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Physical Activity

Effects on Muscle Morphology, Strength and Endurance

Even though the most visible aspect of SCI involves impaired muscle function ranging from slight weakness to complete paralysis, there is far more research addressing aerobic training than pure resistance training for enhancing strength, endurance and other aspects of muscle function (Jacobs and Nash 2004). The effects of aerobic exercise on aerobic capacity will be summarised in a subsequent section that is focused on cardiovascular health. The present section describes the effects of various forms of exercise (i.e., not only pure resistance training but also those that incorporate the more frequently implemented endurance training as well) and the various adaptations that result in increased muscle mass. These adaptations are characterized as those pertaining to muscle morphology or muscle function. Muscle morphological changes in response to appropriately configured physical activity interventions are reflected in such outcomes as overall changes to muscle cross-sectional area (i.e, direct or indirect measures such as limb circumference) or in changes to individual muscle fibres as reflected by changes in individual muscle fibre size or fibre type. Changes in muscle function are often assessed by direct measurements of muscle strength or power output or might be reflected in muscular endurance (i.e., exercise capacity changes) such as that seen in the ability to manage greater loads over a longer period of time during a progressive exercise program.

Author YearCountry
Score
Research Design
Total Sample Size
Methods Outcome
Muscle Morphology
Carvalho et al. 2008Brazil

Downs & Black score=21

Prospective Controlled Trial

N=15

Population: Traumatic SCI: Mean age: 31.95±8.01 yrs; Gender: 15 males; Mean body mass: 63.52±9.41 kg; Mean height: 176.28±5.28 cm:; Mean time post-injury: 66.43±48.23 moTreatment: Gait group (n=8): Treadmill gait training at 0.5 km/h (increased according to individual’s capacity) with partial body weight support (BWS) and neuromuscular electrical stimulation (NMES) delivered by a custom built four-channel stimulator (200V at 25Hz with 300ms duration). Training was performed over 6 mo, 2d/wk, for 20 min each session. Control group (n=7) : individuals performed only conventional physiotherapy 2d/wk for 6 mo without using NMES.

Outcome Measures: MRI of bilateral thighs was performed in all participants, to determine the average cross sectional area (CSA) of quadriceps and mean value of gray scale. Outcomes were obtained at baseline and at the end of treatment (6 mo).

1.     At moment of inclusion in this study, the average CSA values for the gait group and control group did not differ significantly.2.     After 6 months, a significant increase of 15% quadriceps CSA occurred in the gait group.

3.     A 7.7% increase in gray scale value was also observed but was not statistically significant.

4.     In the control group, no significant change in CSA or gray scale value was found after 6 months, but there was a noteworthy decrease in gray scale value of 11.4%

.

Scremin et al. 1999USA

Downs & Black score=21

Pre-Post

N=13

Population: Age (range): 24-46 yrs; Gender: 13 males; Level of injury (range): C5-L1; Severity of Injury: ASIA A (100%); Time post-injury (range): 2-19 yrsTreatment: 3 phase, FES induced, ergometry exercise program. Phase 1: quadriceps strengthening; Phase 2: progressive sequential stimulation to achieve a rhythmic pedaling motion; Phase 3: FES induced cycling for 30 min

Outcome Measures: Muscle cross-sectional area and proportion of muscle and adipose tissue measured at baseline, at the first follow-up (mean 65.4 wks), and at second follow-up (mean 98.2 wks)

1.     The cross sectional area of the rectus femoris increased by 31% (p<0.001), the sartorius increased by 22% (p<0.025), the adductor magnus- hamstrings increased by 26% (p<0.001), the vastus lateralis increased by 39% (p=0.001), and the vastus medialis-intermedius increased by 31% (p=0.025).2.     The cross-sectional area of the adductor longus and gracilis muscles did not change. The ratio of muscle to adipose tissue increased significantly in thighs and calves.
Sabatier et al. 2006USA

Downs & Black score=21

Pre-Post

N=5

Population: Mean age: 35.6 yrs; Gender: 5 males; Severity of injury: AISA A (100%); Mean time post-injury: 13.47±6.5 yrsTreatment: Patients underwent 18 wks of home-based neuromuscular electrical stimulation (NMES) resistance training on the quadricpes muscle group 2d/wk with 4 sets of 10 dynamic knee extensions against resistance while in a seated position

Outcome Measures: Femoral arterial diameter resting blood flow, blood velocity, and neuromuscular fatigue. All measurements were made before training and after 8, 12, and 18 wks of training.

1.     Training resulted in significant increases in weight lifted and muscle mass and a 60% reduction in muscle fatigue (p=0.001).2.     Femoral arterial diameter did not increase (p=0.70). Resting, reactive hypermic, and exercise blood flow did not appear to change with training.

3.     Quadriceps femoris muscle CSA was increased in both thighs after 18 weeks.

4.     The mean QF CSA of the right thigh was significantly increased from 32.6 to 44.0 cm² (p<0.05), and the left QF was increased from 34.6 to 47.9 cm² (p<0.05) which is a 35% and 39% increase in CSA respectively.

Kern et al. 2010Austria

Downs & Black score=19

Pre-Post

N=25

Population: Complete conus cauda syndrome:  Age (range): 20-55 yrs; Gender: 20 males, 5 females; Time post-injury (range): 0.7-8.7 yrs;Treatment: Muscles of patients were electrically stimulated at home by large surface area electrodes and a custom designed stimulator.

Outcome Measures: Force induced by electrical stimulation, isometric knee extension torque, force measurements, area and density of quadriceps muscle and hamstring, tissue type distribution recorded before, at 1 yr, and after the 2 yrs of training

1.     Similar increase in muscle excitability and contractility in both legs.2.     Improved feasibility to elicit tetanic contractions with about ten times improvement.

3.     Myofiber size increased by 94% after 2 years of FES.

4.      Functional class improved to a level 4 for 20% of the subjects.

5.     After 2 years of home-based FES, the degenerative phase of LMN denervation was delayed or reverted.

Griffin et al. 2009USA

Downs & Black score=19

Pre-Post

N=18

Population: Traumatic SCI: Mean age: 40±2.4 yrs; Gender: 13 males, 5 females; Time post-injury: 11±3.1 yrsTreatment: FES cycling performed on an Ergys2 automated recumbent bicycle 2–3 d/wk for 10 wks

Outcome Measures: Total body mass, lean muscle mass

1.     Training week had a statistically significant effect on the ride time without manually assisted pedaling. Ride times during training weeks 5–10 were statistically greater than during week 1.2.     Total body mass (3%) and lean muscle mass (4%) significantly increased, while, there was no significant difference in bone or adipose tissue following the 10 weeks of training

3.

