Vertebral Column and Spinal Cord Injuries in Children

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CHAPTER 224 Vertebral Column and Spinal Cord Injuries in Children

Injuries to the spinal cord and vertebral column are relatively uncommon in the pediatric age range from birth to 17 years. The incidence is 1% to 10% of all spinal injuries.¹^–¹³ Data from major pediatric spinal trauma centers^11,¹⁴^–²⁰ indicate that injury to the juvenile spine differs from its adult counterpart with respect to anatomic and biomechanical features, mechanism of injury, response to deformation, injury pattern, and outcome. Several injury types are also unique to or prevalent in children, such as spinal cord injury without radiographic abnormality (SCIWORA), pure ligamentous injuries, atlanto-occipital dislocation (AOD), and atlantoaxial rotatory fixation (AARF). Finally, special problems are encountered in immobilizing the child’s inherently mobile yet fragile spinal column. This chapter deals with all these issues.

Classification of Injury Type

Pediatric spinal injuries are classified according to findings on plain x-ray films and computed tomography (CT). Although magnetic resonance imaging (MRI) reveals abnormalities in soft tissues, which can be helpful in assessing stability, it is less useful in the classification of injury types. Thus, based on skeletal information alone, four injury patterns are seen in children: (1) fracture of the vertebral body or posterior elements with subluxation; (2) fracture without subluxation; (3) subluxation without fracture, that is, pure ligamentous injury; and (4) spinal cord injury (SCI) without fracture or subluxation, or SCIWORA. A rough measure of the degree of instability of the injury is implicit in this classification. Similar to the adult counterpart, fracture-subluxations in the juvenile spine are unstable, whereas fractures without subluxation may or may not be unstable, depending on the amount of ligamentous disruption. Thus, a small compression fracture of the vertebral body is stable, but an undisplaced type II odontoid fracture and some spinous process fractures may not be stable. Pure ligamentous injuries (with displacement) are, by definition, unstable, even though in some cases the instability does not become manifest until months later as a progressive kyphotic deformity. SCIWORA is associated with a type of “radiographically occult” instability that is not demonstrable by conventional radiographs but poses a serious risk of recurrent injury to the spinal cord if no immobilization measures are taken (see later).

Biomechanical Considerations

In contrast to the adult spine, the juvenile vertebral column is inherently more malleable to deforming forces. This physiologic hypermobility allows considerable movement between vertebral segments without damage, but at the expense of providing less protection to the underlying spinal cord, which suffers deformation poorly. Several unique features of the juvenile spine account for this physiologic hypermobility. First, the ligaments and joint capsules are elastic and can withstand considerable stretching without tearing.²¹^–²⁵ This explains the phenomenon of pseudosubluxation in young children, or seemingly “excessive” angular displacement between C2 and C3 and, to a lesser extent, between C3 and C4.²¹^–²⁹ Second, because of their high water content, the intervertebral disk and annulus in children are also exceedingly expansile in the longitudinal axis, with the vertebral column of neonates being able to lengthen by as much as 2 inches without rupture when forcefully distracted.³⁰ Third, the facet joints are shallow and oriented more horizontally than in adults,^21,²⁴^–²⁶ which permits translational as well as flexion and extension movements. Fourth, the immature vertebral bodies are wedged anteriorly²¹^–²⁶ such that forward slippage between adjacent segments is enhanced. Fifth, the uncinate processes of the mature vertebral body, which normally restrict lateral and rotational movements, are absent in children younger than 10 years.^31,³² Sixth, the biologically active and hypervascular growth zone in the end plate represents another potential site of shifting; this structurally brittle zone splits readily from the primary centrum with even moderate shearing stress.³³ Finally, the proportionally large size of the infant’s head, coupled with the relatively delicate nuchal musculature, predisposes the infant’s neck to wide flip-flop swings when subjected to flexion and extension forces.³⁴

