Spasticity after spinal cord injury

Introduction
Unequivocally, 'spasticity' is understood to be among the symptoms resulting from injury to the upper motor neurons within the central nervous system (CNS) and is a common but not an inevitable sequelae of spinal cord injury (SCI).1, 2, 3 The most commonly cited definition for spasticity is that published by Lance in 1980:4 'Spasticity is a motor disorder characterized by a velocity-dependent increase in tonic stretch reflexes (muscle tone) with exaggerated tendon jerks, resulting from hyperexcitability of the stretch reflex, as one component of the upper motoneuron syndrome'. There remains, however, discrepancy in the literature about the definition of spasticity; whereas some authors include symptoms such as clonus, hyperactive tendon reflexes, and spasms within the umbrella term 'spasticity',1, 5, 6, 7 others discuss these same symptoms as related to but separate from spasticity, which is defined by these authors as increased muscle tone.3, 8, 9, 10, 11 Decq2 recently has suggested the use of a modified definition, whereby spasticity, in general, is defined as a symptom of the upper motor neuron syndrome characterized by an exaggeration of the stretch reflex secondary to hyperexcitability of spinal reflexes. He follows by separating the various components of spasticity into sub-definitions: (1) intrinsic tonic spasticity: exaggeration of the tonic component of the stretch reflex (manifesting as increased tone), (2) intrinsic phasic spasticity: exaggeration of the phasic component of the stretch reflex (manifesting as tendon hyper-reflexia and clonus), and (3) extrinsic spasticity: exaggeration of extrinsic flexion or extension spinal reflexes. Throughout the discussion to follow, the modified definition of spasticity suggested by Decq2 will be utilized in order to clearly differentiate between the various spasticity-related symptoms that are experienced by individuals with SCI.
The literature has shown that 65–78% of sample populations of individuals with chronic SCI (1 year postinjury) have symptoms of spasticity.6, 12 Although unclear, it has been suggested that the American Spinal Injury Association (ASIA) classification of SCI (severity) and level of injury may predict the likelihood of developing spasticity; for example, in individuals with cervical SCI, 93% of those diagnosed as ASIA A and 78% of those diagnosed as ASIA B–D reported having symptoms of spasticity, whereas in individuals with thoracic SCI, 72% of those diagnosed as ASIA A and 73% of those diagnosed as ASIA B–D reported symptoms of spasticity.6 The greater incidence of lower motor neuron injury associated with lower-level injuries results in a reduced tendency for spasticity development in these individuals.6, 12 Whereas the resolution of spinal shock may coincide with an increase in spasticity symptoms,12 there is no clear relationship between the presence of spasticity symptoms and time since injury beyond the spinal shock period.6
Spasticity has the potential to negatively influence quality of life (QOL) through restricting activities of daily living (ADL), inhibiting effective walking and self-care, causing pain and fatigue, disturbing sleep, compromising safety, contributing to the development of contractures, pressure ulcers, infections, negative self-image, complicating the role of the caretaker, and impeding rehabilitation efforts.3, 6, 7, 13, 14, 15, 16, 17 Reports of problematic spasticity 1, 3, and 5 years following SCI occurred in 35, 31, and 27% of a sample of a population-based cohort of SCI survivors reported to the Colorado Spinal Cord Injury Early Notification System.18 Similarly, of those individuals reporting spasticity in the Stockholm Spinal Cord Injury Study, 40% reported their spasticity to be problematic, in that ADL were restricted and/or the spasticity caused pain.19 In a study by Sköld et al,6 20 and 4% of their total sample perceived their spasticity to restrict ADL and cause pain, respectively. Although Krawetz and Nance20 have identified that severity of spasticity is among the factors that can reduce the degree to which walking is effective in functional ambulators after SCI, Norman et al21 have emphasized that, despite the common association between spasticity and clinical signs of abnormal gait, the nature of this relationship remains unclear. Furthermore, it must be noted that, although spasticity can have a negative impact on QOL, it has been suggested that symptoms of spasticity may increase stability in sitting and standing, facilitate the performance of some ADL and transfers, increase muscle bulk and strength of spastic muscles (thereby helping prevent osteopenia), and increase venous return (possibly diminishing the incidence of deep vein thrombosis).10, 14, 15, 16 This potential for a beneficial effect of spasticity on QOL has a large impact upon decisions regarding its management.7, 16