Carvalho et al. 2009Brazil

Downs & Black score=19

Cohort

N=7

Population: Traumatic SCI: Mean age: 32.8±3.5 yrs; Gender: 7 males; Mean body mass: 65.5±10.6 kg; Mean height: 176.8±8.4 cm; Mean time post-injury: 55.3± 10.6 moTreatment: Individuals performed conventional physiotherapy, 2d/ wk without using NMES for 6 mo. After 6 mo, the CG was provided an additional 6 mo of gait training without NMES.

Outcome Measures: MRI of bilateral thighs was performed on all participants, to determine the average cross sectional area (CSA) of quadriceps. Outcomes were measured 6 months post intervention.

1.     1 year post Carvalho et al. (2008) intervention no significant changes were observed in the quadriceps CSA in individuals receiving conventional physiotherapy.
Giangregorio et al. 2006Canada

Downs & Black score=18

Pre-Post

N=14

Population: Chronic Incomplete SCI: Mean age: 29 yrs; Gender: 11 males, 3 females; Level of injury: Tetraplegia (11), Paraplegia (3); Severity of injury: ASIA C (86%); ASIA B (14%); Mean time post-injury: 7.7 yrsTreatment: Body weight supported treadmill training (BWSTT) program – 144 sessions, 3 d/wk.

Outcome Measures: Lean body mass; Muscle cross sectional area (CSAs).

1.   BWSTT training ↑ whole body lean mass (p<0.003).2.   ↑ muscle CSAs in the thigh (4.9%) and lower leg (8.2%).
Willoughby et al. 2000USA

Downs & Black score=17

Pre-Post

N=10

Population: Age (range): 16-50 yrs; Gender: 5 males, 3 females; Level of injury (range): C4-T12; Severity of injury: AISA A and C; Time post- injury(range):1-9.4yrsTreatment: 12 wk exercise program using the Psycle ergometer. Training 2 d/wk at 75% of each subject’s maximum heart rate.

Outcome Measures: Thigh girth, body weight, and body mass index measured before and after training.

1.     mRNA expression had a significant increase in expression of MHC types IIa and Iix, and significant decreases in the expression for UBI, E2, and 20S.2.     The overall mean decrease for body weight and BMI from pre-training to post-training decreased for all eight subjects1.82±4.4% and 1.40±1.3%, respectively.

3.     There was also an increase of 63.08%, 49.47%, and 61.39% that were significantly different for α-actin (t(7)=2.61 (p=0.0413), MHC type II a (t(7)=3.04 (p=0.0188), and MHC type II x (t(7)=2.51 (p=0.0405) respectively.

Heesterbeek et al. 2005

The Netherlands

Downs & Black score=16

Pre-post

N=10

Population: Chronic Paraplegia; Mean age: 39.3 yrs; Gender: 9 males, 1 female; Severity of injury: ASIA A (90%), ASIA C (10%);  Mean time post-injury: 10.5 yrsTreatment: Exercise program – 4 wks, 8-12 total sessions. Each session consisted of a 5min warm-up, 30min hybrid (voluntary arm and FES-assisted leg) cycling & a 5min cool-down.

Outcome Measures: Leg Volume; Graded Hybrid Exercise Test (GHT) – peak power output (POpeak); Power of the legs (defined by delta power); all @ baseline & 4 wks.

1.   Leg Volume:·       Upper left leg: 8.3% ↑ (p=0.018)

·       Upper right leg: 8.5% ↑ (p=0.047)

·       Lower legs did not change.

2.   POpeak: ↑ 9.3% (p=0.015).

3.   Power of legs: did not change

Chilibeck et al. 1999

Canada

Downs & Black score=14

Pre-post

N=6

Population: Chronic SCI: Age (range): 31-50 yrs Gender: 5 males, 1 female;; Time post-injury (range): 3-25 yrsTreatment: FES training with a leg cycle ergometer- 30 min, 3 d/wk for 8 wks

Outcome Measures: Work rate, duration & total work output/exercise per session; Muscle fibre composition & area; Capillarization.

1.   Mean fibre area: ↑ 23% after training (p<0.05)2.   Capillarization: capillary-to-fibre ratio ↑ 39% (p<0.05) & capillaries contacted with each fibre ↑ 29% (p<0.05).

3.   Mean work rate: ↑ from 0 to 5.1 watts (p<0.05) from baseline to 8 wks.

4.   Mean duration: continuously pedal without assistance ↑ from 4.3 min to 21.2±5.6 min after training (p<0.05).

5.   Mean total work output:  ↑ from 0 to 9.2 KJ at 8 wks (p<0.05).

Crameri et al. 2002

Denmark
Downs & Black score=14
Pre-post
N=6

Population: Chronic complete paraplegia: Age (range): 28-43 yrs; Gender: 5 males, 1 female; Time post-injury (range): 8-36 yrsTreatment: FES leg cycle ergometry training- 30min/d, 3d/wk, for 10 wks

Outcome Measures: Incremental exercise leg test to muscle fatigue (total work output); Histological assessment; Myosin heavy chain (MHC); Citrate synthase and hexokinase.

1.   Paralysed vastus lateralis muscle was altered with ↑ type IIA fibres, ↓ type IIX fibres ↓ MHC IIx and ↑ MHC IIa (p<0.05).2.   Total mean fibre cross-sectional area ↑ 129%, ↑ cross-sectional area of type IIa and IIx fibres (p<0.05).

3.   Number of capillaries surrounding each fibre ↑ (p<0.05).

4.   Citrate synthase and hexokinase activity ↑ (p<0.05).

5.   Total work performed:  ↑ after training (p<0.05)

Mohr et al. 1997Denmark

Downs & Black score=14

Pre-post

N=10

Population: Chronic Complete SCI: Age range: 27-45 yrs; Gender: 8 males, 2  females; Level of injury: Tetraplegia (6), Paraplegia (4); Time post-injury (range): 3-23 yrsTreatment: 1 yr exercise training using an FES cycle ergometer (30 min/d, 3 d/wk)

Outcome Measures: Total work output; Muscle properties; @ baseline & 1 yr

1.   12% ↑ in thigh muscle mass over 1 yr.2.   Muscle atrophy found @ baseline partially improved by 1 yr.

3.   4 fold ↑ in total work output.

Sloan et al. 1994

Australia

Downs & Black score=14

Pre-post

Initial N=12; Final N=9

Population: Age range: 15-54 yrs; Gender: 7 males, 5  females; Severity of injury: complete (1), incomplete (11); Time post-injury (range): 2 -138 moTreatment: Electrical stimulation induced cycling programme: 3d/wk for 3 mo, all programmes were individualized & gradually progressed to 30 min each.

