Muscular Tone and Gait Disturbances

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Chapter 5 Muscular Tone and Gait Disturbances

Muscular tone is conventionally separated into phasic and postural types. Phasic tone is the result of rapid stretching of a tendon, attached muscle, and most importantly, the muscle spindle. The response is rapid and short-lived. Postural tone is the result of a steady, restrained stretch on tendons and attached muscles, with resultant protracted contraction of the involved muscle. Gravity is the most common stimulus for this response. Postural tone is the topic primarily discussed in this chapter, and it is referred to simply as tone.

Tone is functionally defined as resistance to passive movement (i.e., resistance experienced by the examiner while the patient’s relaxed limbs are moved about the joints). Hypotonia is decreased resistance to passive movement. Hyperextensibility is an abnormally increased range-of-joint movement. Hyperextensibility of the elbows, wrists, knees, and ankles usually accompanies hypotonia but is not pathognomonic. The combination of hypotonia and hyperextensibility allows an infant to adopt unusual and awkward-appearing postures.

The term “floppy” is frequently used to describe hypotonic infants. This term is useful only as a shorthand description of clinical manifestations and is not a formal diagnosis.

Hypotonia must not be equated with hyporeflexia or muscle weakness. For example, patients with Down syndrome commonly have normal deep tendon reflexes and normal strength but are usually hypotonic. Conversely, patients with anterior horn cell disease are weak and manifest hypotonia and hyporeflexia.

Pathology

The central and peripheral nervous systems modify tone, but intrinsic physical characteristics of the tendons, joints, and muscles and the anatomic interrelationships of these structures also contribute significantly to tone. In childhood central nervous system (CNS) dysfunction, upper motor neuron (unit) disease may cause increased or decreased muscle tone [Teddy et al., 1984]. Disease involving the lower motor neuron (unit) results in hypotonia and weakness.

The final common pathway of upper or lower motor unit modification of tone is through the gamma loop (fusimotor) system [Gordon and Ghez, 1991; Granit, 1975]. Intimately involved with monitoring and effecting tone are the two stretch-sensitive muscle receptors – the muscle spindles and the Golgi tendon organs (Figure 5-1). It also has become evident that nonreflex, mechanical mechanisms are involved in the maintenance of resting muscle tone. Spinal cord reflex responses depend on ongoing activity in interneurons [Davidoff, 1992].

Fig. 5-1 Muscle spindles and Golgi tendon organs are encapsulated structures found in skeletal muscle.

The main skeletal muscle fibers, or extrafusal fibers, are innervated by large-diameter alpha motor axons. The muscle spindle has a fusiform shape and is arranged in parallel with extrafusal fibers. It is innervated by afferent and efferent fibers. The Golgi tendon organ is found at the junction between a group of extrafusal fibers and the tendon; it is therefore in series with extrafusal fibers. Each tendon organ is innervated by a single afferent axon.

(Adapted from Houck JC, Crago PE, Rymer WZ. Functional properties of the Golgi tendon organs. In: Desmedt JE, ed. Spinal and supraspinal mechanisms of voluntary motor control and locomotion. Progress in Clinical Neurophysiology, vol. 8. Basel: Karger, 1980:33.)

Stationed in all areas of the skeletal muscle is the muscle spindle, a fusiform-shaped receptor structure (Figure 5-2). The spindle is composed of contractile fibers at each end and a capsule covering a central fluid-filled dilatation. Sensory endings wrap around the central sections of the intrafusal fibers and monitor the stretch of these fibers; they communicate through the afferent axons that are described later in this chapter. Through efferent axons, gamma neurons within the anterior horn of the spinal cord innervate the contractile muscle portions on each end of the intrafusal fiber and enhance the sensitivity of the sensory endings to stretch [Gordon and Ghez, 1991]. Gamma motor neurons that innervate muscle spindles comprise the fusimotor system.

Fig. 5-2 The main components of the muscle spindle are intrafusal fibers, sensory endings, and motor axons.

A, The intrafusal fibers are specialized fibers; their central regions are not contractile. The sensory endings spiral around the central regions of the intrafusal fibers and are responsive to stretch of these fibers. Gamma motor neurons innervate the contractile polar regions of the intrafusal fibers. Contraction of the intrafusal fibers pulls on the central regions from both ends and increases the sensitivity of the sensory endings to stretch. B, The muscle spindle contains three types of intrafusal fibers: dynamic nuclear bag, static nuclear bag, and nuclear chain fibers. A single group Ia afferent fiber innervates all three types of intrafusal fiber, forming a primary ending. A group II afferent fiber innervates chain and static bag fibers, forming a secondary ending. Two types of efferent axons innervate different intrafusal fibers. Dynamic gamma motor axons innervate only dynamic bag fibers; static gamma motor axons innervate various combinations of chain and static bag fibers.

(A, Adapted from Hullinger M. The mammalian muscle spindle and its central control. Rev Physiol Biochem Pharmacol 1984;101:1; B, Adapted from Boyd IA. The isolated mammalian muscle spindle. Trends Neurosci 1980;3:258. Reproduced with permission from Elsevier.)

The intrafusal muscle fibers are divided into three types: nuclear chain fibers, dynamic nuclear bag fibers, and static nuclear bag fibers. These fibers derive their names from the configuration of their nuclei in the fiber center. Chain fibers have nuclei arranged in a single column, whereas bag fibers have nuclei aligned in rows of two or three. A solitary Ia afferent fiber provides primary sensory innervation for all three types of intrafusal fibers. A group II afferent fiber innervates chain and static bag fibers providing secondary sensory endings. The various sensory endings on the different types of intrafusal fibers have different sensitivities to rate of change of length. Dynamic gamma motor axons innervate the contractile portions of dynamic nuclear bag fibers, and static gamma motor axons innervate the contractile portions of the static bag fibers [Gordon and Ghez, 1991]. This intricate system of muscle spindle innervation allows the muscle stretch receptors to monitor muscle tension, length, and velocity of stretch, and provide input for maintenance of tone [Carew, 1985].

