Lower Extremity

Cervical, thoracic, and/or lumbo-sacral SCI, regardless of age at injury, often results in trunk and lower extremity paralysis and/or weakness. The resulting functional impacts include a spectrum of limitations of trunk control and balance, standing, transferring and walking. The approach to these impairments and their functional impact has primarily involved the introduction of braces and assistive devices to compensate for paralysis/weakness, achieving functional alternatives for the tasks of upright trunk posture, standing, and walking. This treatment approach is consistent with the assumption that the impairments and functional impact of SCI are permanent. Recent evidence, however, points towards some potential for partial functional recovery below the level of the spinal cord lesion. From this vantage point, physical rehabilitation extends to recovery-based strategies tapping into the intrinsic biology of the neuromuscular system to partially restore its capacity for motor control.

The ‘Lower Extremity and Trunk’ evidence for Spinal Cord Injury Research Evidence is presented relative to three therapeutic goals: 1) Trunk control, 2) Standing, and 3) Walking. The literature is further presented within the context of two rehabilitation approaches: 1) compensation (i.e., development of new adaptive behaviours, use of devices/equipment) and 2) restoration (or recovery). Both perspectives have guided the development and use of outcome measures and therapeutic interventions to achieve the goal of improved function. Accordingly, the tables of evidence for lower extremity and trunk outcome measures and interventions for the goals of standing, walking, and trunk upright posture are organized to differentiate the ‘solutions’ as either 1) compensation strategies to achieve functional alternatives or 2) restorative interventions to achieve neuromuscular capacity supporting typical functional behaviors to stand, walk, and maintain an upright trunk posture. Defining the parameters of performance for each goal is critical to compare the intervention strategies.

Discussion

Compensation-Focused Interventions for Standing and Gait/Walking

The evidence for compensation-based approaches to standing and walking in pediatric SCI spans from 1994-2017. The use of functional electrical stimulation (FES) to stand has been tested in small-scale studies and includes examination of the criteria for eligibility for surface lower extremity stimulation (Triolo et al., 1994), study of FES home use for standing/mobility (Moynahan, Mullin, et al., 1996), comparison of percutaneous intramuscular electrodes to leg braces for those with thoracic complete SCI (Bonaroti et al., 1999a; Bonaroti et al., 1999b), a 3-year follow-up study in one subject with percutaneous intramuscular electrodes (Betz et al., 2002), and FES compared to long-leg braces (knee-ankle-foot orthoses, KAFOs)(Betz et al., 2002), and FES for upright mobility (Johnston et al., 2003) and for walking via swing-to gait pattern (Johnston et al., 2005). While able to achieve standing with surface FES, researchers noted significant barriers to use of surface FES, such as the impracticality of application of electrodes for function, and reluctance of the participant to use the system for the entire day (Moynahan, Mullin, et al., 1996). Implanted FES systems showed comparable functional impact when compared to KAFOs and even better performance in accomplishing certain tasks (Betz et al., 2002; Johnston et al., 2005; Johnston et al., 2003). While promising, the most relevant information is that the FES surface and implantable systems did not advance from experimental study to clinical translation for use by children and adolescents with SCI in the home and community.

Standing frames, braces, and assistive devices to achieve upright standing and ‘walking’ (i.e., brace-walking) have also been investigated as compensatory strategies for lower-limb paralysis. Lower limb braces provide external support and joint alignment to achieve the standing position and possibly swing-through gait with a walker or forearm crutches. Vogel and colleagues (1995) provide a thorough description of the pediatric population using braces and devices to achieve standing and walking describing ‘who’ (e.g., age, injury level, time since injury), progress to a different device (e.g., parapodium to reciprocating gait orthosis, RGO), and duration of use (including age at point of change to another device, abandonment or ceasing to ambulate, i.e., approximately age 10 years).  Choksi et al. (2010) reported outcomes of 32 child and adolescent patients with subacute SCI who received inpatient rehabilitation (occupational therapy and physical therapy) using the Pediatric Evaluation of Disability Inventory.  While significant gains in distance and speed were achieved for basic indoor, outdoor locomotion and more complex locomotion (i.e., being able to carry objects and walk independently without devices) did not significantly change. Several case studies addressed the type of assistive device being used during gait training and its potential impact on outcomes (Altizer et al., 2017), thus demonstrating the merits of certain types of equipment. Research concerning the use of braces and assistive devices to achieve ‘brace-walking’ beyond the reports of by Vogel et al. 1995 and 2010 is negligible. This may mean that the use of these strategies remains the standard of care. While robotic devices for ambulation have been introduced to the market for pediatric use, scientifically reported outcomes and follow-up via research are lacking.