Outcome Measures: Quadriceps muscle area & Thigh muscle area – cross sectional analysis (CSA); Neurological muscle charts; @ baseline & 3 mo

1.   Muscle size:·       ↑ Quadriceps CSA (p<0.05)

·       ↑ Total thigh CSA (p<0.05)

2.   Muscle strength:

·       ↑ Voluntary isometric strength (p<0.05)

·       ↑ Stimulated isometric strength (p<0.05) ↑ Stimulated quadriceps endurance (p<0.05)

·       ↑ Quadriceps & biceps femoris grading (p<0.05).

3.   Cycling improvement:

·       9/9 ↑ cycling time by a mean of 11.7 min

·       8/9 ↑ cycling load by a mean of 30N.

·       Speed=constant

Giangregorio et al. 2005 CanadaDowns & Black score=13

Pre-post

N=5

Population: Tetraplegia; Age range: 19-40 yrs; Gender: 2 males, 3 females; Severity of injury: ASIA B (4), ASIA C (1); Time post-injury (range): 66-170 dTreatment: Body-weight supported treadmill training (BWSTT). Initial session started at 5min, ↑ gradually to 10-15min in all but 1 participant during 2d/wk training over a period of 6-8 mo

Outcome measures: Muscle cross-sectional area (CSA) done pre & post treatment; Average adherence.

1.    ↑ muscle CSAs were seen in all patients.2.   Total body lean mass and fat mass ↑.

3.   Partial reversal of muscle atrophy was seen.

4.   Average adherence = 78%.

Crameri et al. 2004 Denmark

Downs & Black score=22

Prospective controlled trial

N=6

Population: Chronic complete paraplegia; Age range: 26-54 yrs; Time post-injury (range): 3-21 yrsTreatment: FES training 45 min/d, 3 d/wk, for 10 wks. One leg: dynamic cycle ergometry involving bilateral quadriceps and hamstring stimulation; Contralateral leg: isometric contractions.

Outcome Measures: Muscle biopsies; Capillary-to-fibre ratio; Muscle proteins; Oxygenation.

1.   The isometric-trained leg showed significantly larger mean improvements force, type 1 fibres, fibre cross-sectional area, capillary-to-fibre ratio, citrate synthase activity & relative oxygenation after static training, in comparison to baseline & the dynamically trained leg.2.   These changes reflect the importance of load in the amount of adaptation to FES.
Hjeltnes et al. 1997 NorwayDowns & Black score=12

Pre-post

N=5

Population: Chronic Complete Tetraplegia; Mean age: 35 yrs; Gender: 5 males; Mean time post-injury: 10.2 yrsTreatment: 8 wks of FES leg cycling, 7d/wk

Outcome Measures: Cross sectional area (CSA) of multiple muscles.

1.   21.3% ↑ from 267cm2 to 324cmin muscle cross-sectional area for hamstrings, quadriceps, gluteus maximus & gluteus medius muscles (p<0.05).
Mahoney et al. 2005

USA
Downs & Black score=11

Pre-post

N=10

Population: Chronic SCI; Mean age: 35.6 yrs; Gender: 5 males, 5 females; Mean time post-injury:13.4 yrsTreatment: Residence-based, resistance exercise training (RET) for  thighs for 12 wks, 2d/wk for 4 sets of 10 unilateral, dynamic knee extensions. RET induced extensions via neuromuscular electric stimulation.

Outcome Measures: Muscle cross sectional area (CSA) – quadriceps femoris; @ baseline & 12 wks.

1.   Muscle CSA: 35% ↑ in right quadriceps femoris (32.6cm@ baseline to 44.0cm2 @ 12 wks) 39%↑ in left quadriceps femoris (34.6cm2 @ baseline to 47.9cm2 @ 12 wks) (p<0.05).
Stewart et al. 2004

Canada

Downs & Black score=10

Pre-post

N=9

Population: Incomplete SCI; Gender: 8 males, 1 female; Mean time post-injury: 8.1 yrsTreatment: Body weight-supported treadmill training, 3 d/wk for 6 mo

Outcome Measures: Treadmill performance; Muscle biopsy – Fibre type & Myosin heavy chain (MHC) analysis.

1.   Muscle biopsy:·       ↑ mean muscle-fibre area of type I & IIa fibres (p<0.001)

·       ↓ in mean type IIax/IIx fibres (p<0.05)

·       ↓ IIx myosin heavy chain (p<0.05)

·       ↑ mean type IIa fibres (p<0.01)

2.             Treadmill performance:

·       135% ↑ treadmill velocity (p<0.05)

·        55%, ↑ in session length (p<0.05)

·       amount of externally supported weight ↓ as the result of training (p<0.05)

Strength
Needham-Shropshire et al. 1997USA/CA

PEDro=8

RCT

Initial N=43; Final N=32

Population: Chronic Tetraplegia; Mean age: 18-45yrs; Gender: 31 males, 3 females; Mean time post-injury: 3yrsTreatment: Subjects randomly assigned to one of three groups: Group 1 – received 8 wks of neuromuscular stimulation (NMS) assisted arm ergometry exercise. Group 2 – received 4 wks of NMS assisted exercise, and then 4 wks of voluntary arm crank exercise. Group 3 (control group) – voluntary exercise for 8 wks without the application on NMS.

Outcome Measures: Manual muscle test.

1.   No significant difference was found at the 4-week evaluation between Groups 1 and 2 or between Groups 2 and 3.2.   Subjects in Group 1 had a higher proportion of muscles improving one or more muscle grades after 4 weeks of NMS cycling compared with Group 3 (p<0.003).

3.   Following the second 4 weeks of training, a significant difference was found between Groups 1 and 3 (p<0.0005) and between Groups 2 and 3 (p<0.03).

4.   No statistical difference was found between Groups1 and 2.

Glinsky et al. 2008Australia

PEDro=8

RCT

Initial N= 32

Final N= 29

Population: Intervention group: Mean age: 37±16 yrs; Gender: 12 males, 3 females; Control group:  Mean age:  47±20 yrs; Gender: 15 males, 1 femaleTreatment: The intervention group carried out a progressive resistance exercise program on one wrist 3 d/wk for 8 wks. It consisted of three sets of 10 repetitions (maximum) of one wrist muscle group, which was increased if the participant could do more than 10 repetitions and decreased if 10 repetitions were not achieved.

Control group received routine physiotherapy and occupational therapy with no progressive resistance exercise program for the wrist.

Outcome Measures: Strength measured as maximal voluntary isometric torque in Nm, muscle endurance measured as fatigue resistance and participants’ perceptions about use of their hands using the Canadian Occupational Performance Measure (COPM). Measurements were taken at the beginning of the program and at end of 8 wks.