It is through their effect on the gamma motor neuron that portions of the CNS (i.e., motor cortex, thalamus, basal ganglia, vestibular nuclei, reticular formation, and cerebellum) modify tone, with ensuing hypotonia or hypertonia (i.e., spasticity) [Alexander and Delong, 1985; Brooks and Stoney, 1971; Carew, 1985; Ghez, 1985].

The Golgi tendon organs, unlike the muscle spindles, are found in series with the skeletal muscle fibers (Figure 5-3), and are attached at one end to the muscle and at the other to the tendon. A number of individual skeletal muscle fibers enter a Golgi tendon organ through a constricted collar. The muscle fibers are attached to collagen fibers within the Golgi tendon organ. A single Ib axon enters each capsule and forms branches that are interlaced among the collagen fibers. The afferent axon branches are compressed when muscle contraction occurs and impulses are transmitted. Tendon organs are much more sensitive to muscle contraction than muscle spindles. Conversely, tendon organs are much less sensitive to stretch than muscle spindles. Each of these relative sensitivities plays a specific role during the performance of various motor tasks [Gordon and Ghez, 1991].

Fig. 5-3 Golgi tendon organs are specialized structures found at the junctions between muscle and tendon.

Collagen fibers in the tendon organ attach to the muscle fibers. A single Ib afferent axon enters the capsule and branches into many unmyelinated endings that wrap around and between the collagen fibers. When the tendon organ is stretched (usually because of contraction of the muscle), the afferent axon is compressed by the collagen fibers (inset) and increases its rate of firing.

(Adapted from Schmidt RF. Motor systems. In: Schmidt RF, Thews G, eds. Human physiology [Biederman-Thorson MA, translator]. Berlin: Springer, 1983:81; inset, adapted from Swett JE, Schoultz TW. Mechanical transduction in the Golgi tendon organ: a hypothesis. Arch Ital Biol 1975;113:374.)

Evaluation of the Patient

History

The age at which hypotonia is first evident may be diagnostically crucial. The presence of hypotonia at birth or shortly thereafter can help differentiate among a number of conditions [Brooke et al., 1979; Dubowitz, 1985]. The presence or absence of weak fetal movements or the change from apparently normal fetal movements to those of decreased amplitude and vigor should be determined. Hypotonia in the setting of polyhydramnios signals prenatal interference with swallowing.

A careful genetic history must be sought because several conditions characterized by hypotonia are hereditary. In a retrospective review of hypotonic infants, Birdi et al. reported a family history of neuromuscular or neurologic disorders in almost half [Birdi et al., 2005].

Examination

Preterm infants, even when healthy, are normally hypotonic relative to a term newborn; therefore, corrected ages must be considered when assessing preterm infants during the first months of life. The finding of fixed contractures in the neonatal period suggests that hypotonia is associated with primary disorder of bone or muscle or an antenatal insult.

The infant’s tendency to assume unusual postures may indicate the presence of hypotonia – especially the “frogleg” position, in which the supine infant lies with the lower limbs externally rotated and abducted. Hypotonia is often associated with generalized weakness, with resultant poor suck, cry, and respiratory effort in addition to a paucity of spontaneous limb movements. Weakness should be suspected if the infant does not briskly withdraw a limb or cannot sustain the raised limb position in response to painful stimuli.

Tone should be assessed both in the active state and when the neonate is at rest; active tone of the extremities is normally higher than passive tone. Passive pronation, supination, flexion, and extension of the limbs and gently shaking the hands and feet are the best ways to assess tone. The hands move over a large amplitude when the arms are shaken gently at the wrists. Often, in the hypotonic infant, the elbows can be extended beyond their normal range. The scarf sign involves wrapping the infant’s arm across the chest toward the neck on the contralateral side and is positive when the elbow can be readily moved beyond the midline. While abnormal in the term infant, it can normally be seen in preterm infants. The traction maneuver is one of the best means to evaluate tone, since it allows simultaneous evaluation of head control, flexion of elbows during infant participation, and general body and back posture (see Figure 3-7). The hypotonic infant’s foot can be brought to the opposite ear, and extreme passive foot dorsiflexion may be possible when hypotonia is profound.

The hypotonic infant will slip through the hands of the examiner when held under the axillae (i.e., vertical suspension maneuver). If the hypotonic infant is supported by the trunk in an outstretched prone position (i.e., horizontal suspension maneuver), gravity causes flexion, or droop of the head and extremities (“inverted comma”). The normal response is anti-gravity with neck extension, straight back and limb flexion.

Weakness of facial muscles, weakness of muscles necessary for adequate suck and swallow, and paresis of the eyelid levators and extraocular muscles are often associated with genetic myopathies. The tongue should be carefully examined for atrophy and fasciculations. Evaluation of muscle weakness can be facilitated with the traction maneuver and by ascertaining the withdrawal response to appropriate stimuli and the ability to resist gravity. Paucity of movement signals the likely presence of concomitant weakness. If limb weakness is present, localization of the weakness to the proximal or distal extremities should be attempted. Older children may present with talipes planus, pronation at the ankles, and genu recurvatum.

The pectus excavatum deformity and a bell-shaped chest indicate relative weakness of intercostal muscles compared to better-preserved strength of the diaphragm during respiratory efforts. Skeletal deformities and fixed contractures are often present in congenital myotonic dystrophy and some congenital myopathies. Fixed contractures of the limbs may signal the presence of arthrogryposis multiplex congenita, which may result from dysfunction at a number of lower motor neuron unit sites [Lebenthal et al., 1970; Yuill and Lynch, 1974] (see Chapter 88).