Recovery-Focused Interventions for Standing and Gait/Walking

The plethora of research providing foundational rationale and arguments for recovery-based approaches to achieve walking via repair of the neuromuscular system through activity-dependent plasticity (Edgerton et al., 2004) is beyond the scope of this review. This critical new knowledge of the neurobiological control of posture and locomotion, however, provides a physiological and neural basis for training strategies to focus on accessing the ‘smart’ spinal cord below the lesion for practical use. Published research in adults with SCI using activity-based locomotor training or activity-based restorative therapy have preceded research and clinical use of these strategies for children with SCI.  Most literature regarding activity-based locomotor training and activity-based restorative therapy in pediatric SCI are case studies or studies with small sample sizes. Nevertheless, they introduce the potential for a new direction in rehabilitation.

Prosser et al. (2007) and Heathcock et al. (2014) reported the benefits of ‘locomotor training’ in case studies of children during the acute phase post-injury (< 1 year) with the potential for interaction with ‘natural recovery’. In addition, the case study by Heathcock and colleagues (2014) was the first to report use of activity-based locomotor training in a child who had not yet mastered ambulation as a developmental milestone prior to their injury. In comparison, Behrman et al. (2008) and Fox et al. (2010) (follow-up) reported achievement of a reciprocal pattern of walking in a child with chronic, cervical SCI and non-ambulatory (American Spinal Injury Association Impairment Scale C, lower extremity motor score < 10) via locomotor training.  Similarly, Behrman et al. (2012), O’Donnell and Harvey (2013), and Hornby et al. (2005) reported positive outcomes in standing and walking using treadmill training for adolescents with incomplete SCI. Both manually-facilitated stepping and robotic-assisted stepping were reported, though not compared.  Similar to the literature in adult SCI, achievement or improvement in ambulation using activity-based locomotor training/activity-based restorative therapy appears most effective in those with incomplete SCI. The findings for 26 consecutively-enrolled children in a clinical activity-based locomotor training program demonstrate the high percentage of improvements in walking for children with incomplete SCI and the very low percentage of children with complete injuries who achieve even therapeutic or household ambulation (Andrea L Behrman et al., 2019). Clinicians may thus speculate that activity-based locomotor training should be abandoned for those children with complete injuries. Evidence from research with adults with complete SCI, however, may once again point the direction for children with severe SCI and motor paralysis. Recent literature on epidural stimulation combined with activity-based locomotor training to achieve reciprocal walking in adults with SCI (Angeli et al., 2018) and the use of transcutaneous spinal stimulation to enable stepping behavior in adults and a 17-year-old with acute SCI (Baindurashvili et al., 2020) may suggest important future directions (Baindurashvili et al., 2020) may for the rehabilitation of children with severe SCI and motor paralysis. Reporting the findings for adults with SCI is beyond the scope of this chapter.  Pilot work studying the use of transcutaneous spinal stimulation combined with activity-based locomotor training to enable stepping in non-ambulatory children with chronic SCI is ongoing and findings have yet to be published (Clinicaltrials.gov # NCT04077346).

Three reviews are also considered among the body of evidence for achievement of ambulation post pediatric SCI (Damiano & DeJong, 2009; Funderburg et al., 2017; Gandhi et al., 2017), and are each discussed below.

