Table 2.
Author; Citation; Sample Size/Sex; Group (G): Modality |
SCI Level; Severity; Duration |
Training Duration; Frequency; Time; Parameters |
Skeletal Site Evaluated and Outcomes Reported | Baseline BMD | BMD (% Difference versus Baseline) | |||
---|---|---|---|---|---|---|---|---|
UNCONTROLLED INTERVENTIONAL TRIALS | ||||||||
FES | ||||||||
Rodgers et al. [108] N = 9 M, 3 F FES KE RT |
C4-T10; incomplete and complete; 0.7–17 yr |
12 wk (actual 12–18 wk); 3 d/wk; 30 min/d Training parameters: 100 mA, 35 Hz, 300 µs |
Total cohort Distal tibia trabecular vBMD Acute participant Distal tibia trabecular vBMD |
Baseline 235 mg/cm3 400 mg/cm3 |
12–18 wk −5.4% −26% |
Note: vBMD assessed on N = 1 acute and N = 7 chronic SCI. Values = avg of the total and acute cohorts. Chronic cohort data are in Table 4. | ||
MULTIMODAL | ||||||||
Astorino et al. [103] N = 11 M, 2 F Multimodal ABPT regimen |
C4-L1; Complete and incomplete; 1.9 ± 2.7 yr (0.2–9.3 yr) |
6 mo; >2 d/wk; 2–3 h/d Training parameters: Individualized protocol that included active assistive exercise, lower extremity, and core RT, upper extremity cycle ergometry, bodyweight supported elliptical training, BWSTT, OGW, vibration training, and/or FES cycling |
Total body aBMD Lumbar spine aBMD R Total hip aBMD L Total hip aBMD R Femur neck aBMD L Femur neck aBMD R Femur trochanter aBMD L Femur trochanter aBMD R Distal femur aBMD L Distal femur aBMD R Proximal tibia aBMD L Proximal tibia aBMD |
Baseline 1.24 g/cm2 1.27 g/cm2 0.96 g/cm2 0.99 g/cm2 0.98 g/cm2 0.99 g/cm2 0.75 g/cm2 0.79 g/cm2 0.92 g/cm2 0.92 g/cm2 0.88 g/cm2 0.89 g/cm2 |
3 mo −1.6% * +3.2% * −3.1% * −4.0% * −2.0% * −3.0% * −2.7% −5.1% * −5.4% −4.4% −3.4% −4.5% |
6 mo −2.5% * +4.7% * −6.3% * −7.1% * −5.1% * −4.0% * −6.7% * −8.9% * −11% −7.6% −8.0% −11% |
Note: BMD determined on N = 8 <1 yr SCI and N = 5 chronic SCI. Values are avg of the total cohort and were not determined separately for acute and chronic SCI cohorts. | |
CONTROLLED INTERVENTIONAL TRIALS | ||||||||
BWSTT | ||||||||
de Bruin et al. [112] N = 13 M G1: BWSTT + standing, N = 4 M G2: Standing, N = 5 M G3: Low activity, N = 4 M |
C4-L1; AIS A-D; 1–5 wk |
6 mo; 5 d/wk; 60 min/d Training parameters: G1: 20–80% BWSTT (30 min/d), standing (30 min/d), ≥5 h/wk G2: Standing, ≥5 h/wk G3: Loading, 0–5 h/wk |
Distal tibia + diaphysis G1: Trabecular vBMD G2: Trabecular vBMD G3: Trabecular vBMD G1: Cortical vBMD G2: Cortical vBMD G3: Cortical vBMD |
Baseline N/R N/R N/R N/R N/R N/R |
6 mo −0.4% † −0.5% † −8.0% † −0.7% −1.1% −0.6% |
Note: † indicates statistically significant difference between G1 and G2 vs. G3, when indicated. | ||
