Relationship between bone mineral density and functional parameters of paraplegic patients in short-term after spinal cord injury/Omurilik yaralanmasi sonrasi kisa donemde paraplejik hastalarin kemik mineral yogunlugu ile fonksiyonel parametreleri arasindaki iliski.
Abstract: Aim: To determine the relationship between bone mineralization and functional activity level of paraplegic patients in short-term after spinal cord injury (SCI).

Material and Methods: Thirty paraplegic patients and twentynine healthy controls were admitted to this study. Bone mineral density (BMD) and Z-scores, together with serum calcium, phosphorus, alkaline phosphatase, parathyroid hormone and 25-hydroxyvitamin-D levels, urinary calcium and deoxypyridinoline excretion were measured. All patients underwent a rehabilitation program including range of motion and progressive resistance exercises, upper body ergometry exercises, standing training with long leg orthosis, wheelchair ambulation or walking either by orthosis or walking aids five times/week during hospitalization.

Results: There was no difference between the groups regarding BMD values and Z-scores. Mean serum calcium and parathyroid hormone levels were lower (p=0.016 and p<0.001, respectively), serum phosphorus and alkaline phosphatase levels were higher (p<0.001 and p=0.049, respectively) in the paraplegics as compared to the controls. Positive correlations were found between the radius BMD values and total duration of upper body ergometry exercise (r=0.550, p=0.027) and wheelchair use (r=0.622, p=0.010) and also between the femur BMD values and total duration of therapeutic standing (r=0.351, p=0.039). There was an inverse relationship between the femur BMD values and total duration of immobilization (r=-0.404, p= 0.033).

Conclusion: Early rehabilitation interventions may prevent bone demineralization. Paraplegic patients should be followed and evaluated also in long term for the increased risk of osteoporosis. (From the World of Osteoporosis 2008:14: 57-61)

Key words: Spinal cord injury, bone mineral density, bone turn over markers, osteoporosis

Amac: Paraplejik hastalarda fonksiyonel aktivite duzeyi ile kemik mineralizasyonu arasindaki iliskiyi omurilik yaralanmasi sonrasi kisa donem icinde arastirmaktir.

Gerec ve Yontem: Calismaya otuz paraplejik hasta ve yirmidokuz saglikli kontrol alindi. Kemik mineral yogunlugu (KMY) ve Z-skorlari olculdu. Serum kalsiyum, fosfor, alkalen fosfataz, paratiroid hormon ve 25-hydroksivitamin-D duzeyleri, idrar kalsiyum ve deoksipridinolin duzeyleri calisildi. Tum hastalar yatislan suresince haftada bes kez eklem hareket acikligi egzersizleri, progresif direncli egzersizler, ust ekstremite ergometri egzersizleri, uzun bacak yurume cihaziyla ayakta durma egzersizleri, tekerlekli sandalye ile ambulasyon egitimi ve ortez veya yardimci cihazla yurume egitimine alindi.

Bulgular: Kemik mineral yogunlugu degerleri ve Z skorlari acisindan gruplar arasinda fark yoktu. Paraplejik grupta kontrol grubuna gore ortalama serum kalsiyum ve paratiroid hormon duzeyleri dusuk, (sirasiyla p=0.016 ve p<0.001), serum fosfor ve alkalin fosfataz duzeyleri yuksek (sirasiyla p<0.001 ve p=0.049) bulundu. Radius KMY degerleri ile ust ekstremite ergometri toplam egzersiz suresi (r=0.550, p=0.027) ve toplam tekerlekli sandalye kullanim suresi (r=0.622, p=0.010) arasinda ve femur KMY degerleriyle terapotik ayakta durma toplam suresi (r=0.351, p=0.039) arasinda iliski saptandi. Femur KMY degerleri ile immobilizasyon toplam suresi arasinda ise tern iliski saptandi (r=-0.404, p-0.033).

