Table 4.

Musculoskeletal system

Article	Methods	Results
Catz et al.67 Israel D & B = 7 N = 29 Longitudinal	12 men and 1 woman; mean age 37 ± 5 years. (24–67 years) at injury; mean YPI 19 ± 3 years. 3 persons had non-trauma etiologies and 1 had an unknown etiology. Lumbar spine dimensions assessed twice over a 10-year interval. Comparison with AB controls (n =16). Outcome measure: lumbar AP radiographs.	The IALS dimensions found in the follow-up radiographs were similar to those taken 10 years earlier (P > 0.05).
Kiratli et al.58 USA D & B = 11 N = 434 Cross-sectional with AB controls	239 men and 7 women with SCI; age range 21–78 years; YPI range 0.1–51 years. Comparison of BMD throughout the femur and geometric properties at the femoral midshaft with AB controls (n =188), age and gender matched. Outcome measure: DEXA; radiographs.	SCI group had ↓ BMD (P < 0.0001) in all femoral regions (27, 25, and 43% for femoral neck, midshaft, and distal femur, respectively). Group with SCI were ↓ (P < 0.0001) in cortical area of femoral midshaft.
Garland et al.57 USA D& B = 11 N = 48 Cross-sectional with AB controls	31 women with complete SCI; mean age 43.9 ± 19.7 (20 – 77 years); mean YPI 16.9 ± 7.7 (2–40 years). BMD measured from lumbar spine, hip, and knee. Comparison with AB controls (n =17), age and gender matched. Outcome measure: DEXA.	BMD of spine in youngest (≤ 30 years), middle (31–50 years.), and oldest (50 >) SCI groups were 98, 108, and 115% of the densities of respective AB control groups (P < 0.0001). BMD of spine of oldest SCI group was equal to youngest AB control group. Mean loss of BMD in the knee in youngest, middle, and oldest SCI groups was 38, 25, and 25% compared with AB control group (P < 0.0001).
Vlychou et al.63 Greece D & B = 11 N =149 Cross-sectional with AB controls	33 men and 24 women with paraplegia; mean age 37.8 (21–66 years); YPI range 6 months-27 years. Comparison of BMD of the proximal and distal forearm, the femoral neck, the greater trochanter, and Ward’s triangle with AB controls (n =92), age and gender matched. Outcome measure: DEXA.	Group with SCI had ↓ BMD of femoral neck (P < 0.001 – male, P < 0.001 – woman), greater trochanter (P < 0.001 and P = 0.001), and Ward’s triangle (P = 0.001 and P = 0.005). Among men, 23.3% ↓ in femoral neck, 22.5% ↓ in greater trochanter, and 20.8% ↓ in Ward’s triangle compared to AB controls. In women, ↓ were 24.1%, 24.3%, and 24.2%.
Szollar et al.60 USA D & B = 11 N = 204 Cross-sectional with AB controls	135 men with SCI; mean age 48 ± 8 (20–78 years); YPI range 0–59 years. Comparison of BMD of the lumbar spine, femoral neck, Ward’s triangle, and the greater trochanter with AB controls (n =69), age and gender matched. Outcome measure: DEXA.	Lumbar spine BMDs of the 40- to 59-year old and the 60+ patients were ↑ (P < 0.012) than the AB control group. Femoral region BMDs of the 20- to 39-year old and 40- to 59-year old patients were all ↓ (P < 0.027) than the AB control group. Hip region BMD loss occurred starting at 1 YPI, plateaus at 19 YPI and then improves. Spine BMD in patients never ↓ significantly and started ↑ as YPI ↑. Femoral neck and Ward’s triangle BMDs ↓ after 1 YPI. After 19 YPI, slight ↑ in both regions.
Szollar et al.61 USA D & B = 13 N = 355 Cross-sectional with AB controls	263 men with SCI; mean age 48.8 ± 1.3 (20–78 years); YPI range 0.8 to 53 years. Comparison of BMD of the lumbar spine, femoral neck, Ward’s triangle, and the greater trochanter with AB controls (n = 92), age and gender matched. Outcome measure: DEXA.	Lumbar spine BMD was stable with a nonsignificant ↓ in persons with tetraplegia at 1–5 YPI in the 20–39 year old group. Lumbar spine BMD maintained in all other SCI groups, increasing with age, regardless of age at injury or level of injury. Persons injured <1 year had comparable BMD to AB controls. Persons aged 20–39 years old who were injured >1 YPI had ↓ (P < 0.01) BMDs in femoral region than AB matched controls and 20- to 39-year olds injured <1 YPI.