Frey-Rindova et al. [114] N = 24 M G1: BWSTT + standing, N = 13 M G2: Low activity, N = 11 M |
C4-L1; Frankel A-C; 1–4 wk |
12 mo; ≥3 d/wk; 30 min/d Training parameters: G1: Partial bodyweight support, ~1.3 km/h G2: Same parameters performed <3 d/wk or <30 min/d |
Distal Tibia G1: Trabecular vBMD G2: Trabecular vBMD G1: Cortical vBMD G2: Cortical vBMD |
Baseline 316 mg/cm3 302 mg/cm3 935 mg/cm3 910 mg/cm3 |
6 mo −7% −3% −2% −1% |
12 mo −8% * −20% * −6% ** −8% ** |
||
STANDING | ||||||||
Alekna et al. [109] N = 44 M, 10 F G1: Standing, N = 22 M, 5 F G2: No standing, N = 22 M, 5 F |
C2-L1; AIS A-B; 11 ± 3 wk |
2 yr; ≥5 d/wk; ≥1 h/d Training parameters: G1: Passive standing G2: No standing |
G1: Total body aBMD G2: Total body aBMD G1: Lumbar spine aBMD G2: Lumbar spine aBMD G1: Pelvis aBMD G2: Pelvis aBMD G1: Whole leg aBMD G2: Whole leg aBMD |
1.26 g/cm2 1.26 g/cm2 1.28 g/cm2 1.26 g/cm2 1.18 g/cm2 1.18 g/cm2 1.36 g/cm2 1.38 g/cm2 |
1 yr −8.9% * −12% * −11% −14% −12% −15% −20% * −24% * |
2 yr −11% * −15% * −14% −17% −15% *† −21% *† −25% *†† −34% *†† |
||
Ben et al. [110] N = 16 M, 4 F G1: Unilateral standing, N = 20 G2: Untrained limb, N = 20 |
N/R; Nonambulatory; 4 ± 2 mo | 12 wk; 36 sessions; 30 min/d Training parameters: G1: Passive unilateral standing G2: No loading |
G1: Proximal femur aBMD G2: Proximal femur aBMD |
Baseline 0.91 g/cm2 0.91 g/cm2 |
12 wk −6.1% −6.7% |
|||
FES/NMES | ||||||||
Arija-Blazquez et al. [99] N = 8 M G1: FES RT, N = 5 M G2: SHAM FES, N = 3 M |
T4-T12; AIS A; G1: 5.5 ± 1.1 wk G2: 5.8 ± 1.7 wk |
14 wk; 5 d/wk; 47 min/d Training parameters: Both: 8 sets × 10 contractions G1: 0–140 mA, 30 Hz, 200 µs G2: 0 mA, 30Hz, 200 µs |
G1: Lumbar spine aBMD G2: Lumbar spine aBMD Femur G1: Total hip aBMD G2: Total hip aBMD G1: Femur neck aBMD G2: Femur neck aBMD G1: Ward triangle aBMD G2: Ward triangle aBMD G1: Trochanter aBMD G2: Trochanter aBMD G1: Intertrochanteric aBMD G2: Intertrochanteric aBMD G1: Whole leg aBMD G2: Whole leg aBMD |
Baseline 0.91 g/cm2 1.23 g/cm2 0.92 g/cm2 1.08 g/cm2 0.79 g/cm2 0.96 g/cm2 0.65 g/cm2 0.86 g/cm2 0.70 g/cm2 0.83 g/cm2 1.05 g/cm2 1.22 g/cm2 1.19 g/cm2 1.44 g/cm2 |
14 wk +3.5% +2.1% −7.0% −0.4% −7.6% −8.3% −6.5% −7.7% −9.9% −8.1% −5.9% −1.0% −2.9% −3.3% |
|||
Clark et al. [29] N = 33 (N per sex N/R) G1: FES RT, N = 23 G2: Inactive SCI control, N = 10 |
C4-T12; AIS A-D; 3 wk |
6 mo; 5 d/wk; 30 min/d Training parameters: G1: 2 × 15 min/d; 4:8 s on:off G2: Inactive control |
G1: Total body aBMD G2: Total body aBMD G1: Lower extremity aBMD G2: Lower extremity aBMD G1: Femur neck aBMD G2: Femur neck aBMD G1: Femur proximal aBMD G2: Femur proximal aBMD |
