Introduction

Injuries to the spinal cord result in profound disability and involve many body systems, resulting in severe physiological changes. The most obvious consequence is paralysis, which occurs immediately after injury and may persist throughout life ( ). Paralysis and deconditioning are responsible for reduced mobility and independence and play a significant role in secondary health complications, such as cardiovascular and respiratory dysfunction, metabolic syndrome, bone demineralization, immunosuppression, and musculoskeletal deterioration ( ).

Despite all rehabilitation efforts to promote recovery of the injured spinal cord, more than 50% of individuals face long-term disability ( ). Traditionally, rehabilitation strategies have been successful in improving independence mainly by providing compensatory strategies focused on the use of the preserved muscles above the level of injury and using leverage and momentum to move weak or paralyzed body parts. However, most individuals only have access to physical interventions during the acute and subacute phases of injury through inpatient and outpatient rehabilitation programs ( ). After discharge from hospital, most individuals with a spinal cord injury (SCI) face several barriers to continue to exercise and be active in the community, such as lack of specialized professionals, programs, and facilities. Inactivity and sedentary behavior during the chronic phases of injury can lead to decline in mobility and independence and impose a greater risk of developing co-morbidities ( ).

The reduction in physical activity levels and the systemic impairments after injury result in a sedentary lifestyle ( ). Sedentary behavior and inactivity are the main risk factors for the development of metabolic and cardiovascular disorders and reduction in muscle strength and aerobic capacity. Therefore, it is necessary to offer specialized physical therapies, exercise programs, sports, and recreation to individuals with SCI to increase their physical activity levels and improve health ( ).

Over the past years, there has been growing evidence related to the central nervous system plasticity, repair, and regeneration. However, the concept of an irreparable, “hard-wired” nervous system still guides rehabilitation after SCI in most countries. In general, physical rehabilitation still focuses solely on teaching patients how to achieve day-to-day function by using compensatory strategies and assistive devices, despite significant neurological deficits ( ).

Activity, defined as both function-specific motor tasks and exercise appears to be a necessity for optimization of functional, metabolic, and neurological status in chronic paralysis ( ). Exercises that target systems below the level of injury (sensory, musculoskeletal, vascular) are essential to promote recovery after SCI and prevent secondary complications related to paralysis, such as pressure injuries, joint contractures, and pneumonia, promoting a better life ( ). And even more important, as the life expectancy after SCI approaches that of the able-bodied population and when the worldwide number of survivors continues to grow to over 2 million people ( ).

The evidence regarding spinal cord plasticity that emerged from animal ( ) and human studies ( ) and the knowledge that augmented sensory stimulation and repeated active movement can lead to functional improvements ( ) led to the necessity of developing more comprehensive rehabilitative interventions. New interventions focused on functional improvement through neurological recovery aroused. Those interventions were termed Activity-Based Therapies (ABT), and numerous programs emerged globally with the goal of assisting people with SCI at any level or severity to achieve their maximal potential for recovery ( ).

Recovery after spinal cord injuries

The advances in the acute medical management of people with a spinal cord injury (SCI), such as early spinal decompression, pharmacological interventions, and intra-operative temperature management ( ) have been successful in reducing secondary neuronal damage and the extension of the injury, resulting in greater clinical recovery and better outcomes. Neuroprotective strategies have reduced the incidence of complete injuries and have increased the chances for functional recovery.

However, the intrinsic potential for recovery of the spinal cord after injury seems to be limited and not responsive to the conventional treatment strategies. It is well known that during the first weeks, and even months after injury, spontaneous recovery may occur due to the resolution of the swelling and return of the neural activity below the lesion site in response to the acute injury ( ). Spontaneous motor and sensory recovery have been reported during the first 2 years, with major recovery occurring between 3 and 6 months post-injury ( ). Critical factors in determining recovery in the first year after a traumatic SCI include the initial neurological level of injury, initial motor strength and, most importantly, the severity of injury. investigated the rate of neurological recovery of 987 individuals with a traumatic SCI during their first 5 years and found small degrees of neurologic recovery between 1 and 5 years, with 5.6% of cases presenting late conversion from a sensorimotor complete to an incomplete lesion status, demonstrating that spinal cord plasticity, similarly to the brain, can persist for many years post-injury.

