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Systematic Review of the Exercise or Health-Related Benefits of FES Cycling and Locomotor Training Approaches after SCI 1989-2009

Conducted by the Shepherd Center with support from the National Institute on Disability and Rehabilitation Research.


Table of Contents

Plain language summary
Methods and procedures
Results and conclusions
Acknowledgements and statement concerning conflict of interest

The Activity-Based Interventions to Improve Health systematic review and narrative synthesis involved collecting and grading research information for rigor and meaning. The Shepherd Center Systematic Review Group utilized the system for grading research in terms of rigor and meaning developed by the BU Supported Housing Study Group (Farkas, Rogers and Anthony, 2008). The Shepherd Center Group used the same instruments, the first being: “Standards for Rating Program Evaluation, Policy or Survey Research, Pre-Post and Correlational Human Subjects” (Rogers, Farkas, Anthony & Kash, 2008) and the second: “Standards for Rating the Meaning of Disability Research” (Farkas & Anthony, 2008). The lead author of the Activity-Based Interventions to Improve Health is Deborah Backus. A full listing of contributors is contained in the section “Contributors”.

Plain language summary

The average life expectancy of people with spinal cord injury (SCI) has continued to increase over the past 25 years, although it remains lower than that found in people without neurological injury or disease.  This increase in the lifespan, however, brings with it other issues that require attention in people with chronic SCI.  Namely, people with chronic SCI not only experience a decrease in mobility and challenges to their daily life, they also are at risk for other conditions that increase the potential for greater health problems.

Cardiovascular disease (CVD) is the leading cause of death in the able-bodied American population.  People with SCI are at an even greater risk of CVD due to an increase in the factors associated with the development of CVD.  Some estimates report that over 20% (22.4%) of all deaths among people with SCI are caused by, or exacerbated by, CVD.  Several factors increase the risk of CVD in persons with SCI above those in people who do not have neurological injury or disease, including level and extent of injury, decreased physical activity, poor nutritional habits, changes in muscles, lipid disorders, and insulin resistance and obesity.

Exercise has been shown to reduce the CVD risk factors in both those without injury and those with SCI.  However, getting adequate exercise to combat CVD is difficult after SCI.  The predominant mode of exercise for this population requires use of their arms and using the arms poses a problem. This problem is due to several issues.  One issue is that persons with SCI are already placing a lot of stress and demand on their arms with every day activities, such as transferring to and from their wheelchair, pushing their wheelchair, or even using crutches if walking is an option.  In addition, the arms are comprised of small muscles, and may not be able to exercise at a level to induce the cardiac, vascular and muscular stress required to elicit meaningful change in the risk factors associated with CVD.  Finally, the arms themselves may be further incapacitated by paralysis and weakness in people with cervical SCI, making it more difficult to exercise at an intensity required for inducing cardiovascular, metabolic and lipid-related changes.  Exercise that uses the larger muscles of their legs would:

  • provide an avenue for placing a demand on the heart, lungs, and mucles;
  • potentially decrease the risks associated with SCI and the subsequent decrease in mobility; and
  • spare the arms unwarranted stress.

Activity-based interventions have received a lot of attention recently, primarily in relation to their putative effects on neural and functional plasticity after SCI.  These interventions include cycling with functional electrical stimulation (FES cycling) and locomotor training approaches, such as robotic locomotor training and manual locomotor training.  The high intensity of these activities and their potential to activate the large muscles of the legs, make these interventions viable options for obtaining the amount and intensity of exercise that may reduce the presence of the risk factors associated with CVD.

This review evaluated the literature related to the health and exercise benefits of FES cycling and locomotor training interventions.  Eighteen articles published between 1989 and 2009 were identified, based on their meaningfulness to persons with SCI, their caregivers, medical and health providers, and payers.  Additionally, these articles were identified based on the scientific rigor of the studies, i.e. how well the research was conducted.  All studies reviewed evaluated some form of health- or exercise-related outcomes in persons with SCI who participated in training or testing on either the FES cycle or locomotor training.

FES cycling involves a person cycling using a lower extremity ergometer or bike with the assistance of electrical stimulation to the lower extremity muscles, typically the gluteal, quadriceps and hamstring muscles.  In some cases there is a motor that assists the cycling, but in other, especially earlier cases, trained personnel assist the cycling motion until the leg muscles are stimulated adequately to cause the muscle contraction.

Locomotor training approaches include both robot- and manually-assisted body-weight supported treadmill training (BWSTT); both approaches involve the participant walking with weight support via a harness over a treadmill.  Manual assistance is provided in manually-assisted BWSTT, meaning that trained personnel facilitate stepping movements and pelvis motion during walking on the treadmill.  In robot-assisted BWSTT, a computer controlled orthosis supports and assists motions of the legs while the person steps on a treadmill.

The vast majority of the studies reviewed related to the effectiveness of FES cycling (n=10) for health-related outcomes in persons with either acute or chronic (greater than one year post-SCI), complete (no motor or sensory function below the level of injury) or incomplete (some sensory and/or motor function below the level of injury) tetraplegia or paraplegia.  The remainder (n=8) evaluated the effectiveness of locomotor training approaches, i.e. robot-assisted BWSTT, or manually-assisted BWSTT.

“Exercise effects” include changes or modifications in cardiorespiratory (heart and lungs) or vascular (blood vessels, i.e., arteries, and veins) responses, metabolism (providing energy in the body), and muscle parameters (size, girth, volume, blood flow, metabolism).  “Health-related benefits” includes measures of cardiac (heart) function and indicators of cardiac disease, metabolic function and indicators of diabetes or other metabolic instability or disease.

Twelve of the 18 studies evaluated the effects of FES cycling and BWSTT on cardiorespiratory function, four on vascular health, six on muscle morphology change pre and post intervention, and six on metabolic function.  Of these 18 studies, 14 were performed in persons with chronic (greater than one year post-SCI) SCI, two were in those with acute injury, and two included persons with both chronic and acute SCI.  The vast majority of participants in these studies were male, but several studies also included females.  Only two of the 18 studies were performed in children, and these both evaluated the impact of FES on health-related variables.

The findings from these studies suggest that training with the FES cycle for durations as short as 12 weeks, or as long as 6 months can lead to cardiorespiratory and muscle benefits, as well as vascular improvements, in persons with both chronic and acute, complete or incomplete, tetraplegia or paraplegia.  In fact, even persons with complete injury obtain health-related benefits from FES cycling.  FES cycling early after injury (less than one year) does not appear to be harmful to the muscles, as was demonstrated in the two studies that were conducted in persons with acute SCI.  The muscle size increased, potentially preventing and overcoming the early onset muscle atrophy reported in persons with SCI.  Finally, persons with tetraplegia received benefits from exercising on the FES cycle, which is particularly meaningful given their high risk for cardiovascular disease.

The data from the BWSTT studies also support the use of this intervention to improve cardiorespiratory and muscle health in persons with chronic or acute, complete or incomplete injury.

Improving cardiorespiratory fitness is known to decrease the risk of CVD.  Increasing the size of muscle in persons with SCI may lead to better glucose tolerance, and therefore perhaps decrease the risk of diabetes in these persons, which may further decrease the risk of CVD.  Additionally, evidence is suggesting a decreased risk of pressure sores, decreased secondary complications and decreased mortality related to SCI in persons who exercise. Exercise may not only improve the overall health and well-being for persons with SCI, but may also decrease the cost and burden to society associated with chronic SCI.

There are some challenges to consider in a review of the literature on the health benefits of FES cycling and BWSTT interventions. First, the methods used in each study, namely the training paradigms and the outcome measures, differ, making it difficult to determine which training approach would be best for any particular person with SCI.  Secondly, these interventions have not included a cost-benefit analysis to determine if there are potential cost savings after providing the interventions. Such information would be meaningful to payers when making decisions in regards to equipment purchases and therapy to provide the interventions.    Further study is needed to determine the best exercise approach for any given person with SCI, based on their level and extent of injury, sex, chronicity of injury, and potentially other variables as well.  Persons with SCI who desire pursuing FES cycling or locomotor training approaches for exercise should consult with their physicians about the safest and potentially most effective approach for them.