Baseline N/R N/R N/R N/R N/R N/R N/R N/R |
3 mo −2.2% †† +0.7% †† −2.4% −2.3% −4.5% −3.2% −6.0% −3.7% |
6 mo −3.0% −1.9% −7.1% −4.7% −11.6% −6.5% −11% −8.4% |
||
Dudley-Javoroski et al. [113] N = 24 M, 9 F G1: FES standing, N = 6 M, 1 F G2: Passive standing, N = 5 M G3: No standing, N = 13 M, 3 F |
C5-T12; AIS A-B; G1: 0.2–2.1 yr G2: 0.2–0.7 yr G3: 0.2–24 yr Note: G2 had N = 5 acute and N = 2 chronic SCI |
3 yr; 5 d/wk; 30 min/d Training parameters: G1: FES 10 min/d while unilateral standing, 0–200 mA, 20 Hz, 200 µs, 5:5 s on:off (2 bouts × 60 100-pulse trains), produced 150% bodyweight compressive load G2: 40% bodyweight compressive load G3: 0% BW (no standing) |
G1: Distal femur vBMD G2: Distal femur vBMD G3: Distal femur vBMD G1: Proximal tibia vBMD G1: Proximal tibia vBMD G1: Proximal tibia vBMD G1: Distal tibia vBMD G2: Distal tibia vBMD G3: Distal tibia vBMD |
Baseline N/R N/R N/R N/R N/R N/R N/R N/R N/R |
1 yr vs. G2 +30% † +23% +13% |
1 yr vs. G3 +48% † +29% −11% |
3 yr vs. G2 +41% † +21% −14% |
3 yr vs. G3 +102% † +47% −37% |
Dudley-Javoroski et al. [116] N = 11 M, 1 F G1: FES standing, N = 6 M, 1 F G2: Passive standing, N = 5 M |
C5-T12; AIS A-B; G1: 0.2–2.1 yr G2: 0.2–0.7 yr |
3 yr; 3 d/wk; 30 min/d Training parameters: G1: FES 10 min/d while unilateral standing, 0–200 mA, 20 Hz, 200 µs, 5:5 s on:off (2 bouts × 60 100-pulse trains), produced 150% bodyweight compressive load G2: 40% bodyweight compressive load |
Femur distal (trabecular) G1: Antero-lateral vBMD G2: Antero-lateral vBMD G1: Antero-medial vBMD G2: Antero-medial vBMD G1: Postero-lateral vBMD G2: Postero-lateral vBMD G1: Postero-medial vBMD G2: Postero-medial vBMD |
Baseline 233 mg/cm3 233 mg/cm3 188 mg/cm3 188 mg/cm3 220 mg/cm3 220 mg/cm3 224 mg/cm3 224 mg/cm3 |
0.25- 0.50 yr −1.6% −22% +3.8% −25% +3.3% −20% +6.4% −15% |
0.50- 0.75 yr −3.5% −19% −1.8% −20% −0.5% −12% +2.4% −9% |
0.75- 1.0 yr −0.6% −24% +2.3% −26% −4.8% −21% +0.9% −15% |
1.0- 1.5 yr −12% −19% −9.2% −17% −12% −23% −6.3% −14% |
Groah et al. [51] N = 22 M, 4 F G1: FES RT, N = 15 M, 1 F G2: SCI control, N = 7 M, 3 F |
>T12; AIS A-B; 35.9 ± 23.3 d |
6 wk; 5 d/wk; 1 h/d Training parameters: G1: 0–125 mA, 25 Hz, 300 µs, 5:5 s on:off G2: Standard of care control |
G1: Lumbar spine aBMD G2: Lumbar spine aBMD G1: Total hip aBMD G2: Total hip aBMD G1: Distal femur aBMD G2: Distal femur aBMD G1: Proximal tibia aBMD G2: Proximal tibia aBMD |
Baseline 1.32 g/cm2 1.27 g/cm2 1.19 g/cm2 1.19 g/cm2 1.11 g/cm2 0.96 g/cm2 1.04 g/cm2 0.86 g/cm2 |
