create the summary of the findings "Methods
Subjects
Patients with chronic SCI who were referred to Brain
and Spinal Injury Research center (BASIR) were
invited to participate in this cross-sectional study and
written consent was obtained from each participant
before enrollment. All participants were healthy and
lived with their families. All female patients older than
55-years-old were excluded to omit the bias effect of
menopausally induced osteoporosis. Exclusion criteria
were pregnancy, lactation, any rehabilitation therapy,
amputation, and non-traumatic SCI etiology. Patients
with a history of diabetes, cancer, endocrine disease,
acute infection, use of specific medications such as glucocorticoid, hormones, thyroid hormones, or nutritional
supplements, and smoking or alcohol consumption were
also excluded. The study was approved by the research
ethics committee of Tehran University of Medical
Sciences.
Anthropometric measures
All measurements were conducted by the same investigator. Body weight was measured using a digital wheelchair scale. Body height was obtained by measuring the
supine length, and BMI was calculated as body weight
(in kilograms) divided by height (in meters) squared.
Clinical measurements
All study participants were medically stable upon
inclusion into the study. Patients’ demographic features
such as sex, age, weight, height, supplement and drug
intakes, time since injury, location, and completeness
of injury were assessed by using a questionnaire in an
interview by an experienced investigator.
Dietary intake
Dietary intakes of the patients were assessed by standard
3-day food records and a food frequency questionnaire
validated by the nutrition group of the BASIR.14
Neurological assessment
The International Standards for Neurological
Classification of Spinal Cord Injury (ISNCSCI), which
is an examination used to determine the motor and
the sensory impairment, and the severity of an SCI
was used and the related American Spinal Injury
Association (ASIA) score was estimated.14,15 In this
classification, patients are classified into five groups
as follows: (A) Complete; no motor or sensory function is preserved in the sacral segments S4–S5, (B)
Incomplete; sensory but not motor function is preserved
below the neurological level and includes the sacral segments S4–S5. (C) Incomplete; motor function is preserved below the neurological level, and more than
half of key muscles below the neurological level have a
muscle grade <3. (D) Incomplete; motor function is preserved below the neurological level, and at least half of
key muscles below the neurological level have a muscle
grade of 3 or more. (E) motor and sensory function
are normal. The level of spinal injury was also determined by using imaging facilities such as magnetic resonance imaging. Patients with non-traumatic SCI were
excluded. Completeness was classified as either complete (no sensory or motor function preserved in the
sacral segments (S4–S5)) or incomplete (variable
motor function preserved below the neurological level
of injury).14,15
Laboratory measurements
Blood samples were taken to assess serum level of total
calcium (ionized plus albumin attached), phosphor,
and 25-hydroxy vitamin D in Endocrinology and
Metabolism Research Institute. Normal level of phosphor was considered as 2.5–4.5 mg/dl and normal
range of calcium level was 8.5–10.5 mg/dl. Serum 25-
hydroxy vitamin D levels were assessed by a competitive
protein-binding assay and the normal range was considered as 30.0–74.0 ng/ml.
Javidan et al. Evaluation of BMD in patients with chronic traumatic SCI
The Journal of Spinal Cord Medicine 2014 VOL. 37 NO. 6 745
BMD measurements
Dual-energy X-ray absorptiometry which is the proposed method to assess BMD16 was used. Calibration
of bone densitometer Lunar DPXMD device (Lunar
Corporation, Madison, WI, USA) was performed
weekly by using appropriate phantoms. The precision
error for BMD measurements was 2–3 in the femoral
and 1–1.5 in the lumbar regions. All scans were performed according to the manufacturer’s guidelines. Tscores and Z-scores of the femur neck, the trochanters,
the intertrochanteric zone, and also the lumbar vertebra
(L1–L4) were investigated. In patients with spinal
implant, the involved lumbar vertebras were excluded
and the mean bone density of non-involved vertebras
was entered into the analysis. An assessment of the
femur BMD was conducted by using the abovementioned three points (neck, trochanters, and intertrochanteric zone), which seemed to be adequate as an indicator
of long bones. We also measured the total hip BMD.
According to World Health Organization/Osteoporosis
foundations17 diagnostic categories, we defined osteoporosis as BMD T-score ≤ −2.5SD, osteopenia as
−2.5SD < T-score ≤ −1SD, and BMD T-score >−1SD
young adult mean was considered as normal.
Analysis
All statistical analyses were performed using SPSS 18.0
(SPSS, Inc., Chicago, IL, USA). We report results by
expressing percentages, mean ± 95% confidence interval, and the proper comparison of means using t-test
and one-way analysis of variances (ANOVA).
Pearson’s correlation was used to investigate correlations between variables along with linear regression
and univariate models. P < 0.05 was considered statistically significant. The data related to the intakes of
calcium, phosphor, and vitamin D data were analyzed
using Nutritionist IV 3.5.3. (N-Squared Computing,
Salem, OR, USA) modified for Iranian foods.18
The differences of vitamin D, calcium, and phosphor
intake amount and serum levels between those with
paraplegia and tetraplegia and those with complete
and incomplete injuries were determined by independent t-tests. Multivariate analysis with observed power
using α (0.05) was performed to evaluate the relationship between gender, completeness of injury, and
ASIA score with femoral and spinal BMD.
Results
Patients’ demographic features along with their daily
dietary intake and the serum levels of calcium, phosphor, and 25-hydroxy vitamin D are shown in Table 1.
Sex distribution of participants was 116 male (78.4%)
and 32 female (21.6%). Mean BMI was 23.71 in the
male group in which 64.7% had normal BMI (BMI <
25), 28.1% were overweight (BMI: 25– 30), and 7.2%
were obese (BMI>30) according to WHO classification.