1.     No statistically significant evidence was found to suggest that progressive resistance exercise does or does not increase strength and/or endurance. Although, an 11% increase in mean initial muscle endurance and an 8% increase in mean initial strength was noted  in the experimental group compared to the control group2.     The activities of daily living most frequently selected by participants as part of COPM assessment were using cutlery and lifting objects such as bottles and cups. The mean effects of progressive resistance exercise on these activities were –0.3 for participants’ perceptions of performance and –0.3 for participants’ satisfaction. This indicates that the experimental group did not perceive that progressive resistance exercise improved performance of or satisfaction with their activities of daily living compared with the control group.
Alexeeva et al. 2011USA

PEDro=7

RCT

N=35

Population:Fixed Track Group: Mean age: 37.3± 13 yrs ; Gender: 12 males, 2 females; Level of injury: ASIA C (17%), ASIA D (83%); Cause of injury: traumatic (100%)

Treadmill Group: Mean age: 36.4±12.9 yrs ; Gender: 8 males, 1 female; Level of injury: ASIA C (36%), ASIA D (64%); Cause of injury: traumatic (100%)

Physical Therapy Group: Mean age: 43.3±15.8 yrs ; Gender: 10 males, 2 females; Level of injury: ASIA C (11%), ASIA D (89%); Cause of injury: traumatic (75%), non-traumatic (25%)

Treatment: Patients participated in a body weight supported training program (Fixed Track or Treadmill) or comprehensive physical therapy for 1hr/d, 3 d/wk for 13 wks.

Outcome Measures:  ASIA International Standard (AIS) manual muscle test (MMT)

1.   The mean change in muscle strength increased by 6-9% across all groups.2.   There was a significant increase in strength across all groups (p<0.01), but no difference between groups.
Mulroy et al. 2011USA

PEDro=7

RCT

N=80

Population: Exercise/Movement Optimization group:  Mean age: 47±9 yrs; Gender: 31 males, 9 females; Level of injury: ASIA A (62%), ASIA B (23%), ASIA C (8%), ASIA D (2%), Unknown (5%)Control Group: Mean age: 47±12 yrs; Gender: 26 males, 14 females; Level of injury: ASIA A (62%), ASIA B (13%), ASIA C (13%), ASIA D (2%), UNKNOWN (10%)

Treatment: Patients received a shoulder home exercise program 3d/wk for 12 wks.  Stretching, warm-up, and resistive shoulder exercises were included.

Outcome Measures: Shoulder muscle force production using a handheld dynamometer

1.   Strength gains were significantly greater in the exercise/movement optimization group compared with the control group in all 4 motions tested (p<0.01).2.   All muscle groups demonstrated a statistically significant increase in maximal torque production following the intervention in the exercise/movement optimization group (p<0.05).
Hicks et al. 2003Canada

Downs & Black score=20

PEDro=5

RCT

Initial N=34; Final N=24

Population: Chronic SCI; Age (range): 19-65 yrs; Level of injury: C4-L1; Time post-injury (range):1-24 yrsTreatment: Intervention group  participated in progressive arm ergometry exercise training and progressive resistance training in several upper body muscle groups twice weekly for 9 mo-each session offered on alternative days lasing 90-120 min.

Outcome Measures: Muscle strength

1.   Following training, EX group had 81% ↑ sub maximal arm ergometry power output (p<0.05) & 1-35% ↑ in upper body muscle strength (p<0.05).2.   Overall 11 in the EX group (exercise adherence 82.5%) and 13 in the control group completed the study.
Jacobs et al. 2009USA

PEDro=5

RCT

N=18

Population: Traumatic SCI: RT Group: Mean age: 33.7±8.0 yrs; Gender: 6 males, 3 females; Mean body mass: 72.3±18.3 kg: ET group: Mean age: 29.0±9.9 yrs; Gender: 6 males, 3 females; Mean body mass: 83.7±8.9 kgTreatment: Subjects participated in a series of testing sessions before and after a 12wk training period. Patients were randomly assigned to two groups. The endurance training (ET) group performed 30 min of arm cranking exercise using a Saratoga arm crank device during each session at 70%–85% of HRpeak. The resistance training (RT) group performed three sets of 10 repetitions at six Hammer Strength MTS exercise stations (including horizontal press, horizontal row, overhead press, overhead pull, seated dips, and arm curls) with an intensity  ranging from 60% to 70% of 1 rep max (1RM).

Outcome Measures: VO2peak, Graded exercise test (GXT); assessed at baseline and at end of treatment (12 wks)

1.     Significant effects of both modes of training (RT and ET) in the physiological responses to peak GXT were observed.2.     Muscular strength significantly increased for all exercise maneuvers in the RT group with no changes detected in the ET group

3.     VO2peak values were significantly greater after RT (15.1%) and ET (11.8%).

4.     Both RT and ET study groups displayed significant increases in Ppeak and Pmean .

5.     Mean power increased 8% and 5% for the RT and ET groups, respectively, with no statistically significant differences apparent between groups. RT produced significantly greater gains in Ppeak (15.6%) compared with ET (2.6%).

6.     The RT group displayed significantly increased strength values ranging from 34% to 55% for the six exercise maneuvers. In contrast, the ET group did not display increases in muscular strength for any of the six exercises after 12 wks of training.

Harness et al 2008USA

Prospective Controlled Trial

Initial N=31, Final N=29

Population: Intense Exercise Group: Mean age: 37.8±3.6 yrs;  Gender: 18 males, 3 females; Severity of Injury: ASIA A or B (12), ASIA C or D (9) Control: Mean age: 34.5±2.9 yrs; Gender: 8 malesTreatment: Treatment group – multi-modal intense exercise program; Control group – self-regulated exercise.

Outcome Measures: Medical Research Council scale (muscle strength)

1.   At least one muscle increased in strength over 6 months in 15/21 treatment participants compared to 0/8 control participants (p<0.0001); in these 15, the mean number of muscles showing a change was 4.1 (3.2 in lower extremities).
Bjerkefors et al. 2006Sweden

Downs & Black score=20

Pre-Post

N=20

Population: Traumatic SCI: SCI Group: Mean age: 38±12 yrs; Gender: 14 males, 6 females: Mean body mass: 70.8±13.9 kg: Reference Group: Mean age: 35±10 yrs; Gender: 7 males, 3 females; Mean body mass: 76.5±12.7 kgTreatment: 10-wk period of kayak ergometer training using commercially available kayak ergometer (Dansprint, I

Bergmann A/S, DK). Every week subjects completed 3×60 min training sessions of kayak ergometer training.