Chow et al.54; United Kingdom D & B = 9 N = 31 Cross-sectional with AB controls	19 men and 12 women with SCI; age range 19–60 years; mean YPI 5.87 ± 10.21 (5 wks–36 years). Comparison of BMD) of right heel, lumbar spine, and proximal femur region (femoral neck, Ward’s triangle, trochanteric and inter-trochanteric), and of bone structure (stiffness), with AB reference population, age and gender matched. Outcome measure: DEXA; Achilles USBD.	Ultrasonic properties at the calcaneus were ↓ (P < 0.05) in group with SCI. After 1 YPI, BMD in femoral neck ↓ (P < 0.05) in group with SCI compared with AB reference population.
Bauman et al.53 USA D & B = 11 N = 16 Cross-sectional with AB controls	8 men with paraplegia; mean age 40 ± 10 (25–58 years); mean YPI 16 ± 9 (3–26 years). Comparison of total and regional BMC and BMD with monozygotic twin. Outcome measure: DEXA.	Twins with SCI had ↓ total- body BMC (P < 0.001) compared with AB twin controls, with legs (P < 0.0001) and pelvis (P < 0.0001) being predominant sites for loss in BMC and BMD. Duration of SCI, and not age, was associated to degree of bone loss in twin with SCI.
de Bruin et al.50 Switzerland D & B = 13 N = 12 Longitudinal	12 men with SCI; mean age 32.4 ± 9 (23–50 years) at follow-up. Structural and geometric properties of tibia and cortical bone at 5 weeks post-injury and at approx. 2 YPI. Outcome measure: PQCT, bone stiffness measurement device.	Trabecular and cortical bone, and geometric properties of tibia bone ↓ (P < 0.05) within 2 YPI. Phase velocity propagation changed in swing tibia bone in 3 participants within 2 YPI.
de Bruin et al.51 Switzerland D & B = 12 N =10 Longitudinal	9 men and 1 woman with SCI; mean age 40.9 ± 19.7 (19–81 years) at follow-up. Trabecular and compact BMD of tibia and radius at 5 weeks post-injury and at approx. 3 ½ YPI. Outcome measure: PQCT	Trabecular tibia and compact bone ↓ (P < 0.05) within 3.5 YPI No changes in radius trabecular bone were observed. Patterns suggest no steady state of bone BMD following 3 YPI.
Eser et al.56 Switzerland D & B = 14 N = 110 Cross-sectional with AB controls	89 men; mean age 41.5 ± 14.2 (10–65 years); mean YPI 29.3 ± 12.5 (2 months-50 years). Comparison of BMD of distal epiphyses and midshafts of femur, tibia, and radius with AB controls (n =21), age and gender matched. Outcome measure: PQCT.	Group with SCI had ↓ BMD (P < 0.0001) than the AB control group.
Frey-Rindova et al.52 Switzerland D & B = 14 N = 29 Longitudinal	27 men and 2 women with SCI; age range 19 – 57 years. Trabecular and cortical BMD assessed within 1, at 6 at 12, and at 24 months post-injury. Outcome measure: PQCT.	Trabecular BMD of radius and ulna ↓ in persons with tetraplegia at 6 months (radius 19% less, P < 0.01; ulna 6% less, P < 0.005), and at 12 months (radius 28% less, P < 0.01; ulna 15% less, P < 0.05) post-injury. Cortical BMD of radius and ulna ↓ in persons with tetraplegia at 12 months (radius 3% less, P < 0.05; ulna 4% less, P < 0.05) post-injury. Trabecular BMD of tibia was ↓ 6 months (5% less, P < 0.05), and 12 months (15%, P < 0.05) post-injury.
Szollar et al.62 USA D & B = 11 N = 238 Cross-sectional with AB controls	176 men with SCI; mean age 41.2 (20–59 years); YPI range 0.8 to 34 years. Comparison of BMD of the lumbar spine, femoral neck, Ward’s triangle, and the greater trochanter and comparison of serum levels of calcium, calcitonin, biochemical markers of bone formation, and parathyroid hormone (PTH) with AB controls (n =62), age and gender matched. Outcome measure: DEXA; immunoassay methods.	Spine BMD remained stable above fracture threshold in the 20- to 39-year. and in the 30- to 49-year age groups. In all groups, there was progressive ↓ in BMD at proximal femur, and began 1–9 YPI. For the 20- to 39-year. age group, this was significant for all three areas. For the 30- to 49-year. age group, this progressed at a slower rate, reaching threshold at 10–19 YPI for all three areas. PTH levels remained below the reference range, with a slight gradual ↑ after 1 YPI. Results suggest parathyroid dysfunction-related osteoporosis.