Fasciculations of limb muscles are difficult to observe in infants because of abundant subcutaneous tissue. However, the experienced examiner can usually palpate the underlying muscle beneath the fat and estimate the adequacy of muscle bulk.

Deep tendon reflexes should always be elicited at all ages. The triceps reflex may be difficult to elicit in preterm and term newborns; reflexes are variably present at the biceps, easier to obtain at the pectoralis, and usually present at the patellar and Achilles tendons.

Acute onset of progressive, profound weakness and hypotonia in previously normal infants suggests the possibility of infantile botulism [Infant botulism, 2003; Kao et al., 1976; Pickett et al., 1976; Ravid et al., 2000; Thompson et al., 1980]. There is almost always accompanying constipation, poor feeding, and bulbar involvement.

In addition to most of the previously mentioned characteristics, hypotonia in the ambulatory child may manifest with a waddling gait, genu recurvatum, and talipes planus. There may be pronation of the feet at the ankles. The presence of scoliosis suggests associated weakness and neuromuscular disease.

Weakness is often readily diagnosed in the infant and younger child by observation; in the older child, more formal and discrete muscle testing is possible, as described in Chapter 2. Examination also includes deep tendon reflexes, plantar reflexes, myotonic response to percussion and scrutiny of muscles for evidence of fasciculations.

When the lower motor unit is involved, the deep tendon reflexes range from hypoactive to absent. The reflexes are uniformly absent in infantile spinal muscular atrophy [Bundey and Lovelace, 1975; Smith and Swaiman, 1983]. Reflexes tend to be increased or normal when the upper motor unit is involved, but may be decreased in the case of acute injury or concomitant involvement of the basal ganglia or their output tracts.

Further neurologic examination is necessary and should include the search for fasciculations, ptosis, squint, myotonia, and extensor plantar reflexes. The presence of squint or ptosis suggests the possibility of congenital myopathies [Clancy et al., 1980; McComb et al., 1979; Riggs et al., 2003], myotonic dystrophy, myasthenia gravis [Holmes et al., 1980; Namba et al., 1970], or mitochondrial myopathies (see Chapters 37 and 93). Knowledge about the congenital myopathies has grown considerably during the past decade, and the clinical and genetic complexities have become increasingly evident [Bruno and Minetti, 2004; Kirschner and Bonnemann, 2004].

Specific laboratory studies may be essential in establishing the diagnosis. When lower motor unit diseases are considered, serum enzyme determinations, nerve conduction velocities, electromyography, and nerve or muscle biopsies may be of importance. However, there is increasing reliance for specific diagnosis on genetic analysis, which has been replacing the need for biopsy in cases where the clinical phenotype and other laboratory evidence are convergent. When upper motor unit diseases are involved, a careful history, electroencephalography, evoked potentials, brain imaging, specific endocrine evaluations, and specific enzyme determinations may be required.

Diagnosis

For didactic purposes and simplification, the motor pathway from the motor neuron in the motor strip to the skeletal muscle fiber can be divided into upper and lower motor neuron units. The upper motor neuron (unit) includes the pyramidal neuron in the motor cortex and the myelinated nerve fiber, which traverses the corticospinal tract and eventually terminates in the internuncial pool in the spinal cord adjacent to the anterior horn cell. The lower motor neuron (unit) consists of the anterior horn cell, peripheral nerve, neuromuscular junction, and muscle. Disorders affecting muscular tone are divided into upper and lower motor unit disorders. Combined disorders also occur. It cannot be overstressed that upper motor unit disease may result in increased or diminished muscle tone in infants and young children.

It is important to distinguish whether hypotonia is derived from a central or peripheral etiology. While there can be difficulty in distinguishing the localization, one study examined sensitivity and specificity of findings predictive of primary neuromuscular disorders. These included a history of reduced fetal movements with polyhydramnios, significant impairment or absence of antigravity movements, and presence of contractures [Vasta et al., 2005]. Congenital hypotonia may be extremely difficult to categorize; however, certain characteristics may prove helpful in diagnosis (Table 5-1) [Harris, 2008].

Table 5-1 Differentiation of Central versus Peripheral Causes of Congenital Hypotonia

Characteristic	Central	Peripheral
Weakness	Mild to moderate	Significant (“paralytic”)
Deep tendon reflexes	Decreased or increased	Absent
Placing reaction	Sluggish	Absent
Motor delays	Yes	Yes
Antigravity movements in prone and supine	Some (less than normal)	Often absent
Pull to sit	Head lag (more than normal)	Marked head lag
Cognition/affect	Delayed	Typical
Ability to “build up” tone, e.g., tapping under knees with infant in supine to assist him/her in holding hips in adduction	Yes	No

(From Harris S. Congenital hypotonia. Dev Med Child Neurol 2008; 50:889.)

Functional impairment of the lower motor unit causes hypotonia and weakness. Hyporeflexia, fasciculations, and muscle atrophy also result. Certain conditions (e.g., Krabbe’s disease) cause combined upper and lower motor unit impairment and produce initial hypotonia.

Inadequate brain control of the motor pathways, or central hypotonia, is the most common cause of decreased tone. The presence of normoactive or brisk deep tendon reflexes suggests that the child is probably not suffering from lower motor unit impairment. The examiner should be alert for other signs of brain dysfunction, such as lethargy, unresponsiveness to the environment (i.e., visual and auditory stimuli), lack of development of social skills in the early months of life, and delayed development of language and reasoning skills in older children.

Diseases of the upper motor unit may be classified according to pathophysiologic cause (i.e., metabolic, degenerative, traumatic, congenital-structural, infectious, or toxic). A similar classification may be used for lower motor unit diseases; such diseases also may be categorized by the anatomic site of involvement.