Dynamic radiographs show that the upper cervical segments in infants and young children are especially hypermobile in flexion and thus most susceptible to flexion injuries. The fulcrum for maximal flexion is at C2-3 in infants and young children. The horizontal orientation of the facets and the anterior wedging of the vertebral bodies are more prominent in the upper four segments of the cervical spine in this age group.^21,²³ The atlanto-occipital articulation in neonates also allows excessive sliding movements between the occipital condyle and the lateral mass of C1, partly because of the disparate matching between a large foramen magnum and a small C1 arch, the flimsy atlanto-occipital ligaments and condylar capsules,¹ and the convexity of the articulating surfaces.² Moreover, the protective groove on C1 for the vertebral artery, as it winds behind the C1 articular process to enter the cranium, is so shallow in neonates that during hyperextension the artery may be crushed between the condyle and the C1 arch, as was found on postmortem angiography in some victims of sudden infant death syndrome.³⁵

Many of these features of the juvenile spine transform into “adult states” around 8 or 9 years of age.^21,^22,^25,²⁶ In particular, the vertebral bodies become less wedged and more rectangular, the facet joints deepen and become more vertical, the uncinate processes enlarge, and the ligaments gain in tensile strength. With increasing age, the head also assumes a smaller proportion of the body and thus lessens its own lever effect. With this normal transition, pseudosubluxation is seen less often,^23,^36,³⁷ and the fulcrum for maximal flexion shifts from the upper cervical spine to C3-4 around 6 years of age and then to C5-6 in adolescence and early adulthood.^24,^38,³⁹

The age distribution of SCIWORA lesions ^11,^14,^18,^27,^34,⁴⁰ suggests that this biomechanical maturation takes place much more abruptly and successfully in the upper cervical segments such that the upper part of the neck, although vulnerable to flexion forces before the age of 8 years, becomes much more resistant to injury shortly afterward. The lower cervical spine, in contrast, seems to mature more gradually; lower cervical injuries occur with relatively equal frequency from birth to 16 years, even though serious lower cervical cord injuries tend to be more prevalent in younger age groups.

The preceding biomechanical data form the pathophysiologic basis of pediatric spinal cord and vertebral column injuries. Four basic premises can be deduced from these data:

1 A malleable vertebral column with elastic (stretchable) ligaments is less likely to sustain breakage of bones and frank rupture of ligaments when subjected to deforming forces.

2 A malleable vertebral column permits more intervertebral displacement in the presence of external stress and affords less protection to the underlying spinal cord, thus making it possible for the cord to be damaged without evidence of fracture or malalignment.

3 A more adult-like vertebral column with a sturdier osseoligamentous constitution provides better protection for the spinal cord.

4 The adult constitution is much less yielding to deforming forces and is therefore more likely to suffer breakage of bones and frank rupture of ligaments when subjected to high stress.

Based on these premises, the following clinicopathologic predictions can be made: (1) in the younger age group (birth to 8 years), there should be fewer fractures and subluxations and more SCIWORA; (2) SCI in young children should be more severe than in older children (9 to 16 years); (3) because the upper cervical spine is inherently more unstable in the younger age group, there should be more upper cervical injuries, and most of them should be associated with severe cord damage but minimal bony injury; (4) in the older age group there should be more fractures and subluxations than SCIWORA; (5) SCI in the older age group, from whatever mechanism, should be less severe than in the younger age group; and (6) the distribution of spinal injuries among older children should more closely resemble the adult pattern, with a preponderance of lower cervical injuries. Data from large clinical series of pediatric spinal injuries bear out these predictions.

Clinical Characteristics of Pediatric Spinal Injuries

Epidemiology

There is a seasonal peak for all categories of pediatric spinal injuries from June to September because of the increase in extracurricular activities during the summer break from school. The only other solitary peak in the otherwise smooth distribution curve is in the 2 weeks around the Christmas holiday.¹⁷

The cause of injury varies with age (Table 224-1). In the younger age group (0 to 9 years), the two predominant causes of injury are pedestrian-versus-vehicle accidents and falls, together accounting for more than 75% of the injuries.^14,^16,³⁷ In the intermediate age group (10 to 14 years), motor vehicle accidents, including motorcycle crashes, account for 40%, and falls and pedestrian accidents become less prevalent. This reflects the increasing role of older children as illegal drivers. In the late adolescent group (15 to 17 years), motor vehicle and motorcycle accidents become the leading cause of injury (>70%), and sports accidents also rise in number.^14,¹⁶^–¹⁸ ^,37 In keeping with these statistics, injuries in the 0- to 9-year-old group tend to occur at or near home, such as the basement steps, upstairs window ledges, and local playgrounds. Older children and adolescents are more likely to sustain injuries at a greater distance from home.¹⁷