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Lead Reviewer:

Deborah Backus, PhD, PT, Associate Director SCI Research

Shepherd Center
2020 Peachtree Rd, NW
Atlanta, GA. 30075

Shepherd Center Systematic Review Group:

Deborah Backus,
David Apple,
Lesley Hudson,
Rebecca Acevedo

Additional Reviewers:

David Apple, MD
Lesley Hudson, MS
Jennith Bernstein, PT
Amanda Gillot, OT
Ashley Kim, PT
Elizabeth Sasso, PT
Kristen Casperson, PT
Brian Smith, PT
Anna Berry, PT
Angela Cooke, RN

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AIS American Spinal Injury Association Impairment Scale
ASIA American Spinal Injury Association
BP Blood pressure
BWSTT Body weight supported treadmill training
C Cervical
CAD Coronary artery disease
CO Cardiac output
CSA Cross sectional area
CVD Cardioavascular disease
DBP Diastolic blood pressure
FES Functional electrical stimulation
FVC Forced vital capacity
HR Heart rate
MAP Mean arterial pressure
MHC Myosin heavy chain
NIRS Near infrared spectroscopy
NMES Neuromuscular electrical stimulation
O2 Oxygen
Para Paraplegia
RER Respiratory exchange ratio
SBP Systolic blood pressure
SCI Spinal cord injury
SV Stroke volume
T Thoracic
TPR Total peripheral resistance
VCO2 Carbon dioxide output
VO2 Oxygen uptake
VE Ventilatory exchange

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Rationale for the Review.

The average life expectancy of persons with spinal cord injury (SCI) has continued to increase over the past 25 years (NSCISC, 2009).  The cumulative survival rates of patients admitted into Spinal cord injury Model Systems of care have been reported to be 69.14% (20 year survival) and 51.97% (30 year survival) (NSCISC, 2009).  This longevity, however, actually predisposes persons with chronic SCI to health issues that are similar to the able-bodied population.

Cardiovascular disease (CVD) is the leading cause of death in the able-bodied American population, and in 2004, accounted for 36.3% (871,517) of all 2,398,000 deaths in the United States (Rosamond et al, 2007). The risk factors for CVD are listed in Table 1.  People with SCI are at an even greater risk of CVD (See Table 1, where the risk factors exacerbated by SCI are highlighted).  The risk of cardiac disease in SCI is influenced to a great extent by the level and extent of injury.  Persons with tetraplegia have a 16% increased risk of CVD, while those with paraplegia have an astounding 70% increased risk of coronary artery disease (CAD); those with a complete injury have a 44% increased risk of CVD (Groah et al 2007).  Some reports suggest that the leading cause of mortality in spinal cord injury (SCI) is cardiovascular disease (CVD) (Myers, Lee, Kiralti 2007).  According to the most recent report from the Spinal Cord Injury Model Systems (NSCISC, 2009), diseases of the respiratory system were the number one cause of death.  Regardless of the absolute ranking of these, i.e. respiratory or cardiac disease, in persons with SCI, it is clear that these are both important variables to address in this population in order to improve the health and well being in persons with chronic SCI.

The conditions that accompany SCI predispose these persons to obesity, diabetes, metabolic syndrome, and lipid disorders, all concerns in and of themselves.  Metabolic syndrome alone, “…a cluster of the most dangerous heart attack risk factors: diabetes and pre-diabetes, abdominal obesity, high cholesterol and high blood pressure” ( poses serious health related problems.  Metabolic syndrome is present in 23% of persons with SCI, and doubles the risk of CVD in these persons (Lee et al 2005).  In addition to these issues, persons with SCI are also at risk for lipid disorders, with elevated LDL and lowered HDL.  Persons with tetraplegia are at greater risk than those with paraplegia.  The risk factors for metabolic syndrome after SCI include insulin resistance, central obesity, genetics, and physical inactivity.  Studies in persons who do not have a neurological injury or disease, i.e. the able-bodied population, demonstrate that diet and exercise can in large part combat these conditions (Myers, 2003; Daubenmier et al. 2007).

In addition to these associated conditions, the sensory and motor manifestations of the SCI itself poses a significant health problem.  In a very short period of time after SCI, the loss of mobility, and forced inactivity, leads to significant physical deconditioning.  There are many well-documented and profound physiological changes, including severe muscle atrophy and changes in muscle morphology that begin very early after traumatic SCI (Castro et al 1999; Castro, et al 2000; Hicks et al, 2003), and continue to evolve over the course of the lifetime after SCI.  Although in part due to immediate histochemical changes, these alterations in the muscle are exacerbated by the forced inactivity (non-use) resulting from paralysis and weakness below the level of injury.

Finally, the sedentary lifestyle often imposed by SCI further increases the risk of the associated conditions (obesity, diabetes, metabolic syndrome, lipid disorders), and ultimately further decreases mobility, health and independence in persons after SCI.  People with SCI spend less than 2% of their time in physical activities and leisure time activities (Latimer et al 2006).  Given the number of people living in the US with significant disability resulting from SCI, finding and providing interventions that improve overall health and independence in persons with SCI is a critical need.

The benefits of exercise for people with SCI are in part the same as those for the able-bodied population, namely improved cardiovascular function, respiratory endurance and weight control (Hoffman 1986, Jacobs 2001, Nash 2005).  In addition exercise is particularly meaningful to persons with SCI, who need to be healthy and fit in order to meet the physical demands of every day life, since they already have diminished capacity and mobility due to their sensory and motor loss.  The typical mode of exercise for people with SCI tends to be through the use of the upper extremities, simply due to the fact that the lower extremities, if not paralyzed, are often too weak for sufficient exercise.  However, upper extremity exercise is stressful for the able-bodied population, and is even more so for persons with SCI.  This mode of exercise puts potentially dangerous stress on the heart.  Furthermore, depending on the arms to exercise, which are already under extra burden due to wheelchair use and transfers in persons with SCI, may lead to overuse injuries in the arms, and particularly the shoulders, leading to further disability in this already compromised population.  Upper extremity muscles may also be compromised, especially in those with tetraplegia.  Thusit may be difficult to use the arms adequately for exercise.

Activity-based interventions provide an intense way to exercise more muscle groups, and often larger muscle groups (i.e. the legs), since these interventions allow for activation not only of the muscles that are intact (e.g. the arms), but also those below the level of injury (legs and lower trunk), that may be weak or paralyzed.  The use of activity-based interventions to promote health may potentially lead to greater health benefits after SCI, and prevent secondary issues of pain and immobility in the arms. Activity-based interventions are often delivered with novel technologies.  Given that access to exercise equipment is often a problem for persons with SCI, technologies that provide a means to exercise in the home, or in public accessible gyms, may benefit more people.  Finally, given the focus on “recovery” and the tendency of people to pursue activity-based interventions to facilitate recovery and or prepare their body for if the “cure” is discovered, it behooves the SCI rehabilitation field to explore the potential health benefits for people who are partaking in this activity anyway.

Two of the most widely known and applied activity-based interventions are locomotor training approaches and FES cycling.  There is currently no consensus in the field related to the health benefits of these treatment interventions for persons with SCI.  If these interventions can be used to improve health (i.e. decrease weight, improve cardiorespiratory and vascular function, improve metabolic activity) in persons with SCI, the use of them may also decrease the long term health costs and mortality associated with chronic SCI.

Successful recovery and return to a happy and fulfilling life depends on how well these chronic conditions are managed.  Therefore, finding and providing interventions that will improve function, independence, health and well-being will presumably lead to the best possible outcome in terms of health and quality of life.  Beyond improving the persons’ quality of life, ensuring a mechanism for improving and maintaining good health in people with SCI is both a fiscal responsibility and an ethical obligation to thousands of persons with chronic SCI.

Objectives of the Review

The main objective of this review was to evaluate all literature over the last 20 years (1989-2009) related to the efficacy of activity-based interventions for improving health-related outcomes in persons with paralysis and sensory loss due to spinal cord injury (SCI). “Activity-based interventions” include any therapy activity that is focused on activating muscles below the level of injury rather than simply accommodating or compensating for the paralysis and sensory loss due to the SCI by using the intact limbs only.  Such interventions include electrical stimulation, cycling (with or without electrical stimulation), locomotor training (manual or robotic), intense strength training (with combinations of electrical stimulation or other facilitation), and resistance training.  Activity-based interventions do NOT include the use of electrical stimulation or robotics as neuroprosthetics, or tools to replace the lost function below the level of injury.  “Exercise effects” include changes or modifications in cardiorespiratory or vascular responses, metabolism, and muscle parameters (size, girth, volume, blood flow, metabolism).  “Health-related benefits” include markers related to cardiac function and indicators of cardiac disease, and metabolic function and indicators of diabetes or other metabolic instability or disease.

The assumption for this systematic review was that there is important and significant literature that has been published related to the efficacy of activity-based interventions (ABint) to improve health after SCI.  There are few random controlled trials in SCI in general, and even fewer randomized and controlled studies related to the efficacy of ABint for health-related benefits in SCI.  This study group, however, felt that the methods employed by the Supported Housing Study Group (E. Sally Rogers, Marianne Farkas, William Anthony, Megan Kash, Courtenay Harding, Annette Olschewski, at the Center for Psychiatric Rehabilitation) would be useful for examining the issue of ABint for health-related benefits in SCI in the existing literature.