The female group, with a mean BMI of 25.14, consisted
of 57.6% with normal BMI, 37.2% overweight, and
5.2% obese.
Total mean T-score in lumbar vertebras was −0.05 ±
1.99. For each patient, every lumbar vertebrae BMD
(L1–L4) was measured which included a total number
of 592 entries for 148 patients in whom 108 vertebras
were excluded because of implant placement. Mean
BMD of intact vertebrae with no implant was considered as lumbar vertebrae’s total BMD and entered
into analysis. No implant was administered in 78
patients. Female patients showed higher BMD in
femoral neck, trochanter, intertrochanic zone, and
total hip (P values for T-scores: 0.030, <0.0001, 0.006,
and 0.001 with r = 0.18, 0.37, 0.23, and 0.27, respectively) but no significant association between sex and
lumbar vertebrae’s BMD could be detected (Table 2).
Factors triggering BMD in patients with SCI are
shown in Table 3. A positive relationship between BMI
and femur neck, trochanter, and intertrochanteric zone
Table 1 Demographic features, serum level, and dietary intake of calcium, phosphor, and 25-hydroxy vitamin D in patients with SCI
Parameter
Female (n = 32) Male (n = 116)
Mean ± SD Range Mean ± SD Range
Age (years) 42.80 ± 4.81 36–54 51.00 ± 12.89 14–73
Weight (kg) 61.16 ± 12.67 41–98 70.79 ± 14.48 41–115
Height (cm) 156.21 ± 5.77 145–166 172.37 ± 7.17 155–188
BMI (kg/m2
) 25.14 ± 5.63 17.7–43.56 23.71 ± 4.034 17.07–36.30
Calcium level (mg/dl) 8.928 ± 0.551 8–10 9.506 ± 5.885 7.2–10.6
Phosphor level (mg/dl) 3.875 ± 0.385 2.99–4.67 3.772 ± 0.408 2.99–4.6
25-Hydroxy vitamin D (μg/dl) 54.70 ± 113.52 7.5–595 40.90 ± 53.06 6.40–343.10
Dietary calcium (mg) 565.7 ± 270.6 244–1178 835.3 ± 755 106–5910
Dietary phosphor (mg) 1061.6 ± 656.9 386–2560 1174.9 ± 709.88 160–4272
Dietary vitamin D (μg) 0.84 ± 1.23 0–3 1.26 ± 2.21 0–16
BMI, body mass index; SCI, spinal cord injury.
Javidan et al. Evaluation of BMD in patients with chronic traumatic SCI
746 The Journal of Spinal Cord Medicine 2014 VOL. 37 NO. 6
T- and Z-scores was detected only in female patients (P :
0.01, 0.019, 0.001, 0.003, 0.013, and <0.0001, respectively), but there was no significant relationship between
BMI and spinal vertebra BMD. The correlation
between BMI and total hip BMD in female patients
was also significant (P < 0.0001) (Table 3).
There was also no significant correlation between age
and female BMD, but older male patients had lower Tscore in lumbar vertebrae bone density (P < 0.02,
r = −0.21), while this relationship with spinal Z-score of
BMD remained non-significant (P = 0.08). We also
detected a negative relationship between age and femoral
neck BMD Z-score only in male participants (Table 3).
Post injury duration had no significant association
with bone density T- and Z-scores of femoral neck, trochanter, intertrochanteric zone, and total hip (Table 3).
SCI was complete in 77% of patients and incomplete
in 23%. Male patients with complete SCI had lower
BMD in lumbar vertebra T- and Z-score (P : 0.009
and 0.02, respectively), but femoral and total hip
BMD revealed no statistically significant difference
between these two groups. The most common type of
ASIA score in our center was type A (no motor or
sensory function is preserved in the sacral segments
S4–S5). We also detected lower bone density in intertrochanteric zone of femur in patients with ASIA type D
(P = 0.005), but no other relationship between ASIA
score and other bones’ density was found.
Patients’ age, weight, and BMI showed no significant
correlation with serum calcium and phosphor levels.
Mean calcium intake was 565.7 ± 270 mg/day in the
female group and 835.3 ± 755 mg/day in the male
patients with SCI. No supplemental intake existed. As
almost all patients were bedridden or unable to walk, sun
exposure was considered as “very low” for all patients.
Mean serum calcium and inorganic phosphor levels
showed no statistically significant relationship with age,
weight, height, BMI, femoral, and lumbar vertebrae Tand Z-scores of BMD. However, there was a negative correlation between serum 25-hydroxy vitamin D level and
lumbar vertebrae Z-score (P : 0.04, r = −0.18). There
was also no association between completeness of injury
and serum calcium and phosphor level. Renal function,
which was interpreted by creatinine clearance, was
normal in all the patients.
Serum levels of calcium, phosphor, and 25-hydroxy
vitamin D had also no difference between patients with
different ASIA score. The level of injury correlated significantly with the serum levels of calcium, phosphor, and 25-
hydroxy vitamin D as the higher calcium level was in
patients with injury at level T5 (P : 0.04), the highest phosphor level was at level of T6 (P : 0.006), and the highest 25-
hydroxy vitamin D was detected at the injury level of C4
(P : 0.027). Post injury duration had no effect on serum
calcium, phosphor, and 25-hydroxy vitamin D level.
Low levels of 25-hydroxy vitamin D were detected in
64.7% (lower than 30 ng/ml) (Table 4). This investigation
was performed on patients with SCI at their primary referral visits when no medical and rehabilitation treatments
were applied yet. Of course, most of these patients went
through some medical therapies after gathering required
items for this study."