A number of specific diseases can be suggested by historic and physical findings. Marked arching of the back and irritability suggest Krabbe’s disease. Profound hypotonia with obesity, small male genitalia, and poor feeding in the neonatal period suggests Prader–Willi syndrome.

Down syndrome is often evident on clinical grounds alone, although confirmatory chromosomal analysis is necessary. Visceromegaly, particularly hepatomegaly, is found with some diseases associated with hypotonia, including Niemann–Pick disease and cerebrohepatorenal syndrome. Blindness, seizure activity, and hyperacusis in the older infant or toddler suggest Tay–Sachs disease. Marked muscle underdevelopment and flexion contractures are characteristic of arthrogryposis multiplex congenita.

The presence of hypothyroidism is suggested by decreased length and weight, large tongue, and developmental delay. Some conditions associated with hypotonia are listed in Box 5-1 and are discussed in detail elsewhere in this book.

Box 5-1 Selected Conditions Associated with Hypotonia

Adrenoleukodystrophy (neonatal)

Cerebellothalamospinal degeneration

Fukuyama’s muscular dystrophy and encephalopathy

Infantile neuroaxonal dystrophy

Krabbe’s disease (globoid cell leukodystrophy)

Metachromatic leukodystrophy

Zellweger’s syndrome

Upper Motor Unit Disease (Central Nervous System Diseases)

Acute cerebral insult

Cerebrovascular accident (e.g., hemorrhage, thrombosis, embolism)

Hypoxic-ischemic encephalopathy

Infection (e.g., viral, bacterial, fungal, parasitic)

Chromosomal abnormality

Angelman’s syndrome

Down syndrome

Prader–Willi syndrome

Congenital motor disease (cerebral palsy)

Ataxia

Atonic diplegia or paraplegia (periventricular leukomalacia)

Incontinentia pigmenti

Lower Motor Unit (Peripheral Nervous System Diseases)

Arthrogryposis multiplex congenita

Carnitine deficiency

Connective tissue disease, such as Ehlers–Danlos syndrome

Anterior horn cell

Infantile spinal muscular atrophy

Kugelberg–Welander disease

Poliomyelitis

Peripheral nerve

Familial dysautonomia

Guillain–Barré syndrome

Hereditary motor-sensory neuropathies

Polyneuropathy

Neuromuscular junction

Botulism

Myasthenia gravis

Myasthenic syndrome

Neonatal myasthenia gravis (immune- and nonimmune-mediated forms)

Neonatal transient myasthenia gravis

Muscle

Congenital myopathies (e.g., central core disease, congenital fiber type disproportion, myotubular myopathy, nemaline myopathy)

Glycogen storage disease (e.g., acid maltase deficiency, phosphofructose kinase deficiency, phosphorylase deficiency)

Hypothyroidism

Myotonic dystrophy

Polymyositis

Clinical Laboratory Studies

Conventional laboratory studies, such as hemogram, erythrocyte sedimentation rate, urinalysis, and serum electrolyte determinations, are usually not helpful in assessing hypotonia, although creatine kinase and thyroid studies should be performed. Hypothyroidism can be diagnosed from routine thyroid studies. Creatine kinase and other serum muscle enzymes (i.e., enzymes that have escaped the muscle cells and are detectable in serum) are rarely positive in infants with hypotonia, but elevated levels are found in certain congenital muscular dystrophies and mitochondrial myopathies. Some conditions linked to hypotonia require special tests to yield a precise diagnosis. Pertinent portions of this text should be consulted to determine special laboratory testing requirements.

Magnetic resonance imaging (MRI) has replaced computed tomography (CT) as the standard modality for the diagnosis of structural CNS abnormalities. MRI is of particular value in the diagnosis of white matter diseases, including leukodystrophies. Muscle ultrasonography can be helpful to distinguish upper motor from lower motor abnormalities.

Cerebrospinal fluid studies may demonstrate pleocytosis, increased levels of protein, or abnormal proteins, and specific patterns may point to demyelinating conditions or peripheral neuropathy. Assessment for leukocyte enzyme activities associated with certain lipid storage diseases may provide definitive diagnoses for conditions that affect the brain alone, the brain and anterior horn cells, or the brain and peripheral nerves. Some of these conditions affect some non-neural organs.

Some neuromuscular and mitochondrial diseases are associated with cardiomyopathies, and electrocardiography or echocardiography may be of assistance in establishing a diagnosis. Electromyography differentiates neurogenic from myopathic conditions, and should inspire more intense considerations of some diagnostic categories. Studies in infants and young children require patience and experience for optimal studies and interpretation. The conventional assessment of insertion potentials and potentials at rest and during movement is as essential in infants as it is in older children and adults.

The diagnosis of peripheral neuropathy, particularly in conditions that involve the central and peripheral nervous systems, may be readily overlooked without the determination of nerve conduction velocities. Normative data are available for all age groups [Gamstorp, 1963].

The value of muscle biopsy is well established in the diagnosis of neuromuscular conditions and is discussed elsewhere in this book. It is essential that individuals specially trained and experienced in these endeavors are involved in all aspects of muscle biopsy from preparation of the specimens to specific light and ultramicroscopic studies.

Gait Impairment

Gait disturbances in children are often caused by neurologic disease, but it is overly simplistic to attribute all such abnormalities to neurologic dysfunction. Foot deformities are present in 4 percent of neonates, but the natural course of such congenital deformities is favorable, except for clubfoot which often requires surgical repair [Widhe, 1997]. Congenital abnormalities such as hamstring muscle or plantar foot flexor tightness may result in difficulties with posture and back pain [Jozwiak et al., 1997]. Clinical indices are available for the evaluation of gait pathology in children [Romei et al., 2004].