The secondary objective of this review was to develop and disseminate products that will inform consumers related to SCI (patients, caregivers, clinicians, educators, administrators of programs and payers) about the efficacy of locomotor training approaches and FES cycling for improving health in persons with SCI.

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Methods and procedures

Overall, the methods employed for this systematic review were defined by the Supported Housing Study Group at the Center for Psychiatric Rehabilitation, and modified only slightly to accommodate the needs of the SCI field and the literature available in the SCI field.

The ABint study group included any study describing the effects of locomotor training and FES cycling on exercise and health-related outcomes after spinal cord injury (SCI).

Search terms used:

  • Activity-based (activity based) therapy, rehabilitation, exercise
  • Activity-dependent
  • Electrical stimulation, neuromuscular stimulation, Bioness
  • Resistance training, exercise
  • Locomotor training, Gait training
  • Upper extremity training, facilitation
  • Sensory stimulation
  • Muscle
  • Respiratory
  • Diabetes
  • Glucose intolerance
  • Cardiac, cardiac fitness
  • Health
  • Fitness

All terms were paired with spinal cord injury or SCI, paraplegia, tetraplegia and quadriplegia. The following websites/tools were explored with the search terms identified above:

  • Search engines:
    • Pubmed (Medline)
    • Google Scholar
    • Cinahl
  • Databases:
    • PEDro
    • Cochrane Reviews
    • The citations contained in each article for additional potential articles and reports

The following types of studies/publications/documents were included in the primary review:

  • Studies conducted in animal models (included instead as background)
  • Policy statements
  • Needs assessments
  • Instruments related to outcome measures
  • Therapy satisfaction or quality of life studies
  • Program models
  • Conceptual models
  • Process evaluations
  • Reviews (included instead in the background)

Although such documents, as well as conference proceedings, dissertations or government proceedings, are important for the field, they were not included since they could not be subjected to ratings for their rigor and their meaning. Articles that discuss activity-based interventions in patient populations other than SCI are not discussed here (Dromerick et al. 2006).

All studies published in the 20 years prior to the date of the systematic review (1989-2009) were included in this review.  Any evidence prior to these dates was deemed to be unacceptable, given the extent of changes in the field of SCI research in the past 20 years.  The review included papers from twenty years ago since some of the key literature started to come forward in the 1980’s and it would not have provided a complete picture of the health-related benefits if we did not include this literature in the review and discussion.

The lead reviewer queried the databases and located articles.  She scanned the titles and abstracts of articles for relevance to SCI, activity-based interventions and health-related outcomes.  If the title appeared relevant, the abstract was reviewed, and if it was deemed likely to meet inclusion criteria, the article was obtained.  A checklist of inclusion/exclusion criteria was completed for each article to facilitate tracking of articles screened; the article had to report on the use of either locomotor training or FES cycling in the SCI population, and had to include at least one outcome measure that assessed exercise- or health-related variables.

Once a complete list of articles for review was compiled, that list was sent to experts (Joy Bruce, Chris Gregory, Susie Harkema, George T. Hornby, Therese Johnston, Sarah Morrison, Mark Nash, Candy Tefertiller, Leslie VanHiel) in SCI rehabilitation and research.  We asked those experts to review the list to ensure that no relevant article or report was omitted. This step yielded 5 new citations that were not appropriate for review.

The following study designs were accepted for this review:

  • Experimental: Employed methods including a random assignment and a control group or a reasonably constructed comparison group;
  • Quasi-experimental: No random assignment, but either with a control group or a reasonably constructed comparison group;
  • Descriptive: Neither a control group, nor randomization, is used. These included case studies and reports, studies employing repeated measures, and Pre-post designs.

Studies that were poorly described, or poorly defined, planned and executed, were deemed too difficult to determine the study design.  The lead reviewer consulted two other reviewers when this was encountered, and if they were able to define the study design, the article was included.

Training of Reviewers

Three reviewers from a previous systematic review and 5 new reviewers were trained to assist in this systematic review.  All were persons affiliated with Shepherd Center, including the co-investigators of the SCI Model Systems grant, the Associate Director of SCI Research, and four clinicians. Training of the reviewers focused on the goals of this review, how to perform a systematic review (using the guidelines set forth by Rogers and Farkas), the kind of evidence indicating rigor in research, and the criteria that would be used to determine if an acceptable indicator that rigor and meaning had been achieved at each of the points on the respective rating scales. All persons were trained in the use of the rigor and meaning rating scales by reviewing each item in the scale and discussing the meaning of the item and the evidence that could be considered for each indicator.

Research articles were used as training devices by having each rater independently review articles and then discuss their ratings until agreement was achieved. Inter-rater reliability was established through two separate joint ratings of articles over the course of the review period.  Each reviewer independently reviewed the same article for both meaning and rigor, and then the group met as a whole to review these ratings.  When reviewers did not agree on a rating (the typical variation being only one point), these were discussed.  Consensus was achieved by the group in 100% of the cases where there was originally a discrepancy, and the lead reviewer did not need to intervene or request further review by an additional, outside reviewer.

The rigor and meaning scales ranged from a score of “1”, which corresponded to no rigor or meaning, respectively, to a score of “5”, which corresponded to excellent rigor or meaning, respectively.  All items for each scale were then tallied for an “overall meaning” and “overall rigor” rating.  For “overall meaning”, the highest score that could be reached was a “5”.  If all three sections had at least two indicators checked “yes”, the overall rating was Level 5; if all three sections have at least one indicator checked “yes”, the overall meaning was Level 4; if two out of three sections had at least one indicator checked “yes, the overall meaning was Level 3; if one out of three sections had at least one indicator checked “yes”, the overall meaning was Level 2; finally, if no sections had a “yes” checked, the overall meaning was Level 1.

“Overall Rigor” was determined first by the rating on the item that scored the overall methodology for the study:  “Study/research uses rigorous or sound research methods that allow the questions of interest to be addressed”.  Then the overall average score was compared to the rating on this item.  When there was a discrepancy, the lead reviewer examined the cause, and sought out an additional reviewer for that article.  The review from the original reviewer, the lead reviewer and the secondary reviewer were then compared, and the lead reviewer determined the overall score.  This happened for two articles in this review process.  Both articles were deemed not appropriate for this review and were not included in the analysis.

The articles that were deemed to be rigorous and meaningful were then summarized for this review.

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Results and conclusions

Summary of articles reviewed

Forty-nine articles were considered for review.  After various inclusion and exclusion criteria were considered, 23 articles were rated for rigor and for meaning. Of these, 18 met the criteria for both meaning and rigor, and are discussed further in this report.  Four of these 18 included studies that were not intervention studies, but instead were studies of the exercise responses to activity-based interventions in people with SCI.  They are included here since they explore the health-related benefits of ABint on an acute basis.

The majority of the articles reviewed were classified as descriptive (n=12).  The remainder were classified as quasi-experimental (n=4) and experimental (n=2) designs.

Adult vs. Pediatric

Only two studies reported on the findings in a pediatric client, and one report included adolescents, while the remaining only included adults (18 years or older).

Acute vs. Chronic

Of the 18 studies included in this review, the vast majority (n=14) were conducted in persons with chronic SCI (SCI for one year or longer).  The remainder were in persons with acute injury (n=2), or included persons with both acute and chronic injury (n=2).

Types of activity-based interventions included

The two most extensively studied ABint related to exercise and health benefits were FES cycling (n=10), and body weight supported treadmill training (n=8), either with manual or robotic assistance, and with or without neuromuscular electrical stimulation. 

Functional Electrical Stimulation Interventions
Experimental Design Studies

Tables 2 through 4 provide summaries of participant characteristics (Table 2), the intervention variables and descriptors (Table 3), and an overview of areas of outcome assessment (Table 4) for the FES cycling studies.  There were two studies that used a randomized controlled trial approach (Demchak et al. 2005, Johnston 2009).  One was performed in adults with SCI (Demchak et al. 2005), and the other in children with SCI (Johnston et al. 2009).

Demchak et al. (2005) performed the only RCT evaluating the effects of FES cycling on the musculature of adults with acute, motor complete SCI.  Persons with SCI were randomized into either a control group, or an intervention group that participated in 30 minutes of training, 3 days a week for 13 weeks.  These investigators also included a group of able-bodied persons, although the major comparisons were reported between the SCI exercise group and the SCI control group.

Outcome measures included average weekly power output (calculated by the training device, the Stimaster Clinical Ergometry System (Electrologic of America, Inc. Dayton, Ohio)), and needle biopsies of the vastus lateralis 4-6 weeks post-SCI, and then after one week of training on the FES cycle.  In order for the biopsies to be performed, the participants had to be able to tolerate sitting upright for 30 minutes; therefore, these measures were taken between 4 and 6 weeks post-SCI, given individual differences in tolerance. Nuclear density, fiber cross sectional area (CSA), and myosin heavy chain (MHC) composition were all computed from the biopsy findings.