Sonuc: Erken rehabilitasyon uygulamalari kemik deminerlizasyonunu onleyebilir. Paraplejik hastalar, artmis osteoporoz riski acisindan uzun donemde de takip edilmeli ve degerlendirilmelidirler. (Osteoporoz Dunyasindan 2008;14: 57-61)

Anahtar kelimeler. Omurilik yaralanmasi, kemik mineral yogunlugu, kemik dongusu belirtecleri, osteoporoz
Article Type: Report
Subject: Spinal cord injuries (Complications and side effects)
Paraplegics (Research)
Osteoporosis (Prevention)
Osteoporosis (Risk factors)
Bones (Density)
Bones (Research)
Bones (Physiological aspects)
Authors: Kulcu, Duygu Geler
Gonul, Guliz
Tur, Birkan Sonel
Kurtais, Yesim
Kucuk, Ozlem
Yalcin, Peyman
Pub Date: 12/01/2008
Publication: Name: From the Osteoporosis World Publisher: Galenos Yayincilik Audience: Academic Format: Magazine/Journal Subject: Health Copyright: COPYRIGHT 2008 Galenos Yayincilik ISSN: 1300-9141
Issue: Date: Dec, 2008
Topic: Event Code: 310 Science & research
Geographic: Geographic Scope: United States Geographic Code: 1USA United States
Accession Number: 195755877
Full Text: Introduction

It is known that bone demineralization and osteoporosis occur in patients with spinal cord injury (SCI), which may lead to pathological fractures (1).The acute treatment of patients with SCI has always focused on the injury itself, but there are complications which arise immediately after the injury. Bone loss as a consequence of SCI should not be of secondary concern. Bone demineralization occurs rapidly during the first months after injury and slowly continues up to two years before equilibrium between bone resorption and formation is restored (2,3). Many factors may affect bone mineral density (BMD) in spinal cord-injured patients such as age, sex, level of injury, time since injury, ambulatory status, and rehabilitative interventions (1).

Early intervention may be critical to prevent osteoporosis. In order to design the neccessary interventions, it may be useful to understand the relationship between bone demineralization and the patient's functional status in the early stages of SCI. The aim of this study has been to determine this possible short-term relationship by investigating BMD and bone turnover in paraplegic patients.

Material and Methods


Paraplegic patients with traumatic SCI admitted to Physical Medicine and Rehabilitation Department at the Ankara University School of Medicine, were included in this cross-sectional study. In order to minimize the influence of hormonal factors, age limits observed for inclusion in the study were 18 to 60 years for males and 18 to 40 years for females. All female patients were premenopausal. A time limit of maximally 6 months postinjury was also imposed.

Patients with heterotropic ossification, venous thrombosis, reflex sympathetic dystrophy syndrome, history of fracture (other than vertebrae due to traumatic event), chronic osteomyelitis, malignancy, use of drugs and systemic diseases affecting bone metabolism were excluded. The control group was chosen from individuals who had no risk factors for osteoporosis.

Demographic details and neurological status of the patients were recorded. The neurological status was defined and classified according to the American Spinal Injury Association impairment classification (ASIA) (4). Duration of immobilization (months), duration of therapeutic standing with long leg orthosis (months), duration of wheel-chair use (months), duration of ambulation either by orthosis or walking aids (months) and duration of exercise by upper body ergometry (months) were recorded as the functional parameters.

This study was approved by the Medical Ethics Committee of the Ankara University. All participants signed an informed consent.


Bone mineral density

Bone mineral density and Z-scores were measured at the lumbar spine (L2-L4), femur neck and distal radius with dual energy X-ray bone densitometer (Norland XR-36; Norland Co., Madison, WI). Bone mineral density was expressed in absolute terms (g/[cm.sup.2]) and the absolute BMD for each patient was expressed with the Z-score which is the comparison of the measured values with the mean BMD of age and sex matched healthy control group. In this study, Z-score was preferred since it represents the number of standard deviations that the measurement is above or below the age-matched mean BMD.

Biochemical markers and calcium homeostasis

Early morning, fasting blood was collected. Measurements were made of the serum levels of parathyroid hormone (PTH) (measured by immunolight 2000 chemiluminescence), calcitonin, osteocalcin (OC) (measured by RIA), 25 hydroxy vitamin D (measured by HPLC technique), calcium, phosphorus, and total alkaline phosphatase (tALP). Serum OC and serum tALP were the designated bone formation markers.

Twentyfour hour and early morning urine specimens were collected for the estimations of the clearance levels of calcium and deoxypyridinoline (measured by HPLC technique) which were taken as bone resorption markers.