Gait is a demanding, complicated skill that requires integration of many functional components of the nervous system and is the result of a repetitive sequence of limb movements. The walking pendulum mechanism seen in older children and adults is not yet developed when the toddler first learns to walk independently, but by 2 years of age mechanical energy data are already similar to adult patterns [Ivanenko et al., 2004]. Significant changes in plantar pressure of the foot occur during the first year of standing and walking and the age of development of a mature pattern is highly variable [Bertsch et al., 2004]. Sophisticated evaluation of foot kinetics during walking is useful in providing information about gait impairment [MacWilliams et al., 2003]. Development of mature displacement of center of mass of the body during independent walking is a gradual neural process that evolves until the age of 7 years [Dierick et al., 2004]. Optimal gait requires the least expenditure of energy possible. Mechanical energy must be generated and then dissipated in a controlled fashion during each cycle [Gage et al., 1984; Õunpuu et al., 1991]. The encumbrance of additional weight can interfere with optimal walking posture; backpack load and walking distance do not affect stride, but a load of above 15 percent of body weight induces a significant increase in trunk inclination [Hong and Cheung, 2003]. During the gait cycle, posture and balance must be maintained, and the feet must clear the ground without scraping. Quantitative gait evaluation is increasingly precise and useful [Schwartz et al., 2004]. When children with pathologic gait characteristics are being compared with normal children, testing should involve patients and normal controls should be tested at the same walking speed [van der Linden et al., 2002].

Gait must be assessed when the patient’s chief complaint focuses on walking or running; however, assessment of gait affords the clinician rapid appraisal of a number of significant nervous system units when patient complaints are other than those relating to gait. Acquired idiopathic gait difficulties may occur with some frequency in children admitted to some children’s hospitals. Some acquired gait disorders have a definite physical cause, and some are idiopathic [Wassmer et al., 2002]. Further data documenting the incidence of these disorders is needed to evaluate their economic and social impact.

Physiologic Considerations

Skills required for standing must be synthesized into the walking procedure. The walking sequence requires that the non–weight-bearing leg moves forward while weight is shifted smoothly from leg to leg. The definitive components of support and forward movement require separate consideration; the rhythm and duration of each phase require monitoring [Gage and Õunpuu, 1989; Paine and Oppe, 1966]. Conventionally, the period from one heel–ground contact to the next heel–ground contact of one foot is one gait cycle; walking can be divided into stance and swing phases. The instant from which heel–ground contact occurs until the instant when contact terminates is the stance phase. The stance phase can be divided into four parts: initial contact, loading response, midstance, and terminal stance (Figure 5-4 and Figure 5-5). The period beginning immediately after the toe leaves the ground until the heel contacts the ground is the swing phase (see Figure 5-4 and Figure 5-5) [Burnett and Johnson, 1971a, 1971b; Norlin et al., 1981]. The swing phase can also be divided into four parts: preswing, initial swing, midswing, and terminal swing. Decreased knee flexion during the swing phase (i.e., stiff-knee gait) may be caused by overactivity of the rectus femoris [Piazza and Delp, 1996]. Normally, the stance phase occupies 60 percent of the duration of the cycle, and the swing phase occupies 40 percent.

Fig. 5-4 Schematic representation of various phases of a child walking.

(Adapted from Õunpuu S, Gage JR, Davis RB. Three-dimensional lower extremity joint kinetics in normal pediatric gait. J Pediatr Orthop 1991;11:341.)

Fig. 5-5 Graphic representation of the phases of gait and their duration.

(From Õunpuu S, Gage JR, Davis RB. Three-dimensional lower extremity joint kinetics in normal pediatric gait. J Pediatr Orthop 1991;11:341.)

Elaborate methods for the assessment of phases of gait have been devised [Burnett and Johnson, 1971a; Õunpuu et al., 1991]. The center of gravity is affected by several factors during ambulation: pelvic rotation, pelvic tilt, knee flexion at midstance, foot and knee mechanics, and lateral displacement of the pelvis [Saunders et al., 1953]. The center of gravity in older children shifts approximately 4.5 cm during the gait cycle. Pelvic rotation and pelvic tilt are usually necessary for development of independent gait [Burnett and Johnson, 1971a, 1971b]. Children usually acquire adult patterns of walking within 55 weeks of independent gait being achieved [Burnett and Johnson, 1971a, 1971b].

Because walking is such a complex skill, the normal participation of many motor system parts is vital; these include the basal ganglia; sensory cortex; neck proprioceptors; visual receptors; cerebellum; spinal cord motor and sensory tracts, and gray matter masses; peripheral nerves; neuromuscular junctions; and muscles [Norlin et al., 1981; Winter, 1990]. The participation of various muscles varies greatly during each portion of the gait cycle (Figure 5-6).

Fig. 5-6 Graphic representation of the involvement of various muscles during the phases of gait.

(From Õunpuu S, Gage JR, Davis RB. Three-dimensional lower extremity joint kinetics in normal pediatric gait. J Pediatr Orthop 1991;11:341.)

Indices have been devised to quantify deviations from normal gait and prove helpful in overall characterization of the patient’s degree of abnormal gait [Schutte et al., 2000; Schwartz and Rozumalski, 2008].

Evaluation of the Patient

Neurologic assessment should be directed at a number of target points. It is important to determine whether abnormalities are focal or diffuse. Alterations from normal include abnormal muscle tone, weakness, nystagmus, titubation (involuntary head bobbing), and dysmetria. Extrapyramidal movements associated with basal ganglia dysfunction, including dystonia, chorea, and athetosis, may be evident. Extensor toe signs, usually Babinski’s sign, may also be present. Deep tendon reflexes can be assessed, with particular reference to the patient’s response to the tendon stretch elicited by a reflex hammer and to response asymmetry.

To evaluate gait fully, it is important that the examiner be able to see the entire picture, so the patient should be unencumbered by clothing and is best tested wearing only underwear. The child’s back should be carefully examined with special attention to the lower spine. This area should be searched for lipomas, hair patches, hemangiomas, and dimples, all of which may accompany spine and cord deformities. Café au lait spots may signal the presence of neurofibromatosis.