All participants demonstrated improvements in power output (2.4 +/- 0.88 watts at initial testing to 24.5 +/- 3.2 watts at completion of training), and those in the SCI exercise group demonstrated increased power output by week 4.

Prior to the intervention phase, both SCI groups demonstrated a 36% decrease in muscle CSA when compared to the able-bodied control group.  Although there was no difference in muscle CSA between the SCI groups at baseline, the SCI exercise group demonstrated a non-significant 63% increase in muscle CSA after training (p=0.172), which was 171% greater than the CSA in persons in the SCI control group (p=0.05).  There was no difference between groups in terms of nuclear density and MHC composition at baseline, and no significant difference in nuclear density or MHC composition in the SCI exercise group.

The authors attribute the lack of change in nuclear density and MHC composition to the fact that these variables had not yet changed during this early stage of acute SCI, and therefore, there was no need or room for improvement at this point.  The changes in the muscle CSA are meaningful, suggesting that early intervention with FES cycling in persons with acute, motor complete (AIS A or B) tetraplegia or paraplegia not only does not appear to harm the muscle, but also may prevent the early onset of muscle atrophy, and increase the health of the muscle fibers.

Johnston et al. (2009) performed the first randomized controlled trial in children (5-13 y.o.), with chronic (> 1 year post-SCI), complete or incomplete (AIS A, B, C) tetraplegia or paraplegia.  They evaluated the cardiorespiratory and vascular responses to FES cycling or passive cycling performed in the home for 1 hour/day, 3 days/week for 6 months.  Thirty children were randomized to 1 of three groups:  FES cycling, passive cycling, or a non-cycling control group receiving electrical stimulation.  Participants in each group received the same amount of time in therapy.  The parameters of cycling are outlined in Table 3. Children who were in the electrical stimulation group used a portable stimulation unit to bilaterally stimulate their hamstrings, quadriceps, and gluteal muscles, each for 20 minutes at a time, without resistance.

Outcome measures were collected prior to training and upon completion of 6 months of training.  Outcomes included oxygen uptake (VO2) and heart rate (HR) which were measured during an incremental arm exercise test.  VO2 was collected at rest (1 minute), during cycling at 10W for 1 minute, during an exercise period with an incremental increase of 10W every minute until self-determined fatigue, and sitting for recovery (3 minutes).  Forced vital capacity was recorded as the percentage of the norm based on age and height.  Cholesterol, HDLs, LDLS and triglycerides were also assessed.

There was no significant difference in heart rate or forced vital capacity between groups.  Although there was no difference between the three groups in terms of absolute values of VO2 peak at baseline and post-testing, there was a significant difference in the average percent change.  The FES cycling group had a significantly greater increase in VO2 peak when compared to the passive cycling group.  Lipid values did not differ between groups at baseline and post-training, however, when comparing average percentage change, the FES cycling group had significant decrease in cholesterol when compared to the passive cycling group.

The findings from these experimental studies suggest that FES cycling may be a safe intervention, at least in relation to the muscle, in adults with acute SCI.  Early increases in cross sectional area, or even the prevention of the muscle atrophy that occurs early after SCI, may lead to improvements in glucose utilization, preventing or prolonging the onset of diabetes.  Increased muscle health and size may also prevent skin breakdown and pressure sores, decreasing the long term costs associated with this secondary condition.  Furthermore, the results from the Johnston study suggest that children with chronic SCI may exercise safely with FES cycling, and may receive health benefits from FES cycling.  Improved health may lead to better participation in life activities, as well as long term health benefits in persons with early SCI.

Quasi-Experimental Design Studies

The one study that used the quasi-experimental design did so for testing purposes. Bhambhani et al. (2000) used a cross sectional study design to compare the effects of FES cycling during one test session on quadriceps muscle deoxygenation in persons with SCI and those that were able-bodied.  Participants were defined as having “complete lower limb paralysis”, but were not classified with any other classification system, such as American Spinal Injury Association standards.

All participants participated in an incremental cycling exercise test.  The able-bodied persons performed the test on a stationary friction loaded cycle ergometer (Monark Model 834, Made in Sweden), and those with SCI performed the test on an ERGYS II (Therapeutic Technologies Inc., Alpha, Ohio).

During testing, metabolic and cardiorespiratory measures were taken with a metabolic cart, and the following were calculated: VO2, relative VO2, minute ventilation (VE), respiratory exchange ratio (RER).  Heart rate (HR) was collected using a wireless monitor and provided the data for O2 pulse, ventilatory equivalent.  Muscle oxygenation measures were obtained using Near Infrared Spectroscopy (NIRS) at rest, during exercise, and during recovery.

The cardiorespiratory and muscle oxygenation results are presented in Table 5.  While both groups reached (SCI group) or exceeded (able-bodied group) the RER criterion of 1.10 set for this study, indicating maximal effort, there was a significant difference in responses between the SCI group and the able-bodied group.  While the able-bodied group demonstrated a linear increase in all cardiorespiratory variables, the SCI group did not.  Instead, the SCI group demonstrated slight increases in VO2 and heart rate during each stage of testing.  The VE increased significantly from rest in both groups (p<0.05), and by three times baseline in those with SCI.

Muscle oxygenation responses differed significantly between groups.  Those with SCI did not present with the initial increase in oxygenation at the onset with the systematic decrease as exercise progressed, and then a rapid increase during the recovery phase.  Instead, they presented with a decrease in oxygenation throughout the stages of exercise, and only slightly increased during the recovery period.  Similarly, while there was a noted increase in blood volume during the initial phase of exercise in the able-bodied persons, there was no such increase in those with SCI.  This difference in muscle deoxygenation may represent the change in muscle fiber types that occurs early after SCI.

The findings from these studies suggest an acute respiratory response to exercise, even in persons with chronic, motor complete SCI.  These findings are similar to those in children with SCI who train on the FES cycle (Johnston et al. 2007, 2009). However, these responses do not simply mimic those in able-bodied persons, and therefore programs of exercise for the SCI population need to be tailored to their specific health needs, and not simply fashioned after what appears effective for persons who are able-bodied.  Further study is also needed to explore the muscle deoxygenation effects to determine if there are harmful effects of exercise, or if there are mechanisms for improving muscle deoxygenation and reoxygenation in those with muscle compromise due to SCI.

Conclusions from experimental and quasi-experimental design studies

The findings from these studies suggest that FES cycling may lead to cardiorespiratory and muscle benefits in adults with acute and chronic SCI.  Children with chronic SCI may experience cardiorespiratory benefits.  The cardiorespiratory and muscle responses, however, do not mimic those seen in persons who are not injured, and thus, exercise programs for persons with SCI need to be designed to address their specific needs.  Further research is warranted to elucidate the muscle-related effects of SCI.   Demchak et al. (2005) reported positive effects on muscle in persons with acute SCI, and Bhambhani et al. (2000) demonstrated a decrease in muscle function in those with chronic SCI.  The negative effects of exercise on muscle function, i.e. muscle oxygenation, in persons with SCI may be prevented by the introduction of FES cycling interventions earlier in the continuum of recovery.  Of course, increases in muscle cross sectional area may not necessarily lead to the maintenance of fiber types after SCI, or better muscle oxygenation and deoxygenation with exercise.  All of these variables require further study.  Training on an FES cycle may be a viable option for improving health in those with SCI, and therefore prevent the stress on the upper extremities that exercises that use upper extremity muscles may cause.  Further study is required to determine the relative benefits of FES cycling and upper extremity exercises in persons with SCI.

Methodological Conclusions

Each of these studies addressed different health-related problems in persons with different levels, chronicity and completeness of SCI, making it difficult to draw any conclusions from these studies for the general SCI population.  Furthermore, the training duration was different for these three studies.  Demchak et al. used a 13 week training period, whereas Johnston et. al’s participants trained for 6 months, and those in the study by Bhambhani et al. rode the cycle for a single testing session.  Therefore, it is difficult to know which training paradigm would lead to the changes reported, and if another paradigm would lead to better or worse effects.  A study that explores the effects related to the same set of health-related variables across the continuum of recovery (acute and chronic), or in a single session at different points along the continuum, will yield more useful results and allow better decision making related to the use of FES cycling for persons with SCI.

Descriptive Studies

Case Studies and Reports

The first report related to the potential for using FES cycling in children with SCI was conducted by Johnston et al (2007).  In this case report, Johnston and colleagues demonstrated that children with complete SCI (tetraplegia(n) = 2, paraplegia(n) = 2) can perform FES cycling, or passive lower extremity cycling, with parental assistance.  In addition, they evaluated the effects of FES cycling with the RT300 or RT100 (Restorative Therapies Inc., Baltimore, MD) on musculoskeletal and cardiorespiratory and vascular measures:  muscle volume, muscle strength, spasticity, bone mineral density (not reported here), fasting lipid profile, HR, and VO2.  Measures were collected during incremental upper extremity ergometry test performed pre-training and after 6 months of training.