TABLE 224-1 Cause of Spinal Injury Related to Age in 296 Children

The male-to-female ratio in pediatric spinal injuries varies with age, which may indirectly reflect gender differences in injury-prone activities in the different age brackets. The boy-girl ratio is smallest in the 0- to 9-year-old group (1.1 to 1.3 : 1)^14,^16,¹⁸ because pedestrian accidents affect both sexes equally and boys are slightly more susceptible to falls. The ratio increases marginally in the 10- to 14-year-old group but markedly in the 15- to 17-year-old group (2.3 to 2.5 : 1),^14,^16,¹⁸ when aggressive sports and reckless driving are signatures of adolescent masculine behavior.

Age and Injury Pattern

In most series of pediatric spinal trauma,^14,¹⁶^–¹⁸ ^,37 the patients are split evenly between those with SCI and those who are neurologically intact. Among the group with SCI (50% of the total), almost a third have complete cord injuries⁴¹ and two thirds have incomplete cord injuries of varying severity. In addition, about 30% to 40% of the patients with SCI have SCIWORA,^14,^16,¹⁸ although the reported incidence of SCIWORA in children with traumatic myelopathy varies widely from 5% to 67%,^{1–3,7,11,12,14,18,27,42–46} depending on the availability of diagnostic tests and the awareness of this syndrome in the local medical community.

The patient’s age profoundly affects the injury pattern. There is a significantly higher incidence of neurological injury in the 0- to 9-year-old group than in the 10- to 17-year-old group. Among SCI patients, younger children are also much more likely than older children to sustain complete (Frankel grade A) and severe (Frankel grades B and C) cord injuries.^14,¹⁶ These trends reflect the inadequacy of the immature vertebral column as a protector of the spinal cord. In addition, there are more SCIWORA and pure ligamentous injuries in the 0- to 9-year-old group than in the 15- to 17-year-old group and, conversely, more fracture-subluxations in the 10- to 17-year-old group (Table 224-2).^14,^16,^18,²² In several studies, the incidence of cervical spine fractures was 20% to 25% in the 0- to 8-year age range versus 70% to 80% in children older than 13 years.^6,^16,¹⁷ These statistics are also a reflection of the suppleness of the younger spine and its ability to yield without breakage against deforming forces, in contrast to the more “brittle” consistency of the adult-like spine in older children.

TABLE 224-2 Type of Spinal Injury Related to Age in 296 Children

Besides the age factor, the degree of neurological compromise also correlates with the presence of subluxation. Children with only fractures tend to have fewer neurological injuries (20% to 25%) than do those with fracture-subluxations or subluxations without fracture (>50%).¹⁴

Age and Injury Site

The majority of spinal cord and vertebral column injuries in children occur in the cervical region. Osenbach and Menezes reported that all pure ligamentous injuries, 76% of SCIWORA, and 70% of fracture-subluxations involve the cervical spine.¹⁸ Kewalramani and colleagues also found that 76% of pediatric SCIs occur in the cervical spinal cord and only 24% in the thoracic cord and conus.^7,⁸

The patient’s age is a strong determinant of the injury site, as predicted by the developmental changes in biomechanics (Table 224-3). Upper cervical and craniovertebral junction injuries are 2 to 3 times as frequent in children younger than 3 years^14,^18,⁴⁷ because of the extreme hypermobility at these joints in this age group. Lower cervical and thoracic injuries occur with equal frequency in both the 0- to 9-year-old group and the 10- to 17-year-old group because maturation at these joints occurs much more gradually than at the upper cervical articulations.^18,²⁷ Thoracolumbar and lumbar injuries are primarily lesions of adolescence.