The use of varied definitions of spasticity complicate its valid and reliable assessment.14, 22 While the Ashworth and modified Ashworth scales14, 15, 23 are commonly used to assess the severity of spasticity, there is some question about their validity in the lower limbs of persons with SCI.24 As spasticity outcomes vary between clinical patient groups and depend on a variety of factors within each individual, a battery of assessment tools is recommended, incorporating clinical, electrophysiologic, neurophysiological,25 and/or biomechanical techniques.14, 26, 27 It is important to note that there are generally poor correlations among clinical scales and, further, reductions in spasticity are not necessarily correlated with improvement in function.27, 28, 29 The lack of agreed-upon measures of spasticity as a whole or of the various 'components of spasticity' limits the quantification of physical status and the study of effectiveness of management strategies.27 The ideal scale should not only quantify the degree and nature of the spasticity, but patient satisfaction, global function, and technological assessment should be considered.29
Pathophysiology of spasticity in SCI
In general, spasticity is classified as a symptom of the upper motor neuron syndrome, characterized by an exaggeration of the stretch reflex secondary to hyperexcitability of spinal reflexes.2 Upper motor neurons originate in the brain and brain stem and project to lower motor neurons within the brain stem and spinal cord.11 The lower motor neurons are of two types, both of which originate in the ventral horn of the spinal cord: (1) alpha motor neurons project to extrafusal skeletal fibers and (2) gamma motor neurons project to intrafusal muscle fibers within the muscle spindle.11 With a lesion of the CNS comes interruption of the signals sent via the upper motor neurons to the lower motor neurons or related interneurons. Immediately following SCI, a period exists whereby the individual presents with flaccid muscle paralysis and loss of tendon reflexes below the level of the lesion.5 This period was first described in 1750, with the term 'spinal shock' introduced by Marshall Hall in 1850.30 Spinal shock has been reported to end from 1 to 3 days31 to a few weeks postinjury, with the gradual development of exaggerated tendon reflexes, increased muscle tone, and involuntary muscle spasms:5 the symptoms of spasticity. Recent animal research suggested that a recovery of relatively normal motor neuron excitability and plateau potential behavior (sustained depolarizations), in the absence of normal inhibitory control to turn off plateaus and associated sustained firing, may be implicated in the recovery of spinal shock following SCI.32
Intrinsic tonic spasticity
Decq2 has differentiated intrinsic tonic spasticity (increased muscle tone) as that component of spasticity resulting from an exaggeration of the tonic component of the stretch reflex. Briefly, the stretch reflex is a monosynaptic reflex pathway that originates in the muscle spindles embedded parallel to the muscle fibers and travels via a Ia afferent to the spinal cord, where it synapses either first with interneurons or directly with an alpha motor neuron innervating the muscle from which the stimulus originated.11 The tonic component of the stretch reflex associated with increased muscle tone results from a maintained stretch of the central region of the muscle fibers and the reflex is polysynaptic.11 Upon a sustained stretch, both type Ia and type II afferents (from secondary spindle endings) synapse with interneurons within the ventral horn of the spinal cord. Synapses of the interneurons with alpha motor neurons facilitate contraction in the muscle being stretched.11
It is the hyperexcitability of this tonic stretch reflex that is commonly thought to result in increased muscle tone in response to passive stretch following SCI.3 This hypertonia is velocity-dependent, with faster stretching velocities being associated with greater amounts of reflex activity.3 The development of tonic stretch reflex hyperexcitability could be due to a lower threshold, an increased gain of the stretch reflex, or a combination of the two.22 The resultant increase in muscle tone is thought to be due to a combination of increased denervation hypersensitivity2, 3, 5, 9, 33 and changed muscle properties.11, 13, 22, 34, 35 Denervation leads to an initial downregulation of neuronal membrane receptors, followed by an upregulation, with enhanced sensitivity to neurotransmitters.2 Gradual changes in muscle properties also occur following SCI, such as fibrosis, atrophy of muscle fibers, decrease in the elastic properties, decrease in the number of sarcomeres, accumulation of connective tissue, and alteration of contractile properties toward tonic muscle characteristics, which likely contribute to the increased passive tension.11, 13, 22, 34, 35, 36
Intrinsic phasic spasticity
Intrinsic phasic spasticity encapsulates symptoms such as tendon hyper-reflexia and clonus, and is due to exaggeration of the phasic component of the stretch reflex.2 Tendon hyper-reflexia is identified as an exaggerated muscle response to an externally applied tap of deep tendons.7 Reduced presynaptic Ia inhibition is thought to play an important role in this hyper-reflexia, as the occurrence of reduced presynaptic inhibition of group Ia fibers appears to correlate with the excitability of tendon reflexes.36