Results are shown in Table 6.  Adherence to the training program was greater than 90%, suggesting that children will perform this form of exercise, at least for a 6-month period of time, and in the home.  The two children who cycled with FES showed increases in quadriceps muscle volume and strength (45.6%, 52.3%, and 289.3%, 173.6%, respectively).  Only one child who performed passive cycling demonstrated improvement in strength (212.3%), but much less increase in volume (15.3%).

The child with paraplegia who performed training on the FES cycle demonstrated exercise effects in the cardiorespiratory system.  He demonstrated a decline in resting and peak heart rate, and an increase in VO2 max.  The child with tetraplegia did not experience these same changes, and only demonstrated a decreased resting heart rate.  One of the children who exercise passively on the cycle demonstrated an increase in VO2 max.

The lipid profiles were not consistent, and require further study in children performing aerobic exercise.

The findings from this case study, which were further substantiated after the randomized controlled trial in 2009, suggest that FES cycling is a viable option for improving cardiorespiratory health in children with chronic complete or incomplete SCI.  Findings related to lipid profiles remain unclear and require further study.  Furthermore, these findings suggest that the responses in children are similar to those reported in adults.

Repeated Measures

Arnold and colleagues (1992) studied the safety and efficacy of FES cycling in 12 persons with either acute or chronic, complete (n=9) or incomplete (n=1) (Tables 2 through 4 provide details).  Training occurred in three phases (see Figure 1).  Phase one consisted of strengthening with electrical stimulation training to the quadriceps muscle; phase two involved FES cycling for 30 minutes; phase three required the addition of resistance during cycling.  Pulmonary function was assessed approximately 2.5 months into phase 1, then again 2.5 months into phase 2, and finally, after 6 months in phase 3.  Cardiorespiratory outcome measures included tidal volume (TV), VO2  and RER.  Those related to musculoskeletal health included girth measurements of the thigh and calf.

All parameters improved after training, and during all phases.  Significant changes in TV were noted in phase one when compared to phases two (p<0.001) and three (p<0.001). VO2 increased significantly during phase two (cycling) (p<0.002) and phase three (resistance) when compared to phase one (leg extension).  All participants showed a significant increase in thigh girth bilaterally (p<0.002 for right, and p<0.001 for left) over the course of all three phases, but not in the calf muscles (which were not stimulated).  These findings further support those reported earlier that FES cycling may yield cardiorespiratory and muscle health benefits in persons with complete, and potentially those with incomplete (n=1), SCI.  Also interesting to note is the rapid increase during early phases of exercise, as well as those later in the training.

Pre-Post Design

Two studies used the pre-post design to study the effects of FES cycling on cardiorespiratory, metabolic and vascular systems (Faghri et al 1992, Hooker et al. 1992).  Both studied the cardiorespiratory and vascular effects in a similar participant population: predominantly male adults with complete (AIS A) or incomplete (AIS B, C, D) paraplegia or tetraplegia.  Hooker et al. (1992) included persons with acute or chronic SCI, whereas Faghri et al. (1992) only included those with chronic injury.

Faghri et al. (1992) evaluated the effects of FES cycling on cardiorespiratory and vascular responses in 13 persons with motor complete (AIS A or B) or motor incomplete (AIS C or D) chronic SCI (tetraplegia(n)=7, paraplegia(n)=6). The degree of completeness was determined by the Frankel scale (American Spinal Injury Association, 1990).

All participants completed 36, 30-minute sessions of training in an average of 13 weeks.  If participants became fatigued during a session, then they were allowed to have three attempts to complete the 30 minutes.  When capable of completing three consecutive 30 minute sessions, resistance was increased by 6.1 watts.

Outcome measures were collected before and after the 36 sessions, and included metabolic and cardiorespiratory testing at rest and during 5 minutes of FES cycling at 0-W power output.  VO2, carbon dioxide output (VCO2), VE and RER were all calculated from the expired gas.  Transthoracic impedance cardiography revealed central hemodynamic responses (stroke volume (SV) and cardiac output CO).  Heart rate (HR) was determined using ECG, and diastolic and systolic (DBP and SBP, respectively) blood pressure via auscultation.  Mean arterial pressure (MAP), total peripheral resistance (TPR) were then calculated.

Table 7 summarizes the changes seen in the respiratory, cardiac and vascular responses.  In general, all participants with SCI improved from initially being unable to complete the 30 minute sessions to being able to complete 30 minutes of continuous exercise.  Similarly, participants were able to increase the resistance during cycling, and improved to a mean PO of 17.4+/- 2.9W (persons with tetraplegia) and 17.1 +/-3.5W (persons with paraplegia).   All participants demonstrated changes in respiratory, cardiac and vascular (except MAP and DBP), suggesting an acute exercise response.  Both groups demonstrated changes in some cardiac variables (SV and HR) and some vascular variables (SBP, DBP, MAP).  Only the paraplegic group demonstrated significant changes in TPR (i.e. a decrease) both at rest and during the submaximal exercise test post-36 sessions of FES cycling training. Furthermore, the paraplegic group also demonstrated increases in SV, and decreases in all vascular variables at rest post-training.

The findings from these studies reported by Faghri et al. (1992) suggest that short term (36 sessions, 13 weeks) exercise can lead to changes in cardiac and vascular variables in both persons with tetraplegia and those with paraplegia.  However, based on the findings from these studies, it is not likely that with the training delivered at the intensity of this study that they will experience changes in respiratory function either at rest or during exercise.

Using a training program similar to that used by Faghri et al. (1992) (see Table 3 for details), Hooker et al (1992) also evaluated the effects of FES cycling on physiological responses during both a FES cycle stress test, and an untrained upper extremity stress test in males (n=17) and one female with either acute or chronic complete or incomplete SCI.  They included measures of VO2, VE, VCO2, RER (VCO2/ VO2), SV, CO, HR, MAP and TPR.  Data was analyzed for persons with paraplegia and tetraplegia together.  Their findings were essentially the same as those from the study reported by Faghri et al (1992).

All participants were able to increase power output over the time of FES cycle training, and the most rapid change in power output was seen during the first 4 weeks of training.  There was a significant increase in power output seen between pre- and post-testing with the FES cycle stress test, but no change in power output for the upper extremity stress test.  There was a significant increase in power output, VO2, VE, and HR during the post-training on the FES cycle stress test, as well as a lowered TPR.  There were no significant changes in peak SV, MAP or RER.  The lack of changes may be due to analyzing the data from persons with tetraplegia and those with paraplegia together.  There may be different responses in these groups, based on level of injury, and these changes may effectively cancel each other out.  There were no significant changes in any variables during the upper extremity stress test.

Another more recent study explored the effects of FES cycling on arterial compliance.  Zbogar et al. (2008) studied the vascular effects of training on an ERGYS 2 (Therapeutic Alliances Inc, Ohio, USA) FES cycle in four females with chronic, tetraplegia (n=2, AIS B, C4 and C5) and paraplegia (n=2, T4, AIS A and T7, AIS C).  Each participant first habituated on the FES cycle so that they were all able to train for 30 consecutive minutes.  Each then trained for 30 minutes, on average 1.9 days a week, for 12 weeks.  Outcome measures were collected 2 to 7 days after completion of the habituation period, and also 2 to 7 days after completion of the training.  Data were collected related to the large and small arterial compliance using an applanation tonometer (Hypertension Diagnostics/Pulse Wave CR-3000; Eagan, MN, USA).

Initial values for small arterial compliance were 53% less than age and sex matched historical controls, however, large arterial compliance was within normal values.  There was no significant change in large arterial compliance after training, and the average change was only 5% across the group.  There was, however, an increase in small arterial compliance, to about 88% of normal values.  This was a significant increase (p=0.05) of 63% from starting values.  These findings suggest that there are vascular effects from training on an FES cycle in women with chronic sensory and motor incomplete SCI.

Testing only

Theisen et al. (2002) studied the effects of 40 minutes of cycling on power output in five adult (4 males, 1 female) with chronic, AIS A paraplegia (T4-T9) who performed 40 minutes of cycling on a MOTOmed Viva cycle ergometer (Reck, Germany).  Once seated on the ergometer, they rested 10 minutes, then started cycling with a motor at 50rpm.  Stimulation was triggered after the first 5-10 revolutions of the crank, and increased to 120-140mA.  After this point, stimulation amplitude remained constant.