Damiano and DeJong’s (2009) systematic review explored the strength, quality, and conclusiveness evidence on the use of treadmill training and body weight support in those with pediatric motor disabilities. Of the 29 studies identified from the literature search, six involved individuals with pediatric SCI. The outcome results of using treadmill training and/or body-weight support in the pediatric SCI population were positive, with some showing large and clinically significant changes, such as progression from no ability to step, to walking independently with an assistive device by the end of training. However, the authors pointed out that since the studies identified were either individual case reports or individual subject data from a case series, conclusions regarding the efficacy of the use of treadmill training and body-weight support in children with SCI should be drawn with caution, and more controlled studies, especially those utilizing randomized designs, are needed (Damiano & DeJong, 2009).

Funderberg et al. (2017) reported evidence for three approaches: use of orthotics and assistive devices, electrical stimulation (surface and implanted), and ‘treadmill-training.’ It was noted that orthotic studies typically compare one type of orthosis to another for utility, but that the evidence for any orthotic device is not sufficient to warrant development of a clinical guideline. Electrical stimulation, while showing benefit, requires equipment, intensive training, potentially invasive procedures, and lacks long-term assessments for physiological effects and meaningful use. As noted, FES and implantable stimulation has not advanced to a level of clinical application for ambulation goals. Lastly, ‘treadmill training’ leads to use of less restrictive devices and improvements in speed, distance, capacity for walking (number of steps per hour), and community-based activity (number of steps per day) for children with varying impairment levels. Funderberg et al. (2017) recommended this mode of training for functional gains. Infant treadmill training has been reported in the context of spina bifida as potentially beneficial, yet long-term follow-up studies are needed. While not reported in the pediatric SCI literature, Funderberg et al also postulated that early implementation (i.e., at the typical age of cruising, standing, and step initiation) of therapies promoting the sensorimotor experience of walking and activity-dependent plasticity may be advantageous to children injured in utero or under one year of age.

Gandhi et al. (2017) further explored the parameters of training, reporting the many differences across cases and studies with the treadmill being a common thread across studies. In this review, understanding the intent and therapeutic goal in selecting and using specific equipment (e.g., treadmill, partial body weight support), how to perform and deliver the training and make clinical decisions, and progress a child through therapy were highlighted as critical to the success of any training program. It should also be noted that the use of the term ‘treadmill training’ to describe an intervention is felt to be insufficient and likely results in grouping of evidence and outcomes in a way that may lead to misinterpretation and misunderstanding of the therapy and its effect (Behrman et al., 2008). Gandhi et al. (2017) summarized key findings from a review of 13 pediatric studies for walking. First, there was a trend towards greater improvement in studies of greater dosage/duration of training.  Second, 10/13 studies included overground training as a transfer of skill from treadmill to the real-world environment, and this strategy appeared to be beneficial. Third, an argument was made that children with complete SCI should be included in research for walking recovery despite earlier concerns about their potential for recovery. This is based on the likelihood that children have greater potential for recovery relative to those with adult-onset SCI.

Lastly, while advocating for more rigorous studies (e.g., inclusion of blinded assessors) Gandhi et al. (2017) cautioned that the traditional randomized clinical trial may not be feasible with this ‘low-prevalence population’. Thus, the design of studies for pediatric SCI may require alternative methodological design strategies. With the very low incidence of recovery of walking in the chronic stages of SCI, non-ambulatory pediatric subjects serving as their own control should provide optimal ‘controls’, decrease heterogeneity of the sample, and allow for a smaller ‘n’. Understanding ‘who’ benefits beyond the simplistic view of SCI as ‘complete’ or ‘incomplete’ will necessitate more sensitive exploration of predictors and biomarkers for response (Mesbah et al., 2021; Rejc et al., 2020), as well as study of mechanisms for response to interventions.

Measurements: Compensation Focus and Recovery Focus

Outcome measurements for standing/walking are distinct in whether they do or do not take into account the mechanism through which the outcome is achieved (i.e., via compensatory strategies or recovery of function).  Measures that allow the use of compensation strategies emphasize achievement of a ‘functional’ goal regardless of the behavioral strategy or equipment used to accomplish the goal. For instance, a patient may successfully move from sitting to standing using a walker to assist with balance, and strength of the arms to compensate for leg weakness. Achieving standing is the only goal and employed compensation strategies are not “counted against” achievement of the goal. The many outcome measures employed to assess standing/walking in SCI that do allow patients to use compensatory strategies without penalty include:

• Pediatric Evaluation of Disability Inventory
• Spinal Cord Independence Measure
• Time to complete a task
• Functional Independence Measure
• Gait speed
• Years using a device
• Functional Independence Measure for Children
• Timed Up and Go
• Walking Index of SCI I and II – in some instances (e.g., Walking Index of SCI II), the use of equipment is accounted for in the scoring, but equipment and compensation are allowed.