Scoliosis of the spine should be evaluated systematically. The child should bend at the waist while placing both feet together flat on the floor. The child should bend toward the examiner while the spine is examined. If scoliosis is suspected, the length from the anterior spine of the ilium to the midpoint of each medial malleolus should be measured to ascertain leg length discrepancy. A relatively small degree of scoliosis can result in an abnormal gait.

The hip, knee, and ankle joints should be moved through their entire range of motion, and the presence of contractures determined. Any pain associated with joint movement should be evaluated. In infants, congenital dislocation or subluxation of the hip is often associated with skin fold asymmetry along the medial thigh. This abnormality is best seen posteriorly. Abnormal placement of the head of the femur may result in limited range of motion or, alternatively, spasticity may result in subluxation of the femoral head.

Before the patient’s walk is observed, the Romberg test should be performed. Walking should be assessed while the patient is barefoot and while wearing shoes. Patients who wear braces should be examined with and without braces. The child needs an explanation of the walking procedure, which entails walking down the hallway, turning abruptly, and returning.

The clinician should systematically evaluate the components of the child’s gait and associated movements. Among the important characteristics are symmetry of gait from leg to leg; whether walking occurs on the balls of the feet, flat-footed, or on the heels; and the relative stability of the pelvis.

Associated movements of the arms should be carefully observed. The fingers and hands may flex in association with infolding of the thumbs, indicating possible corticospinal tract dysfunction. The arms should move so that the contralateral arm swings forward synchronously with the swing phase of each leg (see Figure 5-4). When the child runs, abnormal arm and hand postures and movements are frequently accentuated. It is important in gait evaluation to measure leg length accurately. Discrepancies of less than 3 percent are not associated with compensatory movements [Song et al., 1997].

An older child should be asked to tandem-walk forward and backward (heel-to-toe); the examiner can facilitate compliance by demonstration. The child should be asked to pivot quickly when changing direction. The backward heel-to-toe walk should also be executed. The child should walk on the toes and reverse direction, remaining on the toes. This process needs to be repeated on the heels. A child who exhibits impaired heel walking may have an Achilles tendon contracture, equinovarus deformity, or foot dorsiflexor weakness.

The clinician should ask the child to circle the examiner, first in one direction and then in the other. If the child has hemispheric cerebellar disease, the child will tend to depart from the circular path toward the examiner or away from the examiner, depending on the side of the lesion.

It is advantageous to have the child climb steps to observe pelvic strength and stamina. Hip girdle strength can be assessed when the child is asked to squat and then stand rapidly. Evidence of hip girdle weakness may also be gained by asking the child to lie down in the supine position and sit up by flexing at the hip.

While the child walks and runs with shoes on, the examiner should listen and observe for evidence of scraping, scuffing, and slapping sounds. As described later, sensory ataxia and steppage gait are associated with “split” sounds.

More precise methods of gait analysis are available. Three-dimensional bilateral kinematic data can be obtained for analysis of the various facets of gait in children. The child is studied from several aspects: sagittal (i.e., the subject is viewed and monitored from the side), coronal (i.e., the subject is viewed and monitored from the front), and transverse (i.e., the subject is viewed and monitored from above). Data are generated from the changes in relationships as measured in angles (degrees) of various skeletal parts during the gait cycle [Gage, 1991; Myers et al., 2004; Õunpuu et al., 1991; Schwartz et al., 2004].

Electromyographic patterns of extrinsic ankle muscles in healthy children between 4 and 11 years old demonstrate the significant effect of walking speed changes but are independent of growth over this age range. This information can also be reduced to and retrieved from a nomograph [Detrembleur et al., 1997].

Differential Diagnosis

Spastic Hemiplegic Gait

Disruption of the corticospinal tract above the medulla results in contralateral abnormal tone, posture, and hemiplegic gait. The ipsilateral side is involved if the lesion occurs below the decussation of fibers in the medulla. Tone is often increased. Posture is characterized by leg extension or slight knee flexion. Hemiplegic gait includes impaired natural swing at the hip and knee with leg circumduction. The pelvis is often tilted upward on the involved side to permit adequate circumduction. With ambulation the leg moves forward and then swings back toward the midline in a circular movement. The heel-walking exercise is impaired as the patient scuffs the lateral sole and the toe of the shoe while dragging the foot. With more severe involvement, the movements are markedly slow and require great effort. Some children with modest spasticity of the knee may assume a position of mild flexion at the knee and hip, keep the foot held in the equinovarus position, and show reduced foot scuffing.

The affected leg bears weight for decidedly less time than the normal leg during ambulation. Involvement of the upper extremity leads to the arm being held in an awkward posture, usually close to the body, flexed at the elbow and wrist, and with a closed fist (i.e., cortical thumb). The expected rhythmic reciprocal swing of the arm with the stance phase of the opposite leg is absent. Dystonia rather than spasticity should be considered if the arm is held behind the plane of the body on a routine basis.

The etiology of hemiplegic gait cannot always be determined, but one should always look for focal brain lesions such as porencephalic cysts, subdural hematomas, cerebral masses, and cerebrovascular accidents.

Spastic Paraplegic Gait

Spastic paraplegia implies bilateral corticospinal tract dysfunction involving both legs out of proportion to upper extremity involvement. Patients with spastic paraplegia often have spasticity with flexion in the hips and knees, and weakness and limitation (or dorsiflexion) of both feet. The resultant posture resembles crouching. Occasionally, a child may manifest extreme spastic extension at the knees. The typical posture of the feet is equinovarus. Adduction of the thighs may cause the knees to brush one another during walking.