Throughout cycling, metabolic and cardiorespiratory data were collected, including VO2, VCO2, VE, and heart rate.  Data were averaged over 30 second periods.  There was a strong time-dependent  response, with PO reaching a maximal level at 6 minutes of exercise.  After this point the power output dropped, and then progressively increased after 19.5 minutes of cycling.  Towards the end of exercise, the power output again decreased slightly.  VO2 also increased significantly from rest after 2 and 6 minutes of cycling, and then decreased again at 40 minutes of cycling. Heart rate decreased initially but then increased to a value significantly higher than the resting value.

More recently, Fornusek et al. (2008) also studied the effects of FES cycling on cardiorespiratory and muscle oxygenation responses in persons with motor complete (AIS A) paraplegia.  Their focus was on evaluating the effects of cycling at different cadences in order to see if there was a workload effect.  Participants performed an exercise test once a week for three weeks.  The order of testing was randomly controlled for the cadence being tested (15, 30, or 50rpm).  Cardiorespiratory responses (Table 8 shows a list of variables) were assessed using a metabolic cart and muscle oxygenation was measured NIRS.  Both were collected throughout the exercise session.  Each exercise test session lasted 35 minutes.

Table 8 summarizes the key findings from the study. Although the power output differed at the three different cadences, there were no significant differences in the variables measured between the cadences.

Conclusions from descriptive studies

Taken together, the findings from these descriptive studies suggest that there are cardiorespiratory, vascular and muscle improvements in both children and adults with both acute and chronic SCI who train with FES cycling.  There is also evidence that persons with tetraplegia do not respond in the same fashion as those with paraplegia to this exercise in terms of cardiorespiratory and vascular responses.  This is not a surprise, given that persons with tetraplegia may have more autonomic disruption that may impact their exercise response.  Therefore, exercise programs designed for persons with tetraplegia may need to be different or modified from those with paraplegia.

Exercising at different cadences may not impact power output and acute responses to exercise, however, it remains unclear what the impact would be with training for longer duration at the different cadences.  Passive cycling may lead to cardiorespiratory benefits in some persons with SCI, and a careful comparison between passive and FES cycling in persons with FES is warranted.  The cost of these two devices is different (i.e., passive cycles are less expensive), and if certain persons can obtain the desired health-related benefits with a less expensive tool or device, this would be desirable.

Methodological Conclusions

There was a fair amount of inconsistency in reporting the method for determining extent of injury throughout these studies, as well as inconsistencies in reporting parameters of the electrical stimulation.  Therefore, it remains difficult to determine which training paradigm would be best for any given person with SCI.  However, the stimulation parameters for those studies that reported them was quite similar across studies, and with different FES cycle devices, suggesting that the responses reported for any given device should be expected if the other devices are utilized.

Body-weight Supported Treadmill Training

Table 9 provides a summary of number of participants, level and extent of injury, chronicity, sex and age of participants in the studies exploring the effectiveness of benefits of locomotor training approaches, all of which utilized body-weight supported treadmill training (BWSTT).  There were no reports of randomized controlled trials evaluating the exercise or health-related benefits of BWSTT in SCI.  Of the 8 studies that employed the BWSTT approach, only 3 employed a control group in a quasi-experimental design, but no randomization.  The remaining 5 used a descriptive study design.  The interventions and outcome measures for all of the reviewed locomotor training studies are summarized in Table 10.  The areas addressed by the BWSTT studies include the function related to cardiorespiratory, muscle, or vascular systems, or metabolic function in general.

Quasi-Experimental Design Studies

The three studies that employed a quasi-experimental approach (summarized in Tables 9 and 10) explored different aspects of health effects due to BWSTT  in adults (Giangregorio, Webber, Phillips et al. 2006; Carvalho & Cliquet 2005; Carvalho, Martins, Cardoso, Cliquet 2005), and used different approaches to BWSTT.

Two studies report on different outcome measures for the same 21 participants (Carvalho & Cliquet 2005; Carvalho, Martins, Cardoso, Cliquet 2005) who participated in BWSTT combined with neuromuscular electrical stimulation (NMES).  The focus of these studies is on the effects of BWSTT on cardiorespiratory and metabolic functions.  All 21 participants were male (mean age 31.95+/-8.01 years), with chronic (> 24 months post-SCI), motor complete (AIS A and B) tetraplegia (C4 to C8).  Participants were assigned to either a control group (CG) or a gait group (GG) (receiving the intervention of BWSTT+NMES).  Those that were not able to attend the hospital in which the study was conducted were allocated to the control group.  The CG received only conventional therapy two times a week for 6 months, and no NMES or BWSTT.  Table 11 summarizes the AIS for participants in the different groups.

Participants in the GG first underwent pre-gait conditioning with electrical stimulation to bilateral quadriceps and tibialis anterior, while seated, for 20 minutes, 2 times a week, for 5 months.  Participants then participated in BWSST + NMES for 20 minutes a session, two times a week, for 6 months.  Body-weight support (BWS) varied between 30 and 50%, and was modified to allow heel strike throughout training.  Manual assistance was provided by trained physical therapists.  All participants started walking on the treadmill at 0.5 km/h; increase in speed was judged primarily by gait quality while walking on the treadmill. Specifically, participants walked at the highest speed at which they could maintain heel strike and “usual patterns” of walking.  The highest speed after 6 months of training achieved was 1.3km/h.

NMES was delivered with a four-channel voltage-source electrical stimulator (25 Hz, 300-µs duration and max intensity 200V).  NMES was triggered by hand to assist stance phase with stimulation to the quadriceps and the swing phase through stimulation of the withdrawal reflex (activation of ankle dorsiflexion, and knee and hip flexion).

All participants were tested with the cardiorespiratory test upon enrollment and after the 6 month intervention period.  The GG was also tested upon completion of the pre-gait NMES training, before the BWSTT was initiated. The CG was not able to do any gait during the testing, and therefore was tested using a knee extension exercise, in order to collect the cardiorespiratory-related outcomes for testing.  The cardiorespiratory test consisted if three phases: 8 min of rest, 10 min of activity (GG = treadmill walking with NMES, CG = alternating left/right knee NMES for knee extension), and 10 minutes of recovery.  Outcome measures included VO2, VCO2, VE, HR and BP.  Respiratory measures were collected using open-circuit spirometry. Heart rate was continuously monitored with electrocardiography, and brachial blood pressure was obtained prior to training, after 10 minutes of training and as soon as training was completed and the participant was sitting.

Both the CG and the GG demonstrated increases in VO2, VE, VCO2, and systolic BP, after training, but the greatest changes were noted in the GG.   Statistically significant increases were noted in the CG during both the resting and exercising phases of cardiorespiratory testing, and in the GG during the exercise phase of testing.  In addition, energy costs were calculated (Carvalho & Cliquet 2005).  Energy consumption decreased significantly during the resting phase of testing, but increased during the exercise phase of testing in the GG; whereas in the CG, energy consumption increased during both the resting and exercise phases of testing.

The findings of these studies (Carvalho & Cliquet 2005; Carvalho, Martins, Cardoso, Cliquet 2005) suggest that persons with chronic, complete tetraplegia, who train with BWSTT+NMES can increase cardiorespiratory and metabolic responses, despite having autonomic nervous system disruption, and paralyzed muscles below the level of injury.

Carvalho et al. (2005) compared manual BWSTT combined with neuromuscular electrical stimulation (NMES) to NMES in sitting in persons with tetraplegia.   Participants were not randomly assigned, but were placed into either a gait group (n = 17) or a NMES endurance exercise group (n = 14).  Tables 10 and 11 show the breakdown of the AIS for the participants in each group.  In summary, the gait group included persons with sensory incomplete (AIS B) and motor incomplete (AIS C, D) SCI, whereas the NMES endurance group included persons with only sensory incomplete (AIS B).  Both groups included persons with complete injury (AIS A), and all had chronic injuries (greater than 17 months).

Participants in the gait group were trained for three sessions with NMES and BWS before the testing.  Testing consisted of eight minutes of rest, 10 minutes of BWS walking and 10 minutes of recovery.  Participants in the NMES endurance exercise group rested for 8 minutes, as well, then performed 15 minutes or quadriceps endurance exercise with NMES in sitting, followed by a 10 minute recovery period.

Outcome measures consisted of VO2, VCO2, RER, and VE using open circuit spirometry.  Heart rate was measured using an ECG.

There was variability observed in the metabolic and cardiorespiratory measures in the gait group, between those with complete and incomplete injuries, leading the investigators to separate these two groups for analysis.  There were no obvious differences between the complete (AIS A) and incomplete (AIS B) injury groups in the NMES endurance exercise group.