6 wk +1.2% −7.2% −1.9% −13% −4.0% −3.5% −0.9% −4.6% |
F/U 3 mo −1.3% −1.9% −15% −12% −7.4% −15% −12% −17% |
||
Lai et al. [31] N = 20 M, 4 F G1: FES cycling, N = 10 M, 2 F G2: SCI control, N = 10 M, 2 F |
C5-T9; AIS A; 26–51 d |
3 mo; 3 d/wk; 30 min/d Training parameters: G1: mA controlled by microprocessor, 20 Hz, 300 µs G2: Control |
G1: Femur neck aBMD G2: Femur neck aBMD G1: Distal femur aBMD G2: Distal femur aBMD |
Baseline 0.93 g/cm2 0.91 g/cm2 1.00 g/cm2 1.00 g/cm2 |
3 mo −4.6% * −5.1% * −2.2% *† −6.7% *† |
F/U 3 mo −9.1% # −9.8% # −9.0% # −14% # |
||
Shields et al. [28] N = 6 (sex N/R) G1: NMES trained limb, N = 6 G2: Untrained limb, N = 6 |
C5-T10; AIS A; 0.16–0.35 yr |
1.65–3.0 yr; 5 d/wk; 20 min/d Training parameters: G1: 4 bouts × 120 trains (10 pulse train, 15 Hz, 667 ms every 2 s), 140% bodyweight compressive force on tibia G2: No NMES |
G1: Hip aBMD G2: Hip aBMD G1: Proximal tibia aBMD G2: Proximal tibia aBMD Both: Lumbar spine aBMD |
Baseline 0.97 g/cm2 0.96 g/cm2 0.29 g/cm2 0.31 g/cm2 1.10 g/cm2 |
1.5–6 mo −14% −13% +4% † −8% † −12% |
6–12 mo −22% # −22% # −4% #† −17% #† −14% |
12–18 mo −36% # −31% # −3% #† −27% #† −13% |
18–36 mo−35% #−34% #−17% #†−32% #†−15% |
Shields & Dudley-Javoroski [115] N = 7 (sex N/R) G1: NMES trained limb G2: Untrained limb |
C5-T10; AIS A; <6 wk |
2–3 yr; 5 d/wk; 35 min/d Training parameters: G1: 0–200 mA at 400 V, 15 Hz, 667 ms, 4 bouts × 10-pulse train every 2 s G2: No NMES |
Tibia Diaphysis G1: Cortical vBMD G2: Cortical vBMD Tibia Distal Epiphysis G1: Trabecular vBMD G2: Trabecular vBMD |
Baseline N/R N/R N/R N/R |
2–3 yr % untrained limb N/R–Not different N/R–Not different +31% vs. untrained |
G, group; BWSTT, bodyweight-supported treadmill training; RT, resistance training; NMES, neuromuscular electrical stimulation; FES, functional electrical stimulation; F, female; M, male; C, cervical; T, thoracic; L, lumbar; AIS, American Spinal Injury Association Impairment Scale; SCI Duration, time since SCI in relation to intervention; aBMD, areal bone mineral density; vBMD, volumetric bone mineral density; min, minute; h, hour; d, day; wk, week; mo, month; yr, year; N/R, not reported; F/U, follow-up after intervention complete; Note: % change was reported in individual papers or was manually calculated from data in tables and/or figures; * indicates <0.05, ** <0.01 vs. the baseline; # indicates <0.05 vs. the initial BMD assessment after the baseline; † indicates a p-value of <0.05, †† <0.01 between the marked groups; a lack of symbols indicates no statistical differences that were reported versus the baseline or between groups.