All patients underwent a rehabilitation program including range of motion and progressive resistance exercises, upper body ergometry exercises, standing training with long leg orthosis, wheelchair ambulation or walking either by orthosis or walking aids. The frequency of physical training was 5 times per week during hospitalization. Physical therapy programs were customized according to the needs of the patients and each patient was physically trained for at least 1 hour a day.

Data analysis

Statistical analyses were performed by using the statistical package SPSS version 9.0. The comparison of BMD values and Z-scores between the patient and the control groups was performed by Mann-Whitney U test. In the patient group, Pearson correlation coefficient was used to determine the correlation of the functional parameters and the BMD values. The acceptance for statistical significance was considered to be p < 0.05 for group comparisons and r-values were considered for correlation analyses.


Patient characteristics

Thirty paraplegic patients were analyzed and compared with twentynine age matched controls. The mean age of patients was 35.3 [+ or -] 11.2 years and the mean age of controls was 36.5 [+ or -] 9.2 years. Fifteen patients had complete lesion according to ASIA. The mean body mass index (BMI) values of the patient group and of the control group were 22.1 [+ or -] 3.5 kg/[m.sup.2] and 23.0 [+ or -] 4.2 kg/[m.sup.2] respectively. There was no significant difference between the groups regarding age and BMI. Demographic and functional properties and neurological status of the patients are shown in Table-1.

Parameters of bone mineralization

The mean BMD values for each region of SCI and control groups are shown in Table-2. There was no significant difference between groups regarding BMD values and Z-scores of all regions (p > 0.05). The radius BMD values were 13% higher, the femur and the lumbar BMD values were 4.7% and 1.9% lower, respectively in patients compared to those of controls.

Parameters of biochemical markers and calcium homeostasis

Parameters of biochemical markers and parameters of calcium homeostasis and their reference ranges are presented in Table-2. The mean serum levels of calcium and PTH of the paraplegics were significantly lower (p= 0.016 and p < 0.001, respectively) than those of the controls but they did not exceeded the reference ranges. Mean serum phosphorus level was significantly higher (p < 0.001) in the paraplegics than in the controls and corresponded to the upper limit of the reference range. The mean serum levels for calcitonin and mean serum 25-hydroxyvitamin-D were not different between the two groups (p > 0.05).

As bone formation markers; the mean tALP level was above the upper limit of the reference range and was significantly higher (p= 0.049) in the paraplegics than in the controls whereas the mean serum OC levels of the two groups did not differ significantly (p > 0.05). Although the bone resorption markers of patients indicated a slight increase as compared to those of controls, they remained within the reference ranges. There was no statistically significant difference between the two groups in terms of the bone resorption markers (p > 0.05).

Correlation of BMD with functional parameters

There was a negative correlation between the femur BMD values and the total duration of immobilization (r= -0.404, p= 0.033). Positive correlations were found between the radius BMD values and the total duration of upper body ergometry exercises (r= 0.550, p= 0.027) and the total duration of wheel-chair use (r= 0.622, p= 0.010). The femur BMD values also positively correlated with the total duration of therapeutic standing (r= 0.351, p= 0.039).


In this study, relationships between BMD and functional parameters have been investigated in the short-term after SCI in paraplegic patients. The results of this study have shown that the radius and the femur BMD levels are significantly correlated with the functional activity level in paraplegic patients.

No BMD difference was found between the two groups in this study. Recent studies, which evaluated BMD of the forearm, femur neck and the lumbar spine have presented conflicting results (5-7). Maimoun et al (8), observed no differences in the BMD of these three regions three months after injury and Roberts et al (9) reported no BMD variation in the femoral neck between 8 and 24 weeks after injury. The results of these studies were similar to the results of our study. These results suggest that the dual X-ray absorptiometry (DEXA) technique for BMD estimation may not show evidence of demineralization in the early stages of SCI. However, in some studies osteoporosis in sublesional areas has been shown shortly after SCI by using the DEXA technique (6,7).

Several reasons may explain our findings. We did not know the basal BMD values of the patients just after injury. These data were estimated from measurements in our control subjects. This might cause bias in estimating the real bone loss. Furthermore, we did not survey and consider the physical activity level before SCI which might affect premorbid BMD level as well as the post-injury BMD level.