Since the two incomplete groups were quite different (i.e. the gait group included those with motor incomplete injuries, whereas the NMES endurance exercise group did not), it is difficult to make much of the findings (see Table 12).  Namely, those in the gait group who had incomplete injuries demonstrated obviously greater changes in all parameters during the exercise phase, whereas in the NMES endurance exercise group, the differences between rest and exercise conditions were much less.   Of interest, however, is the similarity between the complete subgroups in the gait group and the NMES endurance exercise group (Table 13) in the VO2 (l/min), VCO2, and RER.  These groups did differ however, in VO2 (ml/kg/min), heart rate and VE.   Finally, while there were differences between the incomplete (AIS B, C, D) and complete subgroups of the gait group (greater changes between rest and exercise in the incomplete group than in the complete group), there was greater similarity between the incomplete (AIS B) and complete subgroups of the NMES endurance group for all parameters.

These findings suggest several things.  The first is that those with motor incomplete SCI have very different responses to BWSTT with NMES than those with complete injuries.  Furthermore, persons with complete injuries may gain improvements in cardiorespiratory and metabolic measures with NMES endurance exercise that are similar to those seen with BWSTT with NMES.  Finally, those with complete (AIS A) and sensory incomplete (AIS B) injuries may benefit in a similar manner from NMES endurance exercises. That there is no difference in terms of exercise response between those with AIS A and AIS B classified injuries may not be a surprise since the only clinically measured difference between these two groups is the anal sensation. Whether the same is true with BWSTT combined with NMES is not clear from this study alone.

Giangregorio et al. (2006) used a longitudinal prospective, within-subject design and reported on the effects of manual BWSTT (mBWSTT) on bone mineral density and muscle atrophy in 14 persons with chronic (> 1 year post-SCI), incomplete (AIS B or C) SCI.  Only the results related to muscle atrophy are reported here.  The majority (n=12) had some motor ability below their level of injury and were classified as AIS C.  The majority of the participants were male (n=11), and the majority presented with tetraplegia (n=11) between C4 and C6.  Three participants had injuries at T8 (n=1) or T12 (n=2).  All participants were adults (age between 20 and 53 years).  Four other persons are included as a reference group to that receiving the intervention.

All participants in the training group trained for approximately 3 times a week, for a total of 144 sessions over 15 months.   Body weight support (BWS) was adjusted in order to allow full trunk extension and to prevent buckling of the knees in quiet standing on the treadmill.  Participants initially walked 5-15 minutes, depending on endurance, and increased gradually as tolerated.  BWS generally was around 60%; speeds were 0.6km/h or less, and varied between persons.

Walking-related outcome measures were collected at baseline and every three months thereafter; muscle mass and muscle cross sectional area were collected at baseline and at the completion of 12 months of mBWSTT.  Table 10 summarizes the outcome measures for this study.  One participant was not able to complete the assessments, and therefore the results presented are on the remaining 13 participants.  The only significant health-related change was an increase in lean body mass overall, as well as an increase in thigh and calf muscle cross sectional areas.

Conclusions from the Quasi-experimental Studies

The findings from these quasi-experimental studies suggest that there are cardiorespiratory benefits after mBWSTT supplemented with NMES in persons with chronic, motor complete tetraplegia.  This is meaningful since this intervention, BWSTT with NMES, may therefore provide another option for exercise that will not impact the arms, and specifically the shoulders.  One study did report muscle-related benefits, namely increased cross sectional area, which may be meaningful for glucose regulation.  However, it must be noted that these studies were performed in persons with incomplete SCI and the same findings may not be reproduced for persons with complete SCI.

Methodological Conclusions

Further study is warranted in order to determine the health related benefits of BWSTT for individuals with varying levels and extent of injury.

Descriptive Studies

Descriptive studies included all studies that had neither a control group, nor randomization. These included case studies and reports, studies employing repeated measures, and pre-post designs.  Five studies used a descriptive approach.  One used a case study (Hicks et al. 2006), another a case series (Giangregario et al. 2005),

Case Studies and Reports

Hicks et al. (2006) evaluated the effects of 4 months of BWSTT three times a week on skeletal muscle morphology in one 27 year old woman with chronic (5 years post-SCI), motor complete (AIS B) tetraplegia (C4).  The participant trained with manual assisted BWSTT at the amount of weight support and speed that allowed her to extend her knees fully during the stance phase.  She required assistance throughout the training period, but did increase speed and duration of walking in the BWSTT environment over the course of the study.

Outcome measures focused on examining the vastus lateralis muscle fiber size and type pre- and post-training.  Needle biopsies were taken prior to the initiation of training and 3 days prior to the completion of the 48 sessions of training.  The vastus lateralis presented with atrophy pre-training, and the fiber area increased by 27.1% post-training.  In addition, the percentage of type I fibers increased from 1.3% to 24.6%, and the percentage of type IIa and type IIx fiber types decreased (30.8 to 20.8, and 68.0 to 54.5, respectively).  These findings suggest that prolonged training with manual BWSTT in this person with chronic, motor complete tetraplegia may lead to changes in muscle fiber type, and may make the muscle more effective for metabolism and energy consumption.

In a longitudinal prospective case series, Giangregario et al. (2005) examined the effects of manual BWSTT in five persons with acute (2-6 months post-injury) SCI.  Participants in this study trained in manual BWSTT for a total of 48 sessions in a maximum of 8 months.  Training was delivered in the same manner as was reported above (Giangregario et al. 2006).

Outcome measures were assessed pre-training, 24 months into training, and at the completion of 48 sessions of training, except for the bone mineral density which was only collected before and after the completion of training.  Walking outcomes focused on amount of body weight support, walking speed, and walking duration.  Bone biochemical markers were assessed using first morning urine samples and venous samples.  Bone mineral density of the lumbar spine, bilateral proximal femur, and right distal femur and proximal tibia, as well as of the entire body, was assessed using dual-energy X-ray absorptiometry (DXA).  Computed tomography (CT) was used to further assess bone cross sectional area (CSA) and volumetric bone mineral density, as well as muscle CSA at the thigh and lower leg sites.

Giangregario et l (2005) found that in all but one participant (unable to complete the training in the requisite 8 months), completed 1.7 sessions across the 8 month period, for a total of 48 sessions.  Only one participant progressed from being unable to walk over ground (0 on the Modified Wernig Scale), to being able to walk greater than five steps over ground with a rolling frame (score 7 on Modified Wernig Scale).  She also decreased body weight support to zero at the completion of training.  All other participants decreased their body weight support while on the treadmill but continued to require assist with their lower extremities while training.  Of critical note is that this participant with the marked improvements in walking presented with a motor incomplete (AIS C) injury.  All participants increased their speed when walking on the treadmill between the first and 24th sessions, but there was essentially no further gain reported between the 24th and final 48th session.   The participant who made the greatest changes in BWS (i.e. decreased to 0) actually did not demonstrate any significant increases in speed from the first, baseline session, to the post-training (48 sessions). Likewise, walking duration increased between the first and 24th sessions in all participants, but not between the 24th and final session.

All participants demonstrated an increase in both muscle and fat CSA in both the thigh and calf at the completion of BWSTT.  Muscle CSA increased from 60% in the thigh and 65% in the calf, to 72% and 79%, respectively.  Fat CSA increased from 113% to 142% in the thigh, and from 100% to 133% in the calf.  P values were not provided The investigators evaluated the significance of changes in the muscle and fat CSA by comparing the observed change in method error.  If they observed a change for a given variable that was greater than the RMSSD for that variable multiplied by three, then it can be stated with 99% confidence that the change that occurred was greater than what was expected from measurement error.

The findings from these studies demonstrate that intense activity with manual BWSTT in persons with acute, incomplete SCI (n= 1) may lead to improvements in walking ability both on the treadmill and over ground.  Interestingly, this participant did not demonstrate the greatest changes in muscle and fat CSA.  While persons with motor complete (AIS B) SCI demonstrated increases in both muscle and fat CSA in the lower extremities, they did not demonstrate significant gains in walking ability overground.  In fact, in all cases, training with manual BWSTT did not lead to decreases in fat CSA in the lower extremity muscles. Increases in muscle CSA are promising, however, suggesting that manual BWSTT may be a viable option for improving muscle size in persons with motor complete SCI, and requires further study to determine the relationship between these changes, and measures of muscle metabolism, vascularity and the relation of these to health. 

Pre-Post Design

Ditor et al. evaluated the effects of manual BWSTT on cardiovascular responses in persons with motor complete SCI.  Six persons with chronic (> 1 year), AIS A or B, C4-T12 SCI trained three times a week for 4 months.  BWS was adjusted to allow enough support to prevent buckling of the knees during stance, and the speed was set initially at 0.5 km/h, and the duration of exercise totaled 15 minutes per session (three five minute bouts).  Body weight support was decreased and speed and duration were increased as the participants tolerated.  Tolerance was determined by lack of knee buckling, spasticity, and the amount of assistance the trainers needed to provide to move the legs.

Outcome measures were collected at baseline, and upon completion of four months of training, and included:  Doppler ultrasound of carotid, femoral and brachial arteries during session one, and continuous heart rate and blood pressure to determine heart rate variability and blood pressure variability during session two.  Sessions one and two were held on different days.  All measures were collected while the participant was in supine, and proceeded after a five- minute rest period.  Heart rate was also assessed daily during training, and baseline was collected on the third day to allow for habituation to BWSTT.