Clonus has been defined as 'involuntary rhythmic muscle contraction that can result in distal joint oscillation'37 and most often occurs at the ankle.2, 7, 9 Clonus is elicited by a sudden rapid stretch of a muscle.38 The prevailing theory explaining the underlying mechanism responsible for clonus is that of recurrent activation of stretch reflexes.11, 37, 38 According to this theory, dorsiflexing the ankle causes activation of the Ia muscle spindle afferents and induces a reflex of the triceps surae, resulting in plantar flexion of the ankle.11, 37, 38 This reflex contraction is brief, essentially phasic, and ceases rapidly.2 The muscle then relaxes, causing the ankle to be dorsiflexed once again, due either gravity or the stretch being sustained by an examiner.2 The result is a new stretch reflex, etc.2, 37 Ultimately, it is the disinhibition of the stretch reflex due to interruption of descending influences with SCI, that is thought to cause exaggeration of the phasic stretch reflex pathway and, hence, clonus.3
The second theory is that clonus is the result of activity of a central oscillator or generator within the spinal cord, which rhythmically activates alpha motor neurons in response to peripheral events.37, 38 Beres-Jones et al37 outline observations that they feel support such a hypothesis: (1) reports of similar frequencies of clonus among ankle, knee, and wrist muscles, (2) observations that the clonus frequency is not entrained by the input frequency, suggesting that clonus cannot be solely stretch-mediated, (3) the finding that stimuli other than stretch evoke clonus, and (4) the observation of a refractory period following the clonic EMG burst where tendon tap, H-reflex stimulation, and vibration fail to elicit an efferent response. Therefore, whereas reduced presynaptic inhibition of group Ia fibers appears to be among the contributing factors to tendon hyper-reflexia, the underlying mechanism of clonus has not been clearly elucidated.
Extrinsic spasticity
In addition to the various intrinsic factors that contribute to symptoms of spasticity, involuntary muscle spasms can also occur in response to a perceived noxious stimulus originating extrinsic to the muscle: extrinsic spasticity.2, 3, 7 Flexion spasms are the most common form of extrinsic spasticity, triggered by afferent input from skin, muscle, subcutaneous tissues, and joints (collectively referred to as 'flexor reflex afferents'). These flexor reflex afferents mediate the polysynaptic reflexes involved in the flexion withdrawal reflex.3, 35, 39 SCI can interrupt the inhibition of these reflexes by supraspinal pathways, making them hyperexcitable.2, 3, 40 In other words, whereas flexor withdrawal reflexes occur normally in individuals without SCI, upon disruption of normal descending influences, the threshold for the flexor withdrawal reflex may become lowered, the gain of the system may become raised, or both may occur together.3 A recent study has provided evidence to implicate plateau potentials in the spinal interneuronal and motoneuronal circuitry in the hyperexcitability of flexion withdrawal reflexes in individuals with chronic SCI.41 Intrasegmental polysynaptic connections cause the flexor reflex initiated by a localized stimulus to generate a widespread flexor spasm, which can appear as a coordinated flexion of all joints of the leg.35, 39

Management of spasticity following SCI
In contrast to the general lack of agreement within the literature about the definition and evaluation of spasticity, there appears to be widespread agreement that decisions regarding the management of spasticity must be based on the goal of achieving balance between the useful and detrimental effects of spasticity on an individual's QOL.2, 10, 16, 34 The management of spasticity may be desired for the reduction of 'passive problems', such as preventing contracture, reducing pain, facilitating splint wearing, easing positioning and hygiene, and preventing contractures, or of 'functional problems', including the individual's reduced ability to perform useful work with the motor system.9
In general, no one treatment option will successfully manage spasticity in all individuals; the most conservative tactics are utilized first, with a progression from physical rehabilitation modalities, pharmacologic interventions, injection techniques, intrathecal baclofen, and lastly, surgery.15 In general, local treatments are used primarily by individuals with spasticity predominating in only certain muscle groups, such as which occurs mainly in individuals with stroke or traumatic brain injury.42 In the case of SCI, the distribution of spasticity tends to be more diffuse, making regional or systemic treatment preferable.34 The decision whether or not to treat spasticity and, if so, in what manner, is summarized nicely in a flow chart by Parziale et al (Figure 116).