Finsen et al.64 Norway D & B = 11 N = 38 Cross-sectional with AB controls	19 men with SCI; median age at injury 20 (15–64 years); median YPI 4 (7 months–33 years). Comparison of BMD of lower and upper extremities, and of biochemical and bone markers with AB controls (n =19), age and gender matched. Outcome measure: Gambro photonabsorption scanner; radioimmunoassay techniques.	SCI group had ↓ in metaphysis (45%; P = 0.0001) and diaphysis (26%; P = 0.0001) of tibia, while a barely significant difference of distal forearm was detected (diaphysis; P = 0.0418; metaphysic; P = .1611). SCI group had ↓ levels of serum creatinine (P = 0.0001), and ↑ levels of alanine aminotransferase (P = 0.007), serum phosphate (P = 0.014), follicle stimulating hormone (P = 0.016), and SHGB (P = 0.009). Total testosterone was equivalent but when divided by SHGB, ↑ (P = 0.011) in group with SCI.
Vaziri et al.65 USA D & B = 9 N = 54 Cross-sectional with AB controls	40 men with SCI; age range 25 – 69 years; YPI range 3 – 50 years; Comparison of serum PTH, calcitonin, vitamin D (calcitriol), 25 hydroxy (OH) vitamin D, 1,25 (OH)2, ionized calcium (Ca++), and phosphorous with AB controls (n =14), age and gender matched. Outcome measure: immunoassay methods.	Plasma PTH was ↓ in group with SCI (P < 0.001) compared with AB controls, despite equivalent concentrations of Ca++. Plasma calcitrol was ↓ in group with SCI (P < 0.05) compared to AB controls, and ↓ in persons with tetraplegia vs those with paraplegia (P < 0.05).
Dauty et al.55 France D & B = 10 N = 62 Cross-sectional with AB controls	31 men with SCI; mean age 36 ± 12.3 (18 – 60 years); mean YPI 6 (6 months–19 years). Comparison of supra- and sublesional BMD and BMC, and of blood and urine samples that included phosphocalcic parameters with determination of urinary hydroxyproline and deoxypyridinoline with AB controls (n =31), age and gender matched. Outcome measure: dual-photon absorptiometry; immunoassay methods.	SCI group had a ↓ (P < 0.0001) of sublesional BMD of 41% compared with AB controls. This loss of mass is ↑ at the distal femur (−52%) and proximal tibia (−70%). SCI group had ↓ BMD at the femoral neck (30%, P < 0.0001) and at the trochanter (39%, P < 0.0001) compared with AB controls. Also had ↓ BMC in lower limb (48%, P < 0.0001) and pelvis (55%, P < 0.0001). Blood phosphate level and urinary phosphate level were ↑ (P < 0.01) in group with SCI compared with AB controls. Urinary levels of calcium (P < 0.001), hydroxyproline (P < 0.0001), and deoxypiridoline (P < 0.01) are ↑ in group with SCI compared with AB controls.
Bauman et al.66; USA D & B = 10 N = 50 Cross-sectional with AB controls	100 men with SCI; mean age 51 ± 14 years; mean YPI 20 ± 13 (1–48 years). Comparison of serum calcium (Ca), phosphorus (PO4), albumin, alkaline phosphatase (Alk P), and PTH with serum 25-hydroxyvitamin D [25(OH)D] with AB controls (n =50), age and gender matched. Outcome measure: radioimmunoassay methods.	Approximately ⅓ of group with SCI were vitamin D deficient, which was a ↑ (P = 0.05) percentage than AB controls. Mean serum 25(OH) D was ↑ (P < 0.0005) in group with SCI compared to AB controls.
Slade et al.59; USA D & B = 11 N = 36 Cross-sectional with AB controls	19 women with complete SCI; mean age of premenopausal (< 30 years) 23.0 ± 2.55 years; mean YPI 5.6 ± 2.33 years, mean age of premenopausal (>35 years) 42.6 ± 4.66 years; mean YPI 12.2 ± 8.14 years; mean age of post-menopausal 54.5 ± 7.7 years; mean YPI 14.17 ± 11.9 years; Comparison of trabecular bone of the knee with AB controls (n =17), age and gender matched. Outcome measure: DEXA; magnetic resonance imager.	SCI group: trabecular bone was significantly ↓ compared with AB controls. SCI groups had fewer (−19 and −26% less) and thinner trabeculae (−6%) that were spaced further apart (40 and 62% more space between structures) resulting in less trabecular bone volume (−22 and −33%) compared with AB controls.
Amsters & Nitz68 Australia D & B = 8 N = 60 Cross-sectional with AB controls	30 men with tetraplegia; four groups (age > 50 years and YPI< 5 years; age < 40 years & YPI < 5years; age > 50 years & YPI > 15 years; age < 40 years & YPI > 15 years). Comparison of posture with AB controls (n =30), age and gender matched. Outcome measure: photography of bony landmarks.	Group with SCI had ↑ thoracic kyphosis (P < 0.05) than AB controls. Regardless of age and duration of injury, persons with SCI do not sit with greater pelvic tilt than AB controls.