Outcome Measures: Shoulder muscle strength

1.     There was a main effect of kayak ergometer training with increased shoulder muscle strength (in the beginning and middle positions and independent of shoulder movement) after training in persons with SCI.2.     There was no interaction between training, movement and angular position or between training and movement, but an interaction was observed between training and angular position.

3.     The SCI group had less shoulder muscle strength compared to the reference group but the difference was not statistically significant to draw conclusions.

Hartkopp et al. 2003Denmark

Downs & Black score=20

Prospective controlled trial

N=18

Population: HR: Age (range): 29-55yrs; Gender: 8 males, 4 females; Level of injury: C-5/6; Time post-injury (range): 5-38 yrs; LR: Age (range): 32-44yrs;Time post-injury (range): 4-27yrs

Treatment: Wrist extensor muscles were stimulated (30min/d, 5 d/wk for 12 wks) using either a high-resistance (HR group) or low-resistance (LR group) protocol.

Outcome Measures: strength and endurance of contractile properties, muscle metabolism, fatigue resistance measured at baseline and 12wks

1.     Maximum voluntary torque increased in the Hr group (p<0.05), but not the Lr group.2.     For the Hr group the electrically stimulated peak tetanic torque increased only at 15Hz (p<0.1), and the Lr group remained unchanged.

3.     Resistance to fatigue increased (p<0.05) in both the Hr (42%) and Lr (41%).

4.     For the Hr group, the cost of contraction decreased by 38% (p<0.05) and the half-time of phosphocreatine recovery was shortened by 52% (p<0.05).

5.     Electrical stimulation of the wrist increases fatigue resistance independent of the training pattern, but only in the Hr group does increased muscle strength improve aerobic metabolism after training.

Griffin et al. 2009USA

Downs & Black score=19

Pre-Post

N=18

Population: Traumatic SCI: Mean age: 40±2.4 yrs; Gender: 13 males, 5 females; Mean time post-injury: 11±3.1 yrsTreatment: FES cycling performed on an Ergys2 automated recumbent bicycle 2–3 d/wk for 10 wks

Outcome Measures: AIS scores

1.     Training week had a statistically significant effect on the ride time without manually assisted pedaling. Ride times during training weeks 5–10 were statistically greater than during week 1.2.     Lower extremity total AIS scores and the motor and sensory components of the AIS test were all significantly higher following training

3.

Durán et al.2001

Colombia

Downs & Black score=16

Pre-post

N=13

Population: Paraplegia; Age (range): 17-38yrs; Gender: 12 males. 1 female; Severity of injury: ASIA A (85%), ASIA B (7.5%), ASIA C (7.5%); Time post-injury (range): 2-120 moTreatment: 16 wk exercise program (4 wks  adaptation, 1 wk  enhancement, 11 wks specific program (3d/wk, 120 min/session) including mobility, coordination, strength, aerobic resistance and relaxation exercises.

Outcome Measures: Max. strength of upper limbs: max. weight mobilized in one trial or number of reps in 30 sec; Progressive resistance arm crank test: 3 min warm up @ 0 watts, resistance ↑ every 2 min; done pre & post program.

1.   Weight lifted pre-program vs. post-program:·       Bench press – 46% ↑,  42.7 vs. 62.5 (p=0.0001)

·       Military press – 14% ↑, 60.0 vs. 68.3 (p=0.0002)

·       Butterfly press- 23% ↑, 52.3 vs. 64.2 (p=0.0001).

2.   Repetitions pre-program vs. post-program:

·       Biceps (dumbbell) – 10%↑, 26.7 vs. 29.4 (p=0.0001)

·       Triceps (dumbbell) – 18% ↑, 35.8 vs. 42.4 (p=0.0001)

·       Shoulder abductors- 61% ↑, 8.8 vs. 14.2 (p=0.0001)

·       Abdominal in 1′ – 33% ↑, 47.0 vs. 62.4 (p=0.009)

·       Curl back neck – 19% ↑, 112.3 vs. 134.0 (p=0.0001)

3.   Arm Crank Test:

·       Max. resistance ↑ from 90 watts to 110 watts post-program (p<0.001).

Nash et al. 2007

USA

Downs & Black score=16

Pre-post

N=7

Population: Chronic Complete Paraplegia; Age (range): 39-58 yrs; Gender: 7 males; Mean time post-injury: 13.1 yrsTreatment: Circuit resistance training (CRT), 45/min, 3d/wk on non-consecutive days for 16 wks.  Training consisted of low-intensity endurance activities, circuit resistance training, military press, horizontal rows, pectoralis (horizontal row), preacher curls, wide-grip latissimus dorsi pull-downs, and seated dips.

Outcome Measures: Wingate Anaerobic test (power assessment); Strength testing; all @ baseline & 16 wks.

1.   Anaerobic power:·       6% ↑ in  peak power (p=0.005)

·       8.6% ↑ average power (p=0.001).

2.   Strength:

·       ↑ on all maneuvers from 38.6% to 59.7% (p<0.001).

Jacobs et al. 2001

USA

Downs & Black score=15

Pre-post

N=10

Population: Chronic Paraplegia; Mean age: 39.4 yrs; Gender: 10 males; Mean time post-injury: 7.3 yrsTreatment: 12wk training program – 40-45 min/session, 3d/wk on non-consecutive days. Sessions included resistance training (weight lifting) and endurance training (arm cranking).

Outcome Measures: Isoinertial strength testing; Isokinetic strength testing; @ baseline 4, 8 & 12 wks.

1.   16.1% ↑ peak power output (p<0.05).2.   Isoinertial strength:

·       Mean 21,1% ↑ after 12 wks (p<0.01)

·       Improvements noted every month.

3.   Isokinetic strength:

·      ↑ after 12 wks for the shoulder joint internal rotation, extension, abduction, adduction & horizontal adduction (p<0.05).

Petrofsky et al. 2000

USA
Downs & Black score=13

Prospective controlled trial

N=90 (9/group)

Population: Paraplegia; Mean age: 24.9 yrs; Gender: 90 malesTreatment: 10 wk training period – consisted of electrical stimulation of quad muscles with 10 groups examining different variations of session length, frequency of sessions and length of flexion-extension cycle used in exercise program.

Outcome Measures: Isometric strength; 3 experiments were designed looking at: 1) the effect of the length of the training session on performance; 2) the number of days of training/wk on performance; 3) the effect of the length of the extension-flexion cycle on training

1.   Length of training session:·       Greatest ↑ in work capacity in group training for 30min/day vs. 5 or 15 min/day (p<0.01).

·       30 min/day group: rate ↑ of training was more rapid.

·       Quad muscle strength was greater in 30 min/day group than others

2.   Number of days training/wk:

·       Working out 3 days/wk benefitted more than those that worked out for 1 day/wk or 5 days/ wk.

