Systemic Inflammation

High systemic inflammation is related to a high body mass index, a history of pressure ulcers, and urinary tract infections, which are all common consequences of SCI, and can be moderated with regular walking exercise. Cardiovascular health can also be influenced by systemic inflammation and moderated with walking exercise. Inflammation has been independently related to the mode of locomotion in individuals with chronic SCI. In this study, inflammation was lowest in those who walked with an assistive device, walked independently, or used a manual wheelchair.

Muscle Loading

Load bearing by the lower extremities increases muscle activity in those with SCI as reflected in the amplitude of electromyography (EMG), possibly because of sensory input. Based on these observations, minimizing upper limb loading with handrails or parallel bars, while increasing vertical load bearing through the legs, should be encouraged during walking. This practice has been translated into a guiding principle for improving muscle activation in those muscles that are weak.

Cartilage Atrophy

In a study about cartilage health in those with SCI who were ambulators, capable of walking and not confined to their wheelchair, and those who were nonambulators, it was found that nonambulators with SCI experienced increased cartilage atrophy and degradation. Articular cartilage degradation has been associated with elevated collagen type-II levels in individuals with SCI who are nonambulators or physiologic ambulators. The following factors can cause significant differences in collagen type-II levels: injury level Asia Impairment Scale (AIS) A ( Table 1 ), a zero functional ambulation score, and little daily ambulation. Thus, therapy should be initiated as soon as possible after SCI to minimize cartilage atrophy.

Bone Density

Walking retains bone mineral content and should be started as early as possible in the postinjury phase to reduce mineral loss. Nearly one-half of the mineral content below the lesion level is lost within the first year after injury, so walking is vital to bone health. Another recent study suggests that there is an association between circulating sclerostin and bone density in chronic SCI. Sclerostin is a protein that is produced by the osteocyte; it has anti-anabolic effects on bone formation. Levels of sclerostin, a biomarker of osteoporosis severity, were reduced in patients with SCI who used a wheelchair compared with individuals with SCI who walked regularly. Circulating sclerostin was deemed a biomarker of osteoporosis severity in chronic paraplegia rather than a mediator of ongoing bone loss. This finding was in contrast to animal models of mechanical unloading whereby high sclerostin levels suppress bone formation acutely. Bone loss can also be asymmetric in the lower limbs because of walking asymmetries in patients with incomplete SCI (iSCI).

Quality of Life

A change in mobility within the first year after injury can significantly impact perceived quality of life. Individuals with SCI who transitioned from walking at discharge to wheelchair use have low quality-of-life indicators, including high pain and depression scores. The data suggest that marginal ambulators be encouraged to work toward functional independence from a wheelchair rather than depend on primary ambulation during acute rehabilitation. Self-help mental health programs should also be included for inpatient ambulators and those who are discharged as ambulators. Some patients may also have unrealistic expectations about walking that may cause the activity to be abandoned, for example, that it will lead to complete recovery of walking function or recovery from SCI altogether.

Clinical Decision Making

Understanding individual ambulation deficits is critical for clinical decision making because many patients with iSCI require gait reeducation, especially for those at the AIS D level (see Table 1 ). The ambulation prognosis generally depends on muscle power loss, degree of spasticity, type of lower limb joint deformity developed, and availability of treatment. As an adjunct to physical examination and observation, gait analysis can inform treatment with measures of 3-dimensional dynamic joint range motion (kinematics) and estimation of joint forces (kinetics) at the hip, knee, and ankle. These measurements can be combined with walking EMG and energy cost measures to fully understand the gait disturbance.

Systemic Inflammation

High systemic inflammation is related to a high body mass index, a history of pressure ulcers, and urinary tract infections, which are all common consequences of SCI, and can be moderated with regular walking exercise. Cardiovascular health can also be influenced by systemic inflammation and moderated with walking exercise. Inflammation has been independently related to the mode of locomotion in individuals with chronic SCI. In this study, inflammation was lowest in those who walked with an assistive device, walked independently, or used a manual wheelchair.

Muscle Loading

Load bearing by the lower extremities increases muscle activity in those with SCI as reflected in the amplitude of electromyography (EMG), possibly because of sensory input. Based on these observations, minimizing upper limb loading with handrails or parallel bars, while increasing vertical load bearing through the legs, should be encouraged during walking. This practice has been translated into a guiding principle for improving muscle activation in those muscles that are weak.