An inverse relationship between the femur BMD values and the total duration of immobilization and a positive relationship between the femur BMD and the total duration of therapeutic standing have been found in this study. These results show the importance of early mobilization on bone mineralization in the early stages of SCI. Early passive verticalization of the patient, such as therapeutic standing, decreases the magnitude of demineralization (2,10). Gravity associated with vertical positioning of the bones, e.g. standing, provides a stimulus for bone mineralization by increasing the intramedullary fluid pressure (11,12).The increased intramedullary blood pressure has a positive effect on bone mineralization (12). The loss of physical function after SCI leads to the degradation of trabecular bone micro architecture. It is hypothesized that the magnitude of the loads imposed on bone dictates its mineralization and structural design (13). High frequency, low-magnitude stimulation, such as exerted by skeletal muscle contractions during standing or low level functional activity, may be the primary determinant of trabecular bone structure (14,15).

Furthermore, weight loading stimulates the osteoblastic activity in the spine (16,17). Modlesky C et al (18) investigated trabecular bone micro architecture of the proximal tibia and the distal femur in men with SCI by using magnetic resonance imaging and found that they were markedly deteriorated. Although, loading associated with ambulation and normal physical function is suggested to be critical to maintain both the trabecular connectivity and bone mineral mass by several studies (16-18), there are some opposing results reporting that standing or walking by themselves do not improve BMD and do not prevent osteoporosis (3,19,20). Our results are also somewhat contradictory to each other, since there was a positive correlation between the femur BMD values and the total duration of therapeutic standing but not with the total duration of walking. The reason for this observation may be due to limited number of walking patients.

Positive correlations between the radius BMD values and the duration of wheelchair use and upper body ergometry exercise were found in the present study. This result shows the importance of muscle strengthening exercises on bone mineralization. Goemaere et al (21). reported that using wheelchair increases the forearm BMD in SCI patients. In healthy tennis players BMD of dominant extremities was found to be higher than those of normal population which is possibly related to the mechanical stress exerted to the upper extremity used in the sportive activity (22). Although radius BMD values were 13% higher than those of the controls, no significant difference was observed between the two groups in this study. This result was considered to be due to evaluation in the short-term and suggested that radius BMD values might increase in the long-term due to the influence of exercises as reported previously (21,22).

In the present study, calcium homeostasis was found to have deteriorated, but bone formation and bone resorption markers of the patients were not found to be different than those of the controls except for the elevated tALP levels. However, recent studies have demonstrated elevated resorption markers in the early stages of injury by assessing "modern" markers such as N-terminal cross-linked telopeptides of type I collagen (NTX), C-terminal cross-linked telopeptides of type I collagen (CTX), procollagen type I N propeptide (PINP) (9, 23-26). Possible reasons for the differences with our results may be due to the smaller sample size and particularly less specific markers used in this study as compared to those of recent studies.

Since bone mineralization in SCI is multifactorial, medication should be started soon after injury in addition to the rehabilitation interventions, to prevent bone demineralization. Bisphosphonates should be chosen for the treatment since these have been shown by several studies (27-29) to prevent bone loss in SCI. Bisphosphonates inhibit osteoclast recruitment and activity and reduce accelerated bone resorption in SCI (30). Pearson et al (29) have compared the effects of conventional rehabilitation programs with and without cyclic etidronate, and found that BMD loss was prevented in only those patients who had become ambulatory and had received etidronate. In conclusion, functional status of the paraplegic patients in the early stages of SCI was found to be closely related to bone mineralization. Early rehabilitation interventions should have positive effect on preventing bone demineralization. Patients with SCI should be followed and evaluated also in the long term for the increased risk of osteoporosis.


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Duygu Geler Kulcu, Guliz Gonul *, Birkan Sonel Tur *, Yepim Kurtaip *, Ozlem Kucuk **, Peyman Yalcyn *

Yeditepe Universitesi Tip Fakultesi Fiziksel Tip ve Rehabilitasyon Anabilim Dali, Istanbul

* Ankara Universitesi Tip Fakultesi Fiziksel Tip ve Rehabilitasyon, ** Nukleer Tip Anabilim Dali, Ankara, Turkey

Address for Correspondence/Yazisma Adresi: Dr. Duygu Geler Kuku, Basibuyuk Mahallesi Erdemli Cad. Nardty. C2 Blok. No: 24 Maltepe, Istanbul, Turkey

Tel.: 0216 578 41 08 Gsm: 0505 857 51 78 E-mail: Gelis Tarihi/Received: 06.08.2008 Kabul Tarihi/Accepted: 22.10.2008