TABLE 224-3 Level of Injury Related to Patient Age in 301 Children

LEVEL OF INJURY	AGE GROUP, NO. OF PATIENTS (%)
LEVEL OF INJURY	0-9 yr	10-16 yr
Upper cervical (to C3)	42 (53)	47 (21)
Lower cervical (C4-7)	20 (25)	76 (34)
Thoracic	8 (10)	26 (11)
Thoracolumbar	4 (5)	37 (18)
Lumbar	6 (7)	35 (16)
Total No. of patients	80	221

Data from Hadley MN, Zabramski JM, Browner CM, et al. Pediatric spinal trauma: review of 122 cases of spinal cord and vertebral column injuries. J Neurosurg. 1988;68:18-24; and Hamilton MG, Myles ST. Pediatric spinal injury: review of 174 hospital admissions. J Neurosurg. 1992;77:700-704.

Finally, multiple noncontiguous spinal injuries are found in 10% to 16% of patients,^14,¹⁶ thus emphasizing the need to survey the entire vertebral column carefully in every injured child.

Treatment

The same general principles that apply to adults also apply to children regarding the assignment of instability, fracture reduction, spinal immobilization, and surgical fusion. Early surgical intervention is seldom mandated after the fracture has been reduced and the spine immobilized. The only undisputed indication for emergency surgery is progressive neurological deterioration because of either an irreducible subluxation, in which case open reduction and fixation are necessary, or cord compression by a hematoma, extruded disk, or bone fragments, for which decompression and simultaneous fusion are recommended. These circumstances are quite rare in children. In the majority of cases, nonoperative management is the rule for at least the first few days, during which time the cord edema may resolve, serious extraneural injuries are dealt with, and the general prognosis is clarified. Thereafter, the indications for delayed surgery include irreducible fracture-subluxations, markedly unstable fractures, and pure ligamentous instability (see later).^14,^16,^29,⁴⁸^–⁵⁰ The specific treatment varies with the injury type. SCIWORA is, by definition, not associated with overt instability and requires only external immobilization.^27,⁵¹

Among upper cervical spine injuries, such as epiphysiolysis of the odontoid process, hangman’s fracture, C2-3 subluxation, AOD, and AARF, all but the last probably require internal fixation. Among lower cervical injuries, most fracture-subluxations and teardrop fractures are extremely unstable and require surgical fusion. Burst fractures with compromise of the spinal canal should be treated by anterior corpectomy and strut graft fusion reinforced with an anterior cervical plate. Most simple compression body fractures without significant loss of vertebral height, as well as uncomplicated spinous process fractures (“clay shuffler’s” fractures), are stable and can be treated with an external orthosis. On the whole, about 25% to 30% of all pediatric spinal injuries require surgical treatment. About 60% of fracture-subluxations are surgically fused, whereas only 10% to 15% of patients with fracture but no subluxation require fusion.^14,^16,¹⁸ Most pure ligamentous injuries should probably be treated by internal fixation because ligaments tend to heal poorly with just immobilization.¹⁸ The management details and fusion techniques for specific injury types are discussed later in separate sections.

Outcome

In one large review, the mortality rate in children with spinal injury was 28%.¹⁵ This is astounding when compared with an 11% mortality for adult spinal injury during the same study period. The majority of these pediatric deaths occurred at the accident scene and were invariably associated with unsalvageable multiorgan injuries. Only a small number of deaths were directly attributable to the SCI, all of which involved the upper cervical cord and had fatal cardiorespiratory complications. The study predicted that the mortality associated with pediatric spinal injury will not be influenced significantly by changes in treatment strategy and that injury prevention is still the most effective way to improve survival.^15,^16,^51,⁵²

Despite the high mortality, children who survive have a good prognosis for neurological improvement.^14,^16,^18,^50,^53,⁵⁴ The sole determinant of functional outcome is the initial neurological status. In the majority of patients with complete cord syndrome at admission, the injury remains complete; only 5% to 10% show some improvement, and virtually none make a full recovery.^5,¹⁶^–¹⁸ ^,27 Patients with severe cord injuries also tend to remain severely impaired. However, significant improvement is expected in those with mild to moderate cord injuries; 75% to 85% of these patients improve by one to two Frankel grades, and more than half of these patients enjoy a full recovery.^5,¹⁶ The good outcome in pediatric SCI may be related to the enhanced plasticity of the young nervous system.

Pecial Injury Types

SCIWORA

The acronym SCIWORA was first coined and described as a distinct syndrome by Pang and Wilberger ³⁴ in 1982. Children with SCIWORA suffer a traumatic myelopathy without identifiable fracture or subluxation on