Cartilage Atrophy

In a study about cartilage health in those with SCI who were ambulators, capable of walking and not confined to their wheelchair, and those who were nonambulators, it was found that nonambulators with SCI experienced increased cartilage atrophy and degradation. Articular cartilage degradation has been associated with elevated collagen type-II levels in individuals with SCI who are nonambulators or physiologic ambulators. The following factors can cause significant differences in collagen type-II levels: injury level Asia Impairment Scale (AIS) A ( Table 1 ), a zero functional ambulation score, and little daily ambulation. Thus, therapy should be initiated as soon as possible after SCI to minimize cartilage atrophy.

Bone Density

Walking retains bone mineral content and should be started as early as possible in the postinjury phase to reduce mineral loss. Nearly one-half of the mineral content below the lesion level is lost within the first year after injury, so walking is vital to bone health. Another recent study suggests that there is an association between circulating sclerostin and bone density in chronic SCI. Sclerostin is a protein that is produced by the osteocyte; it has anti-anabolic effects on bone formation. Levels of sclerostin, a biomarker of osteoporosis severity, were reduced in patients with SCI who used a wheelchair compared with individuals with SCI who walked regularly. Circulating sclerostin was deemed a biomarker of osteoporosis severity in chronic paraplegia rather than a mediator of ongoing bone loss. This finding was in contrast to animal models of mechanical unloading whereby high sclerostin levels suppress bone formation acutely. Bone loss can also be asymmetric in the lower limbs because of walking asymmetries in patients with incomplete SCI (iSCI).

Quality of Life

A change in mobility within the first year after injury can significantly impact perceived quality of life. Individuals with SCI who transitioned from walking at discharge to wheelchair use have low quality-of-life indicators, including high pain and depression scores. The data suggest that marginal ambulators be encouraged to work toward functional independence from a wheelchair rather than depend on primary ambulation during acute rehabilitation. Self-help mental health programs should also be included for inpatient ambulators and those who are discharged as ambulators. Some patients may also have unrealistic expectations about walking that may cause the activity to be abandoned, for example, that it will lead to complete recovery of walking function or recovery from SCI altogether.

Clinical Decision Making

Understanding individual ambulation deficits is critical for clinical decision making because many patients with iSCI require gait reeducation, especially for those at the AIS D level (see Table 1 ). The ambulation prognosis generally depends on muscle power loss, degree of spasticity, type of lower limb joint deformity developed, and availability of treatment. As an adjunct to physical examination and observation, gait analysis can inform treatment with measures of 3-dimensional dynamic joint range motion (kinematics) and estimation of joint forces (kinetics) at the hip, knee, and ankle. These measurements can be combined with walking EMG and energy cost measures to fully understand the gait disturbance.

Assessments to Measure Walking Function and Recovery

For many years, the initial level of injury and the severity of motor and sensory impairment were considered to reliably predict neurologic recovery of function after SCI; however, it is now known that using impairment scales to predict walking function is unrealistic. The AIS conversion outcome measure is poorly related to the ability to walk in patients with traumatic SCI (van Middendorp and colleagues, 2009). Instead, composite measures are recommended to predict the recovery of walking capacity and function. Outcome measures have evolved to measure the effectiveness of newer activity-based therapies in clinical trials. For example, 6 different outcome measures were related to walking function improvement in a randomized clinical trial for walking plasticity after SCI : (1) motor strength; (2) balance; (3) Walking Index for SCI (WISCI); (4) walking speed; (5) 6-minute walk (walking capacity); and (6) locomotor functional independence measure (FIM), a disability measure. An effort is currently underway to develop a more contemporary functional outcome measure for use in SCI research, which will eventually lead to the SCI computer adaptive test. Functional activities that are important to patients with SCI have been selected using focus group discussions comprised of patients with SCI and clinical staff conducted at 6 US National Spinal Cord Injury Model Systems Programs. The item pool included 326 functional activity items fitting into categories from the International Classification of Functioning, Disability, and Health framework. This item pool is being field tested to develop a calibrated item bank.