Osteoporoz Dunyasindan Dergisi, Galenos Yayincilik tarafindan basilmistir. Her hakki saklidir. I World of Osteoporosis, published by Galenos Publishing. All rights reserved.
Table 1. Clinical and functional characteristics of patients
with SCI

                                       mean [+ or -] sd (a)

Age                                    35.38 [+ or -] 11.2

Body mass index (kg/[m.sup.2])          22.1 [+ or -] 3.5

Time since injury (months)              3.98 [+ or -] 1.9

Immobilization duration (months)        1.25 [+ or -] 0.47

Therapeutic standing duration      2.41 [+ or -] 0.64 (n = 24)

Upper body ergometry exercise       0.85 [+ or -] 0.9 (n = 30)
duration (months)

Wheelchair ambulation              2.60 [+ or -] 0.64 (n = 24)
duration (months)

Walking ambulation duration         1.65 [+ or -] 0.5 (n = 6)

                                                  n       %

Gender                                Male        15     50
                                     Female       15     50

Neurological level                  Thoracal      18     61.5
                                     Lumbar       12     38.5

ASIA (b)                           Incomplete     14     46.2
                                    Complete      16     53.8

Spacticity                             +          8      23.1
                                       -          22     76.9

(a) : standard deviation,

(b) : American Spinal Injury Association Impairement classification

Table 2. Bone mineral density and biochemical parameters of patient
and control groups

                                             SCI group
                                        (Mean [+ or -] SD)

Calcium (8.6-10.2mg/dl)                 9.27 [+ or -] 0.60

Phosphorus (2.7-4.5 mg/dl)              4.15 [+ or -] 0.56

Alkalinephosphatase (35-104UI/L)       119.16 [+ or -] 63.79

PTH (8.0-76pg/ml)                      23.11 [+ or -] 13.32

25OHD3 (10-50 [micro]g/L)               17.60 [+ or -] 8.65

Calcitonin (0-10pg/ml)                  8.34 [+ or -] 6.26

Osteocalcin (4.0-24 [micro]g/L)         12.20 [+ or -] 6.62

Urinary calcium(80-320 mg/24h)        253.86 [+ or -] 196.54

Urinary deoxypridinoline               27.36 [+ or -] 24.01
(8.0-45 pmol/[micro]molcreatinine)

Radius BMD (g/[cm.sup.2])               0.46 [+ or -] 0.10

Radius Z score                          0.79 [+ or -] 1.69

Lumbar BMD (g/[cm.sup.2])               0.99 [+ or -] 0.14

Lumbar Z score                         -0.22 [+ or -] .1.30

Femur BMD (g/[cm.sup.2])                0.81 [+ or -] 0.87

Femur Z Score                           0.08 [+ or -] 0.43

                                           Control group
                                        (Mean [+ or -] SD)         p

Calcium (8.6-10.2mg/dl)                  9.59 [+ or -] .64       0.016

Phosphorus (2.7-4.5 mg/dl)               3.55 [+ or -] .60       0.000

Alkalinephosphatase (35-104UI/L)       83.24 [+ or -] 31.61      0.049

PTH (8.0-76pg/ml)                      44.14 [+ or -] 24.14      0.000

25OHD3 (10-50 [micro]g/L)               19.57 [+ or -] 9.78      0.604

Calcitonin (0-10pg/ml)                  6.20 [+ or -] 3.34       0.308

Osteocalcin (4.0-24 [micro]g/L)         11.89 [+ or -] 6.26      0.992

Urinary calcium(80-320 mg/24h)         149.49 [+ or -] 76.48     0.084

Urinary deoxypridinoline               22.65 [+ or -] 18.33      0.751
(8.0-45 pmol/[micro]molcreatinine)

Radius BMD (g/[cm.sup.2])               0.40 [+ or -] 0.08       0.072

Radius Z score                          1.50 [+ or -] 1.60       0.260

Lumbar BMD (g/[cm.sup.2])               1.01 [+ or -] 0.15       0.555

Lumbar Z score                          -0.69 [+ or -] 1.26      0.334

Femur BMD (g/[cm.sup.2])                0.85 [+ or -] 1.43       0.219

Femur Z Score                           0.89 [+ or -] 0.15       0.360
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