjects

MD Score and Vitamin D
As shown in Table 2, both patient groups had higher MD scores on the hemiplegic than on the nonhemiplegic side. Even on the intact side, the patient groups scored about twice as high as the control subjects. The side-to-side differences in scores were higher in both patient groups than in the control subjects.

View this table: [in this window] [in a new window]   Table 2. MD Score and Serum Vitamin D Levels

The serum concentrations of 25-OHD and 1,25-[OH]₂D were lower in both groups of patients than in the control subjects, and they were lower in the hospitalized patients than in the outpatients. It is noteworthy that in 27 (64%) of the outpatients and 37 (82%) of the inpatients, the serum 25-OHD concentrations were <10 ng/mL (deficient level). Thirteen (31%) of the outpatients and 7 (16%) of the inpatients had vitamin D concentrations between 10 and 20 ng/mL (insufficient level). Among the patients with deficient 25-OHD levels, 7 (17%) of the outpatients and 21 (47%) of the inpatients had levels <5 ng/mL (osteomalacic levels).

Dietary Survey and Sunlight Exposure
Twenty-six (62%) of the outpatients and 37 (82%) of the inpatients consumed less vitamin D than the Japanese recommended daily allowance (100 IU). As shown in Table 2, both patient groups had a lower weekly dietary intake of vitamin D than did the control subjects, and the inpatients had lower consumption of vitamin D than did the outpatients. In addition, all of the admitted patients and 32 (76%) of the outpatients reported that they had no sunlight exposure during an average week.

Interrelationship Among the MD Score, Vitamin D, and Other Variables
The Spearman rank correlation coefficients between the MD score and each variable are listed separately for outpatients and inpatients in Table 3. The MD score on the hemiplegic side and the hemiplegic-nonhemiplegic differences in the score correlated negatively with the serum 25-OHD concentration in both the outpatients and the inpatients, whereas there was no correlation between the MD score of the intact side and the 25-OHD level. The dietary intake of vitamin D correlated negatively with the left-right difference in the score and positively with the serum 25-OHD level (r=.489; P=.0017) in the outpatients only. On the other hand, no correlation was observed between the serum 1,25-[OH]₂D concentrations and the MD scores and the left-right differences in the score. Both the MD score on the hemiplegic side and the hemiplegic-nonhemiplegic side differences in the score correlated positively with the duration of illness in the two patient groups and the length of hospitalization in the inpatients.

View this table: [in this window] [in a new window]   Table 3. Correlation Between MD Score and Each Variable

The MD score of the hemiplegic side correlated with the degree of hemiplegia not only for the affected hand but also for the affected lower limb in both patient groups. The left-right differences in the MD score correlated with the degree of hemiplegia in the hand, upper limb, and lower limb in the outpatients but not in the inpatients. However, the BI did not correlate with the MD score except for the left-right differences in the score in the outpatients.

The serum 25-OHD levels correlated negatively with the duration of illness in both the outpatients (r=-.331; P=.0338) and the inpatients (r=-.346; P=.0233). The BI was not correlated with the serum 25-OHD concentration in either patient group. The serum 1,25-[OH]₂D levels were not correlated with any of the variables examined.

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
There have been only a few reports on the bone changes on the hemiplegic side of stroke patients.^{7 8} In these studies, only small numbers of patients were examined,^{7 8} despite the repeated observation that hip fractures occur almost exclusively on the paralyzed side.^{1 2 3 4 5} Hodkinson and Brain⁷ have examined unilateral osteoporosis in elderly stroke patients with long-standing hemiplegia by comparing the radiographic findings of the two femora. Goodman⁸ has reported that osteoporosis can be detected in the hemiplegic upper limb within 16 weeks of stroke associated with shoulder-hand syndrome.

The MD method proposed by Anderson et al¹⁵ is based on a principle similar to that used in the photon absorption technique, although x-rays are used instead of -rays. The validity of this simple method has been reported by Inoue et al,¹³ who demonstrated a positive correlation for the iliac bone between five indices estimated by the MD method and the severity of osteoporosis as evaluated by photon absorptiometry and confirmed by pathological examination. Among the technologies available for the measurement of bone mass are single-photon absorptiometry, dual-photon absorptiometry, quantitative CT, and dual-energy x-ray absorptiometry. All of these methods, however, have advantages and disadvantages, and at present there is no consensus as to which is optimal. Although precision errors (coefficient of variation) are 3% to 5%,¹³ the precision of an improved MD method is almost the same as that of dual-energy x-ray absorptiometry,¹⁶ which is known as the most reliable means of bone mass measurement.¹⁷