Infants may have a scissoring gait in which the legs cross; the highly increased adductor tone forces them into this position. Each step is deliberate, and the walking process painfully slow. Steps are short, and the toes are scuffed with each forward movement. Weight must be deliberately shifted from foot to foot, and the patient’s balance is unstable. This sequence is further complicated by the equinovarus position of the foot and the subsequent weight-bearing on the toes. Examination often reveals no cerebellar findings and no superficial or deep sensory impairment. The expected findings associated with corticospinal tract dysfunction include hyperactive deep tendon reflexes, ankle and knee clonus, extensor toe signs, and ankle contractures with resultant equinovarus positioning.

The most common cause of spastic paraplegia is prematurity with periventricular leukomalacia, but similar findings can result from hemispheric masses, porencephalic cysts, subdural hematomas, postmeningitic and postencephalitic states, and demyelinating diseases.

Toe walking may be the only indication of spastic paraplegia. However, isolated toe walking has a broad differential diagnosis, including spinal cord lesions (e.g., tethered cord syndrome), and can even be an early sign of autism. Sometimes, it is idiopathic, benign, or on a familial basis without relevance to future development. The clinician should establish the presence of other manifestations of upper motor neuron unit dysfunction before attributing pathologic significance to toe walking [Kelly et al., 1997; Volpe, 1997].

Cerebellar Gait

The cerebellum serves as a coordinating motor center; optimal functioning requires reception and synthesis of sensory information from the peripheral nerves, posterior columns of the spinal cord, and cortex. An unsteady, wide-based, often lurching gait signifies cerebellar pathway dysfunction. Cerebellar hemispheric lesions result in veering to the ipsilateral side. For example, if a child with a right cerebellar lesion is asked to circle the examiner in a clockwise direction, he will collide with the examiner within a few circles. The cerebellar gait is sometimes similar to the walking pattern of individuals under the influence of drugs or alcohol. Titubation and sometimes truncal bobbing movements may occur in any direction but happen most frequently in the anteroposterior direction. Nystagmus is an inconstant feature.

In order for cerebellar impairment to be better observed, the child should be asked to rise from a chair, walk a straight line, and suddenly reverse direction while walking in a tight circle. The child should be asked to tandem-walk along a straight line to facilitate observation of ataxia. The child should be asked to stand with the feet close together, first with eyes open and then with eyes closed. This is the Romberg test, and the child with cerebellar difficulties will maintain a stable or mildly unsteady stance with eyes open, but sway or fall toward the involved cerebellar hemisphere with eyes closed. The Romberg test is most commonly caused by posterior column dysfunction. Occasionally, the same finding can be replicated by severe peripheral neuropathy.

Compromise of the cerebellar hemisphere is associated with abnormal movement of the ipsilateral limbs. If the anterior lobe of the cerebellum or midline cerebellar structures are compromised, only gait may be involved, without abnormalities of the upper extremities. These abnormalities usually include action tremor with resultant difficulties with fine coordination.

Conditions affecting the cerebellum range from congenital malformations to infections, acute and chronic metabolic diseases, and progressive degenerative disorders. Among these conditions are congenital malformations, inherited cerebellar atrophies, aminoacidurias, mitochondrial diseases, lipid storage diseases, anoxic episodes, demyelinating diseases, posterior fossa tumors, hydrocephalus, and intoxication. Many hereditary cerebellar diseases have been described; these conditions often affect only a small number of pedigrees [Brown, 1980].

Acute Cerebellar Ataxia

The sudden, isolated appearance of ataxia without obvious cause requires systematic evaluation. Although the process is most often benign and self-limiting, the differential diagnosis is broad and includes some serious conditions [Hayakawa and Katoh, 1995; Sunaga et al., 1995]. In many cases, the cause is postinfectious, often following an influenza-like syndrome within the preceding few weeks. The patient is usually between 1 and 4 years old with a peak in the second year of life [Weiss and Carter, 1959]. The attacks may be so severe that the patient is bedridden, but more often present with unsteadiness and truncal ataxia. Nystagmus is present in one-half of these children [Cotton, 1957]. Other inconstant features are hypotonia, tremor, and scanning speech. Noncerebellar symptoms may include headaches, photophobia, and lightheadedness.

Lumbar puncture usually includes normal opening pressure, mild pleocytosis and normal glucose and protein, although a slight increase in protein content may be evident after several weeks. Acute cerebellar ataxia has been linked with numerous bacterial and viral infections, including diphtheria, pertussis, typhoid fever, rubella, mumps, varicella, coxsackievirus A9, echovirus 9, and poliomyelitis [King et al., 1958; Mendez-Cashion et al., 1962].

Full recovery, even with corticosteroid treatment, may require several months, but some children return to normal within 10 days, even without treatment. If no improvement in the ataxia occurs after several weeks, the clinician should be alert to the possible existence of a serious underlying cause. Approximately 30 percent of children retain a neurologic deficit, including ataxia and speech impairment [Weiss and Carter, 1959]. The differential diagnosis of ataxia is found in Chapter 67.

The diagnosis of a posterior fossa tumor should be excluded by neuroimaging with MRI. Papilledema is frequently associated with posterior fossa tumors that obstruct spinal fluid flow, but is often not present in intrinsic brainstem gliomas until much later in the disease course. The latter condition is usually associated with cranial nerve dysfunction, particularly the nerves that subserve eye and facial movements.

Ataxia associated with myoclonus may result from a neuroblastoma. The combination of myoclonus and neuroblastoma is known as the myoclonic encephalopathy syndrome, opsoclonus-myoclonus, or “dancing eyes, dancing feet.”

Acute trauma may induce cerebellar edema and subsequent hemorrhage with resultant ataxia. Hartnup’s disease and maple syrup urine disease may cause transient episodic ataxia. Children with absence seizures may appear to be ataxic and this may confound the diagnosis; their episodes of altered awareness, however brief, are a differentiating diagnostic feature.