Both resting HR and average HR during BWSTT remained unchanged over the course of training.  Heart rate in upright was significantly higher than at rest in supine (p<0.001), and while walking on the treadmill than when in upright (p<0.09).  There was a difference in responses between those with tetraplegia and those with paraplegia.  Persons with tetraplegia experienced a greater increase in average HR (67.1+/-39.1%) than those with paraplegia (37.1+/-10.7%).  This response was quite varied in those with tetraplegia, with an average increase range of 26-104%.  Notably, the investigators reported that lesion level alone did not predict the HR responses to exercise.  They report that there appeared to be a relationship between the degree of muscle spasticity (although there are no reports of measures for spasticity), or greater orthostatic instability.  They note a significant correlation between the percentage increase in heart rate and the decrease in mean arterial pressure from rest to upright during baseline testing (p<0.02).

The only significant finding related to the effects of BWSTT on arterial measures was a significant increase in femoral artery compliance (p<0.07).  There did not appear to be any effect on HR or BP variability after four months of BWSTT in these persons.   Thus, changes in blood flow appear to be independent of HR changes.

Of note, there were two adverse events were reported during this training.  One person experienced frequent syncope during sessions, and another developed skin breakdown over the vertebrae due to the harness.  The sore did not prevent training, since it was covered with clear plastic which prevented further skin injury.

Testing only

One study compared the exercise benefits between robotic and manual assisted BWSTT.  Israel et al. evaluated the differences in metabolic costs between manual BWSTT and robotic BWSTT in 12 persons with motor incomplete SCI.  All participants were able to walk over ground prior to the study without assistance, but with orthotic and assistive devices, but were not all at the community level of ambulation.  All but one participant had been injured over 1 year; one had been injured for only 5 months.

There were two protocols for this study.  The first was robotic assisted BWSTT, wherein the participants walked with either the robotic assist and matched the trajectories of the device, or manual assisted BWSTT, and in both cases no visual feedback was provided (trajectory protocol); the second compared robotic BWSTT wherein the participants were instructed to maximize their voluntary effort while walking, and for which they had visual feedback, or manual assisted BWSTT (max effort protocol).  All participants did not necessarily participate in both protocols.  Eight participated in both, while two participated in the first protocol (trajectory protocol), and two participated in the second one (max effort protocol).  BWS was set to 30 to 40% for all participants, and was kept constant.

Metabolic outcome measures included:  the rate of oxygen consumption (VO2) and carbon dioxide production (VCO2) using a metabolic cart for the trajectory protocol, or a portable metabolic unit for the max effort protocol.  Muscle activity was measured using surface EMG.   Tibialis anterior, soleus, medial gastrocnemius, vastus lateralis, rectus femoris, and medial hamstring muscles were all assessed from one limb during walking in all conditions.

Metabolic measures were taken while the participants were seated for five minutes prior to starting walking on the treadmill.  EMG was collected during walking only.  Metabolic costs were collected during two minutes of standing in the BWS system.  After the data collection in standing, participants walked at 3.0 km/h for 10 minutes on the treadmill.  After completion of walking 10 minutes, participants were seated and again assessed in sitting for 10 minutes.  After returning to baseline levels of VO2, participants walked again with the alternate protocol.  The testing order was randomized.  Resting usually lasted for approximately 15 to 25 minutes.  The metabolic cost of walking was calculated by values collected during standing and those collected during walking, and were normalized to body mass.  The relationship between muscle activity and metabolic costs was determined by comparing the change in metabolic costs, and the change in EMG for the rectus femoris, medial hamstring, and medial gastrocnemius.

Metabolic responses were variable between conditions (manual or robotic assisted BWSTT) and between protocols (trajectory and max effort).  VO2 and metabolic costs differed significantly (p<0.05) between the robotic assisted with trajectory match and the manual assisted BWSTT in both the standing and steady state walking conditions.   The VO2 and metabolic costs were more similar between the robotic assisted max effort condition and the manual BWSTT condition.  There was a significant difference (p<0.05) between the robotic trajectory match and robotic max effort conditions.  There was no significant difference between the manual BWSTT conditions in either protocol.

The only significant relationship (p<0.01) between muscle activity and the metabolic costs was found for the rectus femoris during the pre-swing phase of gait.

These findings suggest that in persons with chronic, and potentially in those with acute, SCI, there are differences in exercise responses based on the delivery of BWSTT.  Specifically, in order to increase metabolic costs, participants should attempt to provide maximal effort during training.

Conclusions from Descriptive Studies

The findings from these descriptive studies further suggest that persons with both complete and incomplete SCI can receive cardiorespiratory and muscle benefits from BWSTT.  In addition, the evidence also suggests vascular responses, and specifically, improvements in arterial compliance after exercise.

Methodological Conclusions

As with all other methods (i.e. quasi-experimental), the data from descriptive studies varies based on the training paradigm, the participant characteristics (level, extent and chronicity of injury), and the outcome measures used.  Studies employing similar participants training with identical programs, and receiving the same outcome measures will provide valuable insight related to the positive and negative health effects of BWSTT.

Summary and Conclusions Related to the Efficacy of Activity-Based Interventions for Improving Health-Related Outcomes after SCI

The following conclusions can be made from this review of the FES cycling and BWSTT training effects on health:

  • The following persons may experience cardiorespiratory benefits from FES cycling or BWSTT:
    • Adults and children with complete tetraplegia or paraplegia between C4 and T11;
    • Adults and children with incomplete tetraplegia or paraplegia between C4 and T11;
    • Adults with acute or chronic SCI;
    • Children with chronic SCI.
  • The following persons may experience muscle related benefits from FES cycling or BWSTT:
    • Adults and with acute or chronic complete or incomplete tetraplegia or paraplegia;
    • Children with chronic SCI.
  • Adults with acute or chronic, complete or incomplete SCI may experience positive changes in vascular function that may improve cardiac health.
  • The combination of NMES and BWSTT may lead to greater increases in muscle cross sectional area, as well as metabolism, than BWSTT alone.

The changes in cardiorespiratory, vascular and muscle function are meaningful, and may lead to a decrease in the risk factors associated with CVD.  This may further increase longevity after SCI, and lead to greater health and quality of life in persons with SCI.

In addition to these findings, some points related to safety and application of these training approaches:

  • Changes in heart rate and blood pressure appear to vary based on level of injury, and not intensity of the exercise. Specifically, those with tetraplegia do not demonstrate the same response to exercise as those with paraplegia, and this is most likely due to the autonomic dysfunction that accompanies cervical level injury.
  • Caution should be taken to prevent cardiac disturbances or breakdown due to the training or the harness, respectively.

Considerations for future study:

  • There are variable responses in arterial compliance and lipid profiles that require further study.
  • FES cycling and BWSTT (whether manual or robotic) have not been compared in relation to the exercise and health-related benefits.  Further study evaluating the relative benefits from these training approaches is warranted. This study choud also include cost-benefit analyses to allow persons with SCI, and their payers, to make well-informed choices about which intervention would be most productive and cost-efficient for that person.
  • Further study is also needed to elucidate the differential responses and benefits to FES cycling and BWSTT approaches for persons with different levels, completeness (AIS classification) and chronicity of SCI.  Evidence already suggests the difference between persons with paraplegia and those with tetraplegia in terms of exercise responses, and there may be other differences between persons with SCI that will impact the prescription for exercise.
  • FES cycling, BWSTT approaches and upper extremity exercise should be compared for their relative contributions to exercise and health-related benefits in SCI.

Final recommendations related to training with FES cycling and BWSTT:

  • Persons with SCI who desire pursuing FES cycling or BWSTT for improving health and wellness should discuss with their health care provider the intensity and duration of the program required to effect a change in cardiorespiratory, muscle, vascular, or metabolic variables based on the level, extent and chronicity of their SCI.

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Acknowledgements and statement concerning conflict of interest


The activity-based interventions study group would like to thank the staff of NIDRR for their support of this undertaking including our project officer, Pimjai Sudsawad.  In addition, we would like to thank the principal investigators, E. Sally Rogers and Marianne Farkas for their guidance and support, as well as Megan Kash for development and assistance with the database and analysis tools.  We also appreciate the time and effort of the experts who reviewed our list of references to determine if all relevant articles were included in this review:

Statement Concerning Conflict of Interest

No study group member has a conflict of interest in this area of SCI research.  Shepherd Center has one grant also funded by NIDRR related to evaluating the efficacy of a post-acute activity-based program for persons with incomplete tetraplegia.  However, no member of the study group has a fiduciary interest in the delivery of activity-based interventions for persons with SCI.

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