Measuring the progress of walking through recovery or reeducation therapy requires using measures that standardize injury severity and walking capacity. Standardized severity measures are detailed in the 2011 International Standards for Neurologic Classification of SCI, the clinical gold standard. Measurements of walking capacity have evolved into valid, reliable, and responsive instruments, including the WISCI II; the Spinal Cord Independence Measure (SCIM); the Spinal Cord Functional Ambulation Profile (SCI-FAP); and timed tests, such as the 10-minute walk test (10MWT) and the 6-minute walk test (6MWT). These measurements are necessary for understanding recovery mechanisms and for separating neurologic improvement from adaptation through rehabilitation.

Baseline examination accuracy is especially critical in the acute phase of injury for determining spontaneous walking recovery. Categorical scales, such as the WISCI, generally have floor and ceiling effects, whereas timed measures have excellent reliability, construct validity, and responsiveness to change in measuring SCI walking function. The psychometric properties of these measures are variable, although those developed specifically for the SCI population have excellent reliability and validity. Eight disability outcome measures have been evaluated for acute traumatic SCI. The SCIM had validity and responsiveness and was the best comprehensive measure of functional recovery during rehabilitation, even after discharge. These findings were endorsed by The Spinal Cord Injury Solutions Network. Although initially after the injury, walking capacity and the SCIM mobility items were moderately correlated, the correlations improved at 6 and 12 months. When the patients were divided by injury level, the mobility items were only initially responsive for those at levels AIS A and B. For those at level AIS C and D, the SCIM had responsiveness during the first 6 months; furthermore, the correlation with walking capacity increased over time after injury in those with AIS C but decreased in those with AIS D. In addition, walking capacity was more highly correlated with indoor mobility compared with outdoor mobility. Although the WISCI has validity and reliability for those with acute SCI, more psychometric studies are needed for those with chronic SCI. In addition, some WISCI II categories are redundant and the test has ceiling effects that limit its usefulness.

Timed walking tests, specifically the Timed Up and Go (TUG), the 10MWT, and the 6MWT, are valid and reliable measures for assessing walking function. The reliability of the TUG and 10MWT is negatively influenced by poor walking function, as assessed in a group of 75 patients. Furthermore, although the relationship between the TUG and the 10MWT was strong, it changed over time. In addition, this study revealed that the WISCI II had internal redundancy. The best measure to assess walking capacity was determined to be the 10MWT; but it was advised that a walking endurance measure be included, such as the 6MWT. In another study, the 10MWT and the WISCI II were used effectively to evaluate the efficacy of walking rehabilitation programs. The primary outcome measures for walking recovery and capacity are, thus, the WISCI II, 10MWT, 6MWT, and SCIM. For measuring community ambulation function, the SCI-FAP should be used because it incorporates the timed performance of 7 tasks, including walking and negotiating obstacles, doors, and stairs.

Walking Function Recovery

In those with motor iSCI, a combination of parameters gives a reliable prediction of walking stratification. Eleven measures from the subacute injury period were related to ambulatory outcome measures 6 months after injury, including clinical examination, tibial somatosensory evoked potentials (tSSEP), and demographic factors. The Lower Extremity Motor Score (LEMS), in combination with other measures, can predict walking at a later stage. However, the percentage of correct predictions in patients with paraparesis was lower for those who had a poor walking outcome. The authors’ clinical algorithm also identified a subgroup of patients with tetraparesis and poor ambulatory recovery. The following algorithms were determined:

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  Paraparesis algorithms

  
  
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  WISCI II prediction Z = −13.39 + 0.1(LEMS) + 0.12 (pin prick*)

  
  
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  *Using AIS as the second factor provided similar predictions.

  
  
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  6 – minute walk prediction Z = −0.28 + 0.28(LEMS) – 0.09 (age**)

  
  
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  **Adding age as the second factor did not increase the percentage of correct predictions but did improve the goodness of fit.