A recovery-focused measure, in comparison, provides a means, even stepwise, to assess the neuromuscular capacity to perform a task without behavioral or device/equipment compensation. Thus, a sit-to-stand is performed and the incremental capacity to perform with a typical, kinematic pattern of trunk and limbs is assessed.  The Neuromuscular Recovery Scale and Pediatric Neuromuscular Recovery Scale (Behrman et al., 2017; Andrea L Behrman et al., 2019; Behrman et al., 2012); observational gait analysis, and the Segmental Assessment of Trunk Control (Argetsinger et al., 2019; Goode-Roberts et al., 2021) are examples of recovery- or restorative-focused measures. Compensations are not ‘allowed’ or are noted with scoring relevant to their presence or absence during task performance.

Interventions and Measurements for Trunk Control:

Trunk control is instrumental to the achievement of a variety of tasks from breathing and coughing to sitting/standing upright to reaching overhead to walking. The knowledge that SCI-induced trunk paralysis is irreversible guides the current clinical decision-making by therapists and the medical field (Schottler et al., 2012). Historically, therapy does not expect to restore function, but to adapt the task or environment to achieve a novel solution to the problem (Chafetz et al., 2007; Mehta et al., 2004; Mulcahey et al., 2013; Sison-Williamson et al., 2007).

Clinically, the Trunk Impairment Scale, the Gross Motor Function Classification System, and the Pediatric Berg Balance Scale have been used to measure trunk control in children with SCI. However, independent sitting and standing by participants is a prerequisite for these tests. Therefore, testing trunk control in children who have not achieved independent sitting and in children with a low functional level is limited. In addition, these tests measure trunk performance as a single unit allowing for a compensatory posture (e.g., kyphotic posture). To determine the motor impairment of trunk function, the International Standards for Neurological Classification of SCI is used by clinicians (Mulcahey et al., 2011). Unfortunately, because function of trunk muscles cannot be tested individually, the scale relies on truncal sensory perception (tested with the patient in supine) as a stand-in for trunk motor function (assuming that motor function is preserved at the truncal levels where sensation is preserved). In addition, the scale is only valid for children 6 years and above (Mulcahey et al., 2011).

A new pediatric measurement instrument, the Segmental Assessment of Trunk Control, was recently introduced and validated to assess and track improvements in trunk control in children with SCI who lack independent sitting or in whom sitting control is impaired (Argetsinger et al., 2019; A. L. Behrman et al., 2019). This evidence demonstrated improved trunk control in children with SCI post-activity-based locomotor training and has set forth a paradigm shift in our expectation of recovery of trunk function after SCI. In recent studies, surface electromyography collected during Segmental Assessment of Trunk Control and active trunk tasks revealed apparent preservation of postural extensor muscle activation after pediatric-onset SCI. This preservation reflects residual supraspinal influence on spinal motor circuits and has important implications for the potential to tap into preserved trunk activation below the lesion level in pediatric-onset SCI (Atkinson et al., 2019; Singh et al., 2020). The implications of this finding (beyond a measurable improvement in a performance score (i.e., improved Segmental Assessment of Trunk Control score) without compensation) are unclear. Further investigation is needed to determine any meaningful impact of preserved and trainable trunk control in the home, school, and community for children with SCI, as well as potential reduction of risk for scoliosis (Argetsinger et al., 2020; Goode-Roberts et al., 2021).