Lal72; USA D & B = 7 N = 53 Longitudinal	35 men and 18 women with SCI; mean age 37 (19–81 years) at baseline. Incidence of degenerative shoulder changes at baseline, and every two years until 5–15 YPI. Outcome measure: X-rays.	72% of sample demonstrated radiological evidence of degenerative changes, but only 11% reported shoulder pain. Persons with ↑ age (< 30 years) had ↑ incidence of radiographic changes. Premature shoulder changes appear primarily in wheelchair users of advanced age in less than 10 yrs with predilection of acromioclavicular joint.
Kivimaki & Ahoniemi73; Finland D & B = 23 N = 223 Cross-sectional with AB controls	96 men and 24 women with SCI; age range 18–65 years; mean age of group with paraplegia 47.0 ± 13.1, mean YPI 8.9 ± 12.0; mean age of group with tetraplegia 45.0 ± 14.8, mean YPI 6.7 ± 8.6. Comparison of shoulders with AB controls (n =103), age and gender matched. Outcome measure: ultrasonography.	Osteophytes were found in shoulders of 14% of AB controls, 22% in group with paraplegia, and 26% in group with tetraplegia (P < 0.05). Although no differences were found in the thickness of the supraspinatus tendon between groups, the mean thickness of bicipital tendon sheath was ↓ (P < 0.01) in AB controls compared to group with SCI. Wear and tear changes of the glenohumeral joint appear to be frequent in persons with SCI.
Pentland & Twomey71 Australia D & B = 12 N = 104 Cross-sectional with AB controls	52 men with complete paraplegia; mean age 44 ± 12 years (2 groups: < 45 years; ≥ 45 years); mean YPI 17 ± 11 years (1 – 45 years). Comparison of bilateral upper limb physical functions with AB controls (n =52), age, gender, and activity matched. Outcome measure: concentric isokinetic average torque for shoulder; elbow flexion/extension; shoulder adduction and eccentric shoulder adduction; grip strength; shoulder and elbow active range of motion; upper limb pain.	AB controls had greater bilateral shoulder flexion than group with SCI, but group with SCI had greater bilateral elbow extension. Impairment and activity level were better predictors of strength in 9/14 muscles tested, whereas age was a better predictor in AB group.
Siddall et al.70 Australia D & B = 18 N =73 Longitudinal	60 men and 13 women with SCI; mean age at baseline 40 (21–81 years); mean YPI at baseline < 6 months. Assessed the prevalence, onset, and severity of pain at <1 YPI and at 5 YPI. Outcome measure: pain intensity via numeric scale; psychological distress; Von Korff chronic pain disability to assess pain interference on daily activities.	Mean onset for musculoskeletal pain was at 1.3 ± 1.7 yrs, with a high prevalence at 5 yrs with an initial decline in the first 6 months post-injury.
Jensen et al.69 USA D & B = 14 N = 147 Longitudinal	110 men and 37 women with SCI; mean age at follow-up 48.8 ± 13.0 (21–88 years); mean YPI at follow-up 16.6 ± 10.4 (3.2–57.4 years). Examined the change in the prevalence and intensity of pain over time (range 2–6 years between assessments). Outcome measure: brief pain inventory interference scale; bodily pain scale; SF-36; mental health scale.	The proportion of participants (34.7–48.3%) reporting shoulder pain ↑ (P < 0.001) over time.
Petrofsky & Laymon35 USA D & B = 13 N = 100 Cross-sectional with AB controls	50 men with complete paraplegia; four age groups (20–30 years, 31–40 years, 41–50 years, 51–65 years); YPI range 3 – 10 years. Comparison of strength and endurance during isometric exercise and at rest (leg and arms) with AB controls, age, gender, and height matched. Outcome measure: dynamometer.	Group with SCI were stronger (P < 0.05) in handgrip strength than any of the AB controls in any age group examined. Knee strength was stronger (P < 0.05) in AB controls than in the SCI group. Both controls and SCI group showed a reduction of strength in their quadriceps associated with aging.

Abbreviations: AB, able-bodied; AP, anteroposterior; BMC, bone mineral content; BMD, bone mineral density; D and B, Downs & Black Score; DEXA, dual-energy X-ray absorptiometry; IALS, interpophysolaminar spaces; PQCT, peripheral quantitative computerized tomography; PTH, parathyroid hormone; SCI, spinal cord injury; SHBG, sex hormone-binding globulin; USBD, ultrasound bone densitometer; YPI, years post-injury.