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  Tetraparesis algorithms

  
  
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  WISCI II prediction Z = −10.96 + 0.28 (LEMS) + 1.51 (minimum tSSEP)

  
  
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  6 – minute walk prediction Z = −354.02 + 10.24 (LEMS) + 61.96 (AIS)

Muscle Strength

After an iSCI, those with relatively preserved leg muscle strength have a greater chance for improvements in walking speed after locomotor training (Yang and colleagues, 2011). Lower extremity muscle strength, measured with the manual muscle test can identify key muscle groups related to walking speed improvements. These groups were the knee extensors, knee flexors, ankle plantar flexors, and hip abductors. Although these results are exploratory, they suggested that preserved muscle strength in the legs after iSCI would predict speed improvements after locomotor training. Quadriceps strength alone can be a predictor of walking function. Crozier and colleagues found that patients with motor incomplete injuries who recovered quadriceps strength of greater than 3/5 by 2 months after injury, as tested by the manual muscle test, had an excellent prognosis for ambulation at 6 months. The 3/5 value signified that they could flex and extend the knee against gravity without manual resistance where 5/5 would be normal function. They defined functional ambulators as those patients who were able to walk in the household and/or the community; nonambulators were those who did not ambulate or did so only for exercise.

Cause

Functional outcome may depend on SCI cause, thus comparisons were made between individuals with inflammatory myelopathies and traumatic spinal cord lesions. This study showed that the functional outcome was determined by lesion level, severity, and age rather than by cause. On the other hand, in a study of elderly patients with nontraumatic SCI, differences based on cause were found in rehabilitation length of stay and functional outcomes. Patients with degenerative spinal disease and benign tumors had a higher frequency of independent walking than patients with malignant tumors or spinal abscess, and they had the shortest rehabilitation period. Furthermore, patients with vascular ischemia were less likely to be independent in their walking than those with degenerative spinal disease and benign tumor, and they had the longest rehabilitation period. Finally, a study of 70 adults with nontraumatic SCI undergoing initial inpatient rehabilitation found that disability was significantly reduced during rehabilitation, with 76% discharged home. Of those discharged home, 15% walked unaided, 43% walked at least 10 m with a walking aid, while 42% were wheelchair dependent.

Age and Gender

In patients with nontraumatic SCI, age and gender do not significantly influence most aspects of walking rehabilitation. The only complication that was related to age was pressure ulcers. Age should not discriminate those who will benefit from walking rehabilitation, and individuals with chronic iSCI can also benefit from rehabilitation (Gorgey and colleagues, 2010). Even a twice-weekly dose of body-weight-supported treadmill training (BWSTT) can promote motor recovery for walking when accompanied with resistance training. For example, 10 weeks of BWSTT and resistance training for the knee extensor muscles can enhance walking function as found in one case study. Initially, the patient was a short-distance ambulator (<50 ft) who primarily relied on a power wheelchair and, after training, recovered the independent use of bilateral crutches to walk 200 ft and increased their overground walking speed. The FIM locomotion score increased from 3 to 6, the Berg balance score increased from 11 to 41, and the WISCI score increased from 1 to 10. Three months after discharge, independent functional walking was maintained.

Independence and Walking

The ability to walk might be associated with greater independence and well-being after an SCI. In investigating the association of the locomotion mode with health and well-being, Krause and colleagues found associations between locomotion independence and every health and well-being outcome, whereas nonindependent, nonambulators had poor health and well-being outcomes. Those who ambulated did not, however, uniformly report better outcomes than wheelchair users. For example, those who depended on others for walking assistance had less favorable outcomes.

Weighing the Risks and Benefits of Walking

Along with the benefits from walking are accompanying risks. The problems encountered by those who walk in the SCI population range from shoulder pain to an increased risk of falling. Shoulder pain is typically thought to be related to manual wheelchair use; but in those with chronic SCI, the prevalence of shoulder pain was 33.3% in participants walking without assistance; 47.6% in participants using crutches, canes, or walkers; 46.7% in motorized wheelchair users; and 35.4% in manual wheelchair users. It is, therefore, critical to assess the mechanical and nonmechanical factors that can lead to shoulder pain. Walking can also increase the risk of falls and must be addressed with patients. Brotherton and colleagues identified factors that were independently associated with having had a fall in the past year. The odds of falling were lower with those who had better current perceived health, those who had better perceived health compared with a year ago, individuals who exercised more frequently, and those who used a walker. In addition, the fear of falling, or the self-perception of confidence as measured by the Modified Falls Efficacy Scale, might not be an accurate representation of postural stability in those with low-level paraplegia who walk with bilateral knee-ankle-foot orthoses. The Modified Falls Efficacy Scale was negatively correlated with postural control, suggesting that this scale does not reflect postural control as measured during walking in this population. Clinicians should, thus, consider fear of falling as an influential factor in postural control during rehabilitation.