Conclusion

In reviewing the evidence for lower extremity and trunk control rehabilitation across time (i.e., 1994-2021), a paradigm shift in the intended therapeutic end-goal is observed. The original intent was to achieve upright trunk posture, standing, and walking as a functional goal with the implementation of external support (i.e., leg braces and assistive devices). Now, the intent is to achieve upright trunk posture, standing, and walking via the intrinsic neurobiology for the control of posture, standing, and walking. For instance, leg braces (e.g., knee ankle foot orthoses or reciprocating gait orthosis) are meant precisely as an end goal to train the patient to walk with braces. Thus, the braces serve to compensate for paralysis of the lower extremities. The braces are not a therapeutic step towards standing or walking without braces. The goal is to achieve the ‘functional’ ability to stand or walk dependent upon braces (and assistive devices) to provide external support for an extended position of the knees, stable position of the ankles, and in some cases, advance a step with brace-promoted hip flexion during gait. This functional goal for standing and walking is based on the premise that these goals are achieved only in the context of external support, that the voluntary motor control of the lower extremities is insufficient for standing or stepping, and that the functional goal of standing and stepping is meritorious for a child whether practical, developmentally-appropriate or simply desirable. Achieving standing and walking via this strategy is reported as changing with musculoskeletal growth and aging into adolescence and ultimately adulthood when for practical circumstances (e.g., speed of mobility) brace walking is abandoned for wheeled mobility.

Restorative Treatment

After a pediatric SCI, it has been assumed that paralysis is permanent, especially in the chronic period post-SCI (typically considered >1-year post SCI), and the individual will never stand or walk independently again. Upright posture and mobility provide interactions with the child at the same height as their peers, opportunity for participation in school and community. Therefore, children have been encouraged to use wheeled standers or devices such as orthoses, robotics, and FES (Betz et al., 2002; Bonaroti et al., 1999a; Bonaroti et al., 1999b; Johnston et al., 2005; Johnston et al., 2003; Vogel & Lubicky, 1995). Measurements to evaluate the uses of equipment for upright posture and mobility includes gait speed and the speed to perform a task (Betz et al., 2002; O’Donnell & Harvey, 2013). However, these measures ignore the mechanics of how the task was performed and place increased demands on the upper extremities. Furthermore, the devices that passively produce an upright posture and upright mobility are cumbersome and lead to a high rate of user abandonment, especially as the child develops into adolescence.

Edgerton et al. (1991) identified that a restoration approach may have potential for humans after SCI. His findings were based on a decade of animal research, showing the potential of motor recovery and walking after SCI. Since then, there has been a divergence between compensatory interventions (with braces and wheeled standers) and restorative interventions (including locomotor training). Over a decade of research has supported restoration interventions for children with spinal cord injuries to improve motor function below the level of the lesion (Baindurashvili et al., 2020; Behrman et al., 2008; Andrea L Behrman et al., 2019; Behrman et al., 2012; Fox et al., 2010; Heathcock et al., 2014; Hornby et al., 2005; O’Donnell & Harvey, 2013; Prosser, 2007). No intervention, compensatory or restorative-based, however, has consistently resulted in children with motor complete SCI standing or walking reciprocally independently without bracing or assistive devices. Alternatively, children and adolescents with incomplete SCI demonstrate benefits.

Restoration interventions continue to be a “new frontier” of research, with early research based on case studies (Behrman et al., 2008; Behrman et al., 2012; Fox et al., 2010; Heathcock et al., 2014; Prosser, 2007). Outcomes have measured how the movement occurs, including step length, stride length, and stepping patterns (Fox et al., 2010) and modular contributions to movement patterns across motor tasks (Fox et al., 2013). Restoration interventions require maximizing weight bearing on the legs, promoting normal kinematics, optimizing sensory cues, minimizing compensation strategies, and knowledge of the intrinsic biology for motor control: posture and locomotion, particularly contributions of the spinal circuitry and sensory input. The requirements for restoration interventions significantly contrast the approach to compensatory interventions (Behrman et al., 2008; Roy et al., 2012). The future of compensatory intervention models is focused on robotics, or potentially ‘smart orthotics’ but with no evidence to date in the scientific literature to support application in the clinic for children. Research for restorative interventions is focused on altering the state of excitability of the spinal cord via various interventions from those emphasizing the sensorimotor experience/training of posture and walking to spinal stimulation and combining interventions (Angeli et al., 2018; Gerasimenko et al., 2015; Harkema et al., 2011).