We have previously demonstrated that differences in the MD indices between the hemiplegic and contralateral sides correlated well with the duration of the illness and the degree of hemiplegia for the fingers, arms, and legs. In addition, the same degree of osteopenia occurred in both small capsular and large hemispheric lesions. Thus, the combination of weakness and immobilization may be responsible for the osteopenia in the hemiplegic metacarpal bone.⁹

In the present study, it was demonstrated that many hemiplegic stroke patients have hypovitaminosis D. Overall, 95% of the outpatients and 98% of the hospitalized patients had deficient or insufficient serum levels of 25-OHD. It was surprising that 7 outpatients and 21 inpatients had serum 25-OHD levels that were consistent with osteomalacia (5 ng/mL), although we have no confirmation for the presence of osteomalacia. The mean serum values of 25-OHD in both the outpatients and inpatients were lower than those in housebound elderly Americans, whose mean value was 13.2 to 17.7 ng/mL.¹⁸ Because seasonal fluctuations in vitamin D levels have been reported,¹⁹ we measured the serum vitamin D levels in the patients and control subjects during the same season. Serum 25-OHD is derived from both dietary intake and sunlight-induced production by the skin^{20 21} and is the most abundant circulating vitamin D metabolite.²² It is the most sensitive and useful index of the body's vitamin D supply. On the other hand, the serum 1,25-[OH]₂D concentration does not exhibit seasonal fluctuations.

Importantly, the serum levels of 25-OHD negatively correlated with the hemiplegic limb MD score, as well as the hemiplegic-nonhemiplegic differences in the score, in both patient groups. Therefore, both immobility and vitamin D deficiency may contribute to the osteopenia observed in hemiplegic metacarpal bones. A closer correlation between the MD score on the affected side and the degree of paralysis of the hand was observed in the outpatients than in the inpatients, and the left-right score differences were not correlated with severity of hand paralysis in the inpatients, who had lower serum 25-OHD levels than the outpatients. The hypovitaminosis D was more severe as the duration of illness increased in both patient groups. Also, the chronically hospitalized patients in this study who were more severely disabled had lower serum vitamin D concentration values than did the outpatients. All things considered, vitamin D deficiency may overshadow the severity of paralysis as an osteopenia risk factor in chronically hospitalized patients. It should be explained that because there are not enough nursing homes in Japan for the disabled elderly population, many severely affected stroke patients must be in long-term hospital care.

One might expect to see similar effects in the hemiplegic femoral neck, as evidenced by the positive correlation between the degree of palsy in the lower limb and the MD score of the metacarpal on the hemiplegic side. Because the BI score showed no correlation with the MD scores, the more localized factor of hemiplegia rather than the overall immobility appears to contribute to osteopenia. Similarly, we found that the MD scores did not correlate with the BI score in immobilized patients with Binswanger's syndrome (Y. Sato, unpublished data, 1996). However, in the present study, the scores for the patients' intact sides were higher than those in the control subjects. Although hypovitaminosis D could account for this, it is difficult to rule out some contribution from immobility.

An association between low levels of serum 25-OHD and decreased bone mineral density has been reported in multiple sclerosis patients²³ and elderly nursing home residents.²⁴ However, osteopenia associated with vitamin D deficiency in hemiplegic stroke patients has not been previously reported.

A combination of sunlight deprivation due to immobilization, as evidenced by the BI score, with decreased dietary intake of vitamin D is likely to be the cause of the vitamin D deficiency. A number of studies have reported a relationship between vitamin D deficiency and hip fractures.^{25 26 27 28} Indeed, a hip fracture was demonstrated to be the presenting feature in 11 of 37 cases of osteomalacia in the elderly,²⁵ and osteomalacia was found in 13% of 130 patients with hip fractures.²⁶ The mean plasma 25-OHD concentration in one group of 39 hip-fracture patients was approximately 9 ng/mL.²⁷ In another group of 232 hip-fracture patients with a mean serum 25-OHD level of 17.7±9.2 ng/mL, 20% had values <10 ng/mL.²⁸ A recent study has suggested that daily supplementation with vitamin D (800 IU) and calcium (1200 mg) can reduce hip fracture by 43% in postmenopausal women.²⁹ The incidence of hip fracture in hemiplegic stroke patients may be reduced similarly by the routine use of vitamin D supplements.³⁰

	Selected Abbreviations and Acronyms

 

BI = Barthel Index MD = microdensitometer, microdensitometric 1,25-[OH]2D = 1,25-dihydroxyvitamin D 25-OHD = 25-hydroxyvitamin D

	Acknowledgments

 
The authors would like to thank Masanobu Inoue and Yoriko Sakata for their technical assistance in measuring the vitamin D concentrations.

Received July 8, 1996; revision received August 18, 1996; accepted September 12, 1996.

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