·       Those that worked out 3 & 5 days/wk were significantly more improved (p<0.01).

·       3 days/wk had greater isometric strength in the quads.

3.   Length of extension-flexion cycle:

·       ↑ training effect was assessing training by total work which would be done over the 30 min pd.

Gregory et al. 2007

USA

Downs & Black score=11

Pre-post

N=3

Population: Chronic SCI: Age (range): 22-61 yrs; Gender: 3 males; Level of injury: tetraplegia (2), paraplegia (1) Severity of injury: ASIA D (100%); Time post-injury (range): 17-27 yrsTreatment: 12 wks of lower extremity resistance training in combination with plyometric training (RPT) (2-3 d/wk for 30 sessions)

Outcome Measures: Muscle max cross-sectional area (max-CSA) of knee extensor (KE) & plantar flexor (PF) – MRI; Peak isometric torque, time to peak torque (T20–80), torque developed in initial 220 ms of contraction (torque 220) & mean rate of torque development (ARTD) -Dynamometry; Voluntary activation deficits.

1.   Peak torque production improved following RPT in KE (M=28.9%) & PF (M=35%).2.   ↓ T (20-80), ↑ torque (220) & ↑ mean rate of torque development in both muscle groups.

3.   PF & KE voluntary activation deficits ↓ following RPT.

Cameron et al. 1998USA

Downs & Black score=9

Pre-post

N=11

Population: Chronic SCI: Age (range): 18-45 yrs; Gender: 10 males, 1 female; Level of injury: C4-C7Treatment: Testing of hybrid device, 8 wks of neuromuscular stimulation-assisted exercise with training sessions 3d/wk.

Outcome Measures: Manual muscle test scores biceps, triceps, wrist flexors and extensors.

1.   All subjects showed improvement in one or more of their manual muscle scores, with the most dramatic occurring in the triceps (mean ↑ 1.1 for L triceps, 0.7 for R triceps)2.   Results show neuromuscular stimulation in combination with resistive exercise can be used safely and assists in the strengthening of voluntary contractions

Discussion

Muscle Morphology

A variety of benefits related to gross muscle morphology have been demonstrated in numerous investigations employing multi-week progressive exercise programs of FES-assisted cycling in which lower limb muscles (i.e., typically quadriceps, hamstrings and gluteal muscles) are stimulated to produce cycling movements against resistance (Sloan et al. 1994Hjeltnes et al. 1997Mohr et al. 1997Chilibeck et al. 1999Scremin et al. 1999Crameri et al. 2004Heesterbeek et al. 2005Griffin et al. 2009). Each of these FES-assisted cycling programs consisted of a minimum of three 30 minute sessions per week with program duration ranging from 8 weeks to 1 year with progressive resistance customized to the individual participant. Of note, Heesterbeek et al. (2005) employed a hybrid FES-assisted cycling protocol in which upper limb cycling was also incorporated into the physical activity intervention and Scremin et al. (1999) had a 4 phase intervention in which the final phase consisted of adding upper limb ergometry to FES-assisted lower limb cycling. These were the only investigations that incorporated upper body exercise although outcome measurement was limited to the muscles of the lower limb. All studies, other than that conducted by Crameri et al. (2004), were uncontrolled investigations incorporating either a prospective pre-post or retrospective case series study design. In addition, all of the studies were relatively small with sample sizes of 18 persons or less. Benefits to gross muscle morphology consisted of significant increases in total body lean muscle mass (Griffin et al. 2009), thigh muscle mass (Mohr et al. 1997), cross-sectional area of overall thigh muscle (Sloan et al. 1994Hjeltnes et al. 1997Scremin et al. 1999) and overall thigh volume (Heesterbeek et al. 2005) as well as significant reductions in muscle atrophy (Mohr et al. 1997). Significant increases were also seen in overall cross-sectional area or mean muscle fibre cross-sectional area within individual muscles (Chilibeck et al. 1999Scremin et al. 1999Crameri et al. 2004).

Other forms of neuromuscular electrical stimulation resistance exercise training have also been shown to produce beneficial muscle adaptations. In a relatively large study, persons with complete denervation due to a conus or caudal lesion (n=20 completing) underwent a two year home-based progressive electrical stimulation program which culminated in 30 minute sessions, 5 days/week involving a combination of twitch and tetanic stimulation patterns focusing on quadriceps but also on gluteal, hamstring and other lower limb muscles (Kern et al. 2010). Quadriceps and hamstring muscle cross-sectional areas were significantly larger with training with these results being more pronounced for the quadriceps. Similarly, significant increases in quadriceps muscle cross-sectional areas were produced in 5 males with ASIA A SCI with a home-based, two day/week program over twelve weeks in which four sets of ten unilateral, dynamic knee extensions were elicited by appropriate stimulation (Mahoney et al. 2005). A later report extended these observations with similar results following 18 weeks (Sabatier et al. 2006).

Other modes of endurance-based resistance exercise also led to similar muscle adaptations. For example, sustained participation in body weight support treadmill training 2 or 3 times/week resulted in significant increases in overall muscle cross-sectional areas in the thigh and lower leg muscles (Giangregorio et al. 2005Giangregorio et al. 2006Carvalho et al. 2008) as well as increases in mean individual muscle fibre sizes (Stewart et al. 2004) and partial reversal of muscle atrophy (Giangregorio et al. 2006). Of note, Carvalho et al. (20082009) conducted a controlled trial (n=15) which showed significantly greater increases in MRI-derived quadriceps cross-sectional area with neuromuscular stimulation combined with body-weight supported treadmill gait training as compared to that seen with conventional physiotherapy. This was conducted over a 6 month period after which the gait training was offered to the control group. Gait training sessions consisted of 20 minute sessions at a frequency of twice per week.

To this point, of all studies noted in this section, each of the interventions were applied to individuals with chronic SCI (i.e., > 6 months post-injury) with the exception of Giangregorio et al. (2005) who performed body weight support treadmill training on those more newly injured (i.e., 2-6 months post-injury). In addition, across studies participants had mostly complete or in rare instances near-complete SCI (i.e., AIS A, B or C).

A novel methodology was employed by Crameri et al. (2004) to investigate the effects of load on these types of muscle adaptations. These investigators used a 45 minute/day, three day/week FES-assisted cycling exercise protocol over ten weeks in which only one leg of each study participant was permitted to cycle against minimal load. The contralateral leg was also provided similar stimulation parameters as the “cycling” leg but these were applied against a fixed load so as to provoke rhythmic isometric contractions of the quadriceps and hamstrings against resistance. Exercise progressions were implemented with increases to the work-rest cycle and not to resistance as is often done in trials of FES-assisted cycling ergometry. This controlled investigation demonstrated that the amount of resistance is important in producing a training effect as greater increases in isometric force generation and muscle fibre cross-sectional area were demonstrated for the static, high-resistance training condition.