Substantial functional recovery was seen after SCI in animals in response to training ( ). The degree of sensorimotor recovery was defined largely by the type and intensity of motor training and sensory stimulation provided following the injury ( ). Recovery after SCI has been related to the spinal circuits’ capacity for automaticity and plasticity. Automaticity is the ability of the spinal cord to perform complex motor tasks without supraspinal inputs and plasticity refers to the ability to recover or change, potentially stimulated by biochemical changes at the cellular level in the spinal cord. There is evidence that plasticity can be induced by physical activity, thus leading to sensorimotor recovery ( ). The physiological mechanisms behind spinal cord plasticity are possibly related to changes in the cerebral cortex, growth of new axonal branches, remodeling of synapses, changes in neuronal excitability, and modulation of neurotransmitters in the spinal cord ( ).

Training and exercise seem to play an important role in enabling spinal plasticity by inducing changes at the cellular and molecular levels. It is suggested that the spinal cord has the ability to change when the sensory circuits are repeatedly activated ( ). This capacity can be due to the activation of complex neuron networks, often termed central pattern generators (CPGs), which are responsible for organizing complex motor movements within the spinal cord.

In humans, similar responses to activity and training have been found, demonstrating the capacity of the human spinal cord to respond to sensory inputs and adapt after injury. Repetitive training is critical for promoting changes to the spinal networks resulting in functional recovery. Therefore, physical interventions aimed to optimize the neuroplastic mechanisms of the spinal cord are potential tools to promote functional recovery ( ).

Furthermore, recent studies have shown that approximately 50% of the injuries functionally classified as sensorimotor complete (International Standards for Neurological Classification of Spinal Cord Injury—ISNCSCI A) are actually anatomically incomplete with some degree of preservation of the nervous fibers. This new knowledge unveils the potential for recovery of injuries previously considered immutable, especially in response to interventions aimed at increasing the excitability and activation of the preserved spinal circuitries ( ).

In summary, the scientific findings that support the capacity of the spinal cord to change and recover, even years after injury, warrant that clinicians should employ interventions aimed at the preservation of the function of spinal neuronal circuits under the level of injury as an important condition for regeneration ( ). The dysfunctional central nervous system (CNS) reorganization and repair are dependent on maintaining an optimal level of neurological activity above and below the site of injury ( ).

Conventional rehabilitation after spinal cord injuries

Traditionally, management of a person with SCI involves the determination of the person’s level of injury and functional capacity, and then the generation of a problem list of activity limitations and prescription for therapies, with the overall goal of having the patient achieve their maximum functional capacity, according to the overall level and severity of neurological injury ( ).

Often, clinicians are guided by the World Health Organization International Classification of Functioning, Disability and Health (ICF) framework to assess the rehabilitation needs of people with SCI. The ICF is an integrative and biopsychosocial approach that comprehensively describes the impact of a health condition and health interventions on an individual’s functioning. It consists of assessing three domains: (1) Body structure and functioning; (2) Activity limitations; and (3) Participation restrictions ( ). The ultimate goal of rehabilitation after SCI is to enable the person to return to a productive and satisfying life ( ). Therefore, rehabilitative interventions delivered in the community should focus on strategies to increase activity levels in order to decrease participation restrictions.

Conventional physical rehabilitation aims to restore independence, physical capacity, and community participation, focusing on mobility and self-care ( ). Exercise therapy is often employed to the preserved or partially preserved muscles to improve strength, regulate tone and augment muscle length and joint mobility. Moreover, increased fitness, reduced pain and prevention of cardio-metabolic conditions are priorities. Retraining of motor tasks, such as hand and arm function, bed mobility, transfers and wheelchair use, standing, and walking are frequent goals during inpatient rehabilitation ( ).

To achieve the rehabilitation goals, therapists rely substantially on providing compensatory strategies focusing on the use of the preserved muscles above the level of injury and using leverage and momentum to teach patients how to move weak or paralyzed body parts. Orthotic devices and modifications to the environment are provided to compensate the loss of function, and the use of the upper limbs is encouraged to substitute for lacking movements of the trunk and lower limbs ( ).

While these strategies are effective in increasing mobility, independence and participation ( ), they do not target the recovery of the affected areas below the site of injury and do not consider that further functional gains may be possible. They also neglect the need of exercise and activity to the paralyzed areas in order to preserve the body systems below the site of injury and to prevent the deleterious effects of non-use ( ). Hence, in the last decades, new physical therapies based on the advances in spinal cord neuroplasticity have emerged, leading to a change in the focus of rehabilitation after SCI from the compensatory model to a recovery-based model ( Fig. 1 ).