The clinician must always keep in mind the possibility that ataxia was caused by unintentional poisoning in the young child or, especially in adolescents, the effects of illegal substances and diversion of drugs intended for medical use. Children who accidentally ingest a toxic or medicinal substance are usually too young to provide an accurate history of intake.

Sensory Ataxia

Ataxia results when the hemispheres and cerebellum are deprived of normal sensory input from various portions of the sensory system, including peripheral nerves, posterior roots, posterior columns, or connections leading from the posterior columns to the parietal lobes through the medial lemnisci. The patient experiences marked instability during standing and walking with a wide-based gait. Muscle power remains unaffected. The patient lacks position sense, and avoids obstacles by raising the legs inordinately and stepping sharply downward, the heel striking the ground first (“steppage gait”). A fraction of a second later the toe makes contact and produces the second part of a split sound. The child flexes the body slightly forward, and the gait is marked by variability of stride length. The child often compensates for loss of sensory awareness by looking at the ground during walking.

The child usually has no complaint of sensory abnormality unless ataxia is caused by a global peripheral neuropathy (i.e., one severely affecting all sensory modalities). However, examination will reveal abnormal position and vibratory sense primarily in the lower extremities. Romberg’s sign is positive. Causes for this gait in children include subacute combined degeneration, polyneuritis, demyelinating disease, and Friedreich’s ataxia.

Extrapyramidal Gait

Extrapyramidal gait disturbance is identified by decreased automatic movements, rigidity, and bradykinesia. The patient tilts the trunk and head forward. The arms are flexed at the elbows and wrists, and are held close to the body. The fingers are often extended, unlike the fisting in spastic quadriplegia. Shuffling gait is produced by the inability to lift the feet sufficiently. Steps are short and slow. The patient often leans forward, with a subsequent anterior shift of the center of gravity; this results in propulsion or festinating gait. The child may lose control and fall if the steps become more rapid and the center of gravity shifts unduly forward. This abnormal gait pattern may also be seen when the patient walks backward (retropulsion).

Characteristically, the affected child may have difficulty with the initial step and may take a few short steps or actually hop and shuffle forward before the walking sequence is established. In addition to the gait difficulties, children with extrapyramidal involvement have reduced blinking, are virtually devoid of facial expression (“mask facies”), and seldom fold their arms or cross their legs.

Patients with extrapyramidal gait usually have abnormalities of the structure and/or function of the basal ganglia, such as those seen in Parkinson’s disease, pantothenate kinase 2 deficiency (formerly known as Hallervorden–Spatz) disease, Wilson’s disease, postencephalitic syndromes, and drug toxicity.

Other Dyskinetic Gaits

A number of other movement disorders cause unusual gait patterns. Athetosis, when profound, may be associated with overall stiffness and bizarre body postures. With this condition, the feet may be positioned in plantar flexion, requiring the patient to bear weight on the toes. Inversion and dorsiflexion of the foot occur. After a stride is initiated, the flexed hip is externally rotated, the knee is flexed, and the foot remains in the plantar flexed position. The walk may have an associated dancelike or prancing appearance and may be incorrectly diagnosed as a form of conversion reaction.

This gait pattern is often associated with dystonia, particularly idiopathic torsion dystonia. The arms, hands, wrists, and fingers frequently move in deliberate, writhing movements about the long axis of the limb and then slowly reverse the rotational movement with irregular pace.

Other uncommon gait manifestations may accompany torsion dystonia. The foot may be held in plantar flexion or inversion. During the stationary phase, the leg may be rigid and a shoulder elevated. During the stride, the patient may have lordosis of the trunk, and the pelvis may be tilted forward with resultant partial hip flexion. Flexion of the knees may accompany the dystonia and may intensify as the patient develops dromedary gait. Because this manifestation may fluctuate in intensity, the clinician should be careful not to diagnose a conversion reaction. Children with this condition walk better backward than forward, including during the tandem-walk examination. This pattern of walking better backward than forward also may be found in patients who have quadriceps muscle weakness.

Chorea may also impair proximal hip muscle and trunk muscle action. The result is a rapidly shifting positioning of the trunk and body. The head may also move quickly along, with associated grimacing of the facial muscles, choreiform movements of the trunk and limbs, and irregular breathing patterns and sounds.

The gait of a child with conversion reaction may be outrageously intricate and may vary during the course of the examination. Slowness of gait is common in psychogenic gait disorders [Baik and Lang, 2007]. Short periods of normal walking activity may occur at times. Tremulousness of the fingers and hands during standing or walking may be associated findings. Patients with conversion reactions resembling hemiplegia or monoplegia usually drag the foot along the floor or push it ahead, in contradistinction to patients with corticospinal tract difficulty who elevate and circumduct the leg during each step. When both legs are involved, the patient may be bedridden or use crutches. On occasion, the child lurches out of control but does not fall, demonstrating remarkable coordination and strength (astasia-abasia). In patients with a positive Romberg sign, the swaying is often at the hips with a tendency to separate the legs despite instructions to stand with feet together. Patients with conversion reactions usually do not separate their feet. They may have associated rapid random movements of the head, hands, and hips. If the patient falls, there may be a dramatic aspect to the mishap. Despite dramatic unsteadiness, the patient may be able to run or walk backward without difficulty. One caveat: patients with dystonia musculorum deformans may walk backward smoothly, although they have problems with forward ambulation.

Pediatric patients with conversion reaction gait difficulties are almost never malingerers. Rather, they have physical manifestation of underlying psychological disorder and require supportive and empathetic intervention. Reassurance that they will get rapidly better with a very brief course of physical therapy can often allow them to return to a normal gait; this is more effective than confronting the patient and family with a diagnosis that appears to trivialize their pain and fear. Even if the gait abnormalities resolve completely, patients and parents must receive experienced and measured professional therapy and counseling.