Additionally, muscle biopsies have been performed before and after training, permitting investigation of the effects of physical activity on fibre type. Following SCI, (especially in those with complete or near complete lesions), there is an established transformation of muscle fibres away from type IIa toward type IIx fibres reflecting a functional shift towards less aerobic, more easily fatigable muscle (Grimby et al. 1976Round et al. 1993). This shift was reversed over ten weeks (Crameri et al. 2002) and also at 6 months of a 1 year program (Andersen et al. 1996) of three day/week FES-assisted cycling exercise and with six months of three day/week body weight-supported treadmill training (Stewart et al. 2004) as each of these studies reported an increase in type IIa fibres and a corresponding reduction in type IIx (or IIb) fibres following training. More interestingly, similar results were seen in Crameri et al.’s 2004 investigation of the effect of static load vs. dynamic minimal load conditions with shifts of type IIx to type IIa muscle fibres apparent for both conditions along with the additional finding of a significantly greater increase in type I fibres only for the static, high-resistance trained leg. This represents an even more dramatic adaptation toward the aerobic, oxidative capacity of muscle with this type of training. Kern et al. (2010) demonstrated similar findings with their home-based neuromuscular stimulation promotion with increases in muscle fibre size that reverses the atrophic processes noted in denervated muscle.

There is also some evidence that passive cycling using upper-body assistance to drive paralyzed leg muscles involving 2 day/week sessions over 12 weeks may be sufficient to prevent these inactivity-related shifts towards more “fast” type muscle fibers. Willoughby et al. (2000) demonstrated significant increases in mRNA expression for type IIa fibres (and also for type IIx fibres) in the presence of decreasing proteolytic activity typically associated with muscle degradation. This passive exercise was insufficient to produce a significant increase in muscle size as indicated by no change in thigh girth and it is important to note that the leg movement required upper body voluntary exercise.

Strength and Muscular Endurance

In contrast to those investigations assessing outcomes related to muscle morphology, those assessing strength or muscular endurance were much more diverse with respect to the exercise modes employed. Notably, seven investigators incorporated RCT study designs (Needham-Shropshire et al. 1997Hicks et al. 2003Hartkopp et al. 2003Glinsky et al. 2008Jacobs 2009Alexeeva et al. 2011Mulroy et al. 2011) despite the acknowledged difficulty in fully implementing such features as participant blinding with the physical activity interventions typically associated with this design (Ginis and Hicks 2005).

Of these RCTs, six of seven trials resulted in statistically significant increases in strength, although there were different training paradigms used to achieve these results across the trials. Needham-Shropshire et al. (1997) used a paired-randomization approach to assign subjects with chronic cervical SCI (n=27) to one of three groups: 1) those receiving 8 weeks of neuromuscular stimulation-assisted arm ergometry exercise (NMS); 2) those receiving 4 weeks of NMS assisted exercise followed by 4 weeks of voluntary arm crank exercise; and 3) those participating in a control condition – voluntary exercise for 8 weeks without the application of NMS. Muscle strength was assessed by manual muscle testing in the triceps and the largest treatment effect (i.e., more muscles showing an increase of at least one muscle grade) was seen in Group 1 subjects (p<0.0005) although there were also a significant number of muscles that demonstrated an increase in muscle grade in Group 2 (p<0.03) relative to the control condition. In a pre-post study, Cameron et al. (1998) used a prototype of the NMS-assisted arm crank ergometer used by Needham-Shropshire et al. (1997) to elicit significant improvements to triceps muscle strength following a three days/week upper body training program conducted over eight weeks.

These results are consistent with those reported by Hicks et al. (2003) who conducted an RCT (n=34, with 11 of 21 completing in the exercise group) of a twice weekly progressive voluntary arm ergometry cycling and resistance training exercise program with sessions of 90-120 minutes over nine months. These investigators noted significant increases (p<0.05) in muscle strength for 3 different upper body maneuvers involving triceps, biceps and anterior deltoid bilaterally at nine months as compared to baseline, although these increases in muscle strength showed progressive improvement over the nine months.

Similarly, Mulroy et al. (2011) implemented an exercise/movement optimization initiative in which participants received a shoulder home exercise program consisting of a stretching phase, warm-up phase, and a resistive shoulder exercise phase 3 times/week for 12 weeks. There were statistically significant strength gains in all motions tested (elevation in the plane of the scapula, adduction, internal rotation, and external rotation) compared with the control group (p<0.01). Also, all muscle groups, for those in the intervention group, demonstrated increases in maximal torque production as measured by the Micro-FET handheld dynamometer following the intervention (p<0.05).

Alexeeva et al. (2011) compared two body-weight-supported (BWS) training devices; fixed track and treadmill and comprehensive physical therapy for improving walking speed. One of the secondary outcomes measured was muscle strength as determined by the ASIA International Standard Manual Muscle Test. The training program for all participants included 1 hour/day, 3 days/week for 13 weeks. There was a statistically significant increase in muscle strength across all groups (p<0.01), but no differences between groups. There was a mean increase of 6-9% in muscle strength across all three groups.

Jacobs (2009) compared a resistance training paradigm involving 3 sets of 10 repetitions across six stations at 60-70% of a maximal single effort vs endurance training for 30 minutes involving arm cranking at 70%-85% of peak HR in persons with neurologically complete paraplegia (n=18). There were 3 sessions/week over a 12-wk training period with standardized exercise progressions for both the resistance training and endurance training groups and participants were matched between groups by body mass and gender. Muscular strength was significantly increased (p<0.01) with resistance training for each of the 6 isotonic strength testing maneuveurs corresponding to those involved for each of the resistance training stations. There were no strength changes apparent for those in the arm ergometry group (i.e., endurance training). However, muscular endurance, as indicated by performance on the Wingate anaerobic power test, was significantly improved with both forms of training, although these improvements were most pronounced with resistance training.

Harness et al. (2008) implemented an intense exercise (IE) initiative that included 6 categories (active assistance, resistance training, load bearing, cycle ergometry, gait training/supported ambulation, and vibration training). The intervention group participated in the exercise program for an average of 56 ± 6 days and 7.3 ± 0.7 hours per week over a six month time period. The results demonstrated that 15/21 subjects had increased muscle strength in at least one muscle with a mean of 4.1 muscles (3.2 lower extremities) compared with 0/8 subjects in the control group (p<0.0001). Muscle strength was measured as a secondary outcome to motor function.