Differences between the two concepts of rehabilitation in spinal cord injuries.

Activity-based therapies

Locomotor and gait training

Locomotor training (LT) aims to improve sensory, motor and autonomic functioning, health and quality of life. The main focus is to promote recovery of postural control and walking after SCI. LT is based on the principles derived from studies using animal models that demonstrated recovery of the ability to weight bear on the hind limbs and walk after exposure to repetitive step training (i.e., by training for the specific motor task) ( ).

The LT protocol developed by the NeuroRecovery Network involves the use of an overhead body-weight support system attached to a harness where the individual is suspended over a treadmill. Trained therapists facilitate control of balance and manually assist trunk and leg movements during stepping and standing to generate sensory information that is consistent with locomotion ( Fig. 2 A ). In conjunction with the body-weight supported treadmill training, LT programs usually include an overground training component, where activity limitations are assessed and task-specific training incorporating sensory feedback is performed outside the body-weight support system with the aim to contribute to functional recovery ( ; ).

Examples of locomotor and gait training. (A) Body-weight support treadmill locomotor training, (B) body-weight support overground gait training, (C) overground gait training with walker and assistance, (D) overground gait training in parallel bars and assistance, (E) overground gait training with crutches and supervision.

LT is the most investigated ABT intervention to date and there is mounting evidence of its benefits after acute and chronic SCI. A large number of studies have investigated the effects of LT on walking ability in individuals with incomplete SCI and have demonstrated improvements in walking speed, distance and coordination ( ; ; ). Moreover, neurological recovery has been reported through studies that showed increments in lower extremity motor score and ISNCSCI classification after LT ( ). Gains in balance, functional mobility and independence were also reported ( ).

LT can also be deployed as an exercise modality to improve general health after complete and incomplete SCI. Improvements in cardiorespiratory health ( ), reversal of muscle atrophy ( ), and enhanced autonomic function related to blood pressure control have been reported after LT ( ).

Although LT has demonstrated to be beneficial for individuals with SCI, the training volume required to achieve significant gains is high, ranging from 4 to 5 times per week for 1.5 h per session. Hence, its application in community rehabilitation settings is not always feasible due to the challenges in maintaining adherence and the financial burden to the participants. Therefore, community-based clinics often offer multimodal ABT programs, where LT can be a component of the rehabilitation program. It is worth noting that LT is also employed as a training strategy with the overall aim is to promote neurological recovery and health benefits. The goal may not always be related to walking.

Task-specific gait training strategies are also employed in ABT programs with the aim to promote functional recovery of walking. Similarly to traditional rehabilitation, ABT programs may use external assistance, walking aids and orthotic devices to retrain walking according to the client’s abilities and functional goals, as illustrated in Fig. 2 B–E. However, in ABT, the prescription of orthotic devices and walking aids is delayed, when compared to traditional rehabilitation, and will occur only when the strategies for recovery are exhausted and the recovery of motor function is not achieved. LT and other modalities of gait training can be used in ABT programs as a form of whole-body exercise with the aim of improving gross motor function (when walking is not a goal), and cardiovascular fitness due to the physiological benefits of moving in the upright position.

Neuromuscular electrical stimulation (NMES) and functional electrical stimulation (FES)

When applied to certain body systems, electrical currents have the property of eliciting an electrical response in different cells, such as muscle and neurons. Over the years, novel currents and devices have been developed to safely elicit a neurological response, such as muscle contraction, in paralyzed or weakened muscles to assist individuals with different medical conditions, including SCI, to gain muscle strength and reverse the deleterious effects of paralysis.

Neuromuscular stimulation (NMES) is the technical name used when electric current is used to reduce deficits resulting from clinical conditions, such as non-use. NMES can increase the individuals’ participation in voluntary activities producing contractions of the paralyzed muscles that are still innervated, and as a result can improve muscle trophism, strength, and tone ( ).

Functional electrical stimulation (FES) is a subtype of NMES, in which the stimulation of a nerve or a paralyzed muscle promotes assistance to specific and functional movement such as cycling as illustrated in Fig. 3 A , assisted walking ( Fig. 3 B) or grasping ( Fig. 3 C and D). FES and other types of neuromuscular electrical stimulation improve blood circulation, range of motion, muscle strength and endurance, and reduce spasticity, atrophy and loss of bone mineral density, while increasing metabolism and cardiorespiratory function ( ; ).

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