The RCT conducted by Glinsky et al. (2008) failed to show statistically significant increases in strength or muscular endurance (i.e., fatigue resistance) in wrist extensor or flexor muscles that were at least partially paralyzed in persons with tetraplegia (n=32). There was an overall mean increase of 8% and 11% in strength and muscular endurance respectively with training vs no training groups but this was deemed clinically insignificant. This study involved a resistance training program involving 3 sets of 10 repetitions using a customized device that permitted those with even minimal force generation to participate in a progressive exercise program. These authors noted that unlike other trials (e.g., Hicks et al. 2003), all participants had at least some paresis although it should be noted that there was a slight imbalance between experimental (i.e., training) vs control (i.e., no training) groups with respect to a slightly greater impairment in participants in the training group (i.e., 9 vs 6 persons with ASIA A and 4 vs 0 persons with an initial muscle grade of 2).

A similar training system to that employed by Glinsky et al. (2008) was used by Hartkopp et al. (2003) to examine the effect of electrical stimulation on strength and fatigue resistance in wrist extensor musculature in persons with tetrapegia (n=12 completing trial). This RCT used the non-trained arm as a control and demonstrated significant strength gains with a high resistance protocol, but not a low resistance protocol – each involving 5, 30 min sessions/week over 12 weeks. The high resistance protocol consisted of stimulation against a maximal load, whereas the low resistance protocol used a resistance of 50% of maximal load. Both training protocols were effective in improving resistance to fatigue.

There were also several investigations involving mostly pre-post study designs resulting in improved muscle function with different forms of electrically-stimulated exercise. For example, FES-assisted cycling programs involving the lower limbs and of varying durations and frequencies have demonstrated beneficial effects on muscle function. Griffin et al. (2009) demonstrated improved ASIA motor (and sensory scores) for the lower extremity following FES cycling for 2-3 times per week over 10 weeks in a group of persons with mostly incomplete SCI from C4-T7 (i.e., 13 of 18 with incomplete SCI). In persons with complete chronic SCI, FES-assisted cycling is effective for improving resistance to muscular fatigue as indicated by increases to sustained torque generation with repetitive stimulation in programs employing as little as 3, 30 min sessions/week over 6 weeks (Gerrits et al. 2000). A more extensive long-term program involving 5, 1 hour sessions/week over 1 year also was effective in improving fatigue resistance as well as producing a fivefold increase in maximal electrically stimulated torque (i.e., strength of contraction), although this remained lower than in able-bodied individuals (Duffell et al. 2008). Interestingly, in a later study, Gerrits et al. (2002) demonstrated that fatigue resistance was improved more effectively by low frequency (i.e., 10 Hz) vs high frequency (i.e., 50 Hz) stimulation, although each was equally effective in improving force generation (i.e., tetanic tension development).

In addition, several investigators have employed other approaches to lower limb neuromuscular stimulation such as the long-term home-based stimulation program by Kern et al. (2008) which resulted in a near ten-fold increase in stimulation-elicited muscle force in addition to the benefits to muscle morphology noted above. Sabatier et al. (2006) conducted a smaller pre-post study (n=5 persons with complete SCI) of an eighteen week home-based neuromuscular electrical stimulation resistance training program involving bi-weekly quadriceps training comprised of four sets of 10 dynamic knee extensions against resistance while in a seated position. This resulted in significant increases in strength (i.e., weight lifted), as well as a 60% reduction in muscle fatigue (p = 0.001).

Given the results of these studies, it is clear that there are a variety of approaches involving neuromuscular stimulation to the lower limb that accrue benefits to muscle function. However, information regarding the minimum requirements with respect to frequency, intensity, duration of a training program and how each of these might interact with different patient subgroups remains to be definitively established. Interestingly, Petrofsky et al. (2000) conducted a study to assess the effect of altering various parameters associated with a ten week training program of quadriceps muscle stimulation. These investigators assigned subjects (n=90) to 10 different treatment groups and examined the effect of altering some of the parameters associated with individual treatment sessions. Greater strength changes were seen for 30 minute sessions as compared to 5 or 15 minute sessions and for 3 day/week training as compared to 1 or 5 day/week training programs. In addition, strength gains and total work capacity was optimized by incorporating a pattern of 3 s extension – 3 s flexion – 6 s rest as compared to longer or shorter durations of work-rest cycles. Several investigations of voluntary exercise employing pre-post study designs have demonstrated strength benefits (in addition to other benefits). These studies have been conducted mostly in persons with paraplegia and have included circuit resistance training for 3 days/week (Durán et al. 2001Jacobs et al. 2001Nash et al. 2007), a combination of resistance training and plyometric training (Gregory et al. 2007) and 3, 60 minute sessions/week of kayak ergometer training over 10 weeks (Bjerkefors et al. 2006).

Conclusions

There is level 2 evidence from a single study with support from several level 4 studies that an appropriately-configured program of functional electrical stimulation of lower limb muscles in persons with SCI produces muscle adaptations such as increasing individual muscle fibre and overall muscle size and may result in the prevention and/or recovery of muscle atrophy.

There is level 2 evidence from a single study with support from several level 4 studies that an appropriately-configured program of functional electrical stimulation of lower limb muscles in persons with SCI results in an increase in muscle fibre types with more aerobic (endurance) capabilities, (most notably a shift in type IIx to type IIa muscle fibres).

There is level 1 evidence from a single RCT with support from a single level 4 study that functional electrical stimulation-assisted upper limb cycle ergometry is capable of producing significant increases in upper limb muscle strength in persons with tetraplegia.

There is level 2 evidence from a single RCT that voluntary upper limb cycle ergometry is capable of producing significant increases in upper limb muscle strength in triceps, biceps and anterior deltoid in persons with SCI.

There is level 1 evidence from two RCTs that voluntary upper limb resistance exercise is effective in increasing upper limb muscle strength in persons with paraplegia.

There is conflicting level 1 evidence across two RCTs that electrical stimulation-assisted resistance training of paretic wrist extensors or flexors increases strength and fatigue resistance in persons with tetraplegia.

There is level 1 evidence from a single RCT that body-weight supported fixed track or treadmill training can increase muscle strength in persons with SCI. There is also level 4 evidence from three studies that suggests that body-weight supported treadmill training in persons with SCI produces muscle adaptations of increasing individual muscle fibre size and overall muscle size and may result in the prevention and/or recovery of muscle atrophy.

There is level 2 evidence from a prospective controlled trial and level 4 evidence from several pre-post studies that circuit resistance training and other forms of resistance training combined with other approaches may increase upper limb muscle strength in triceps, biceps and anterior deltoid in persons with tetraplegia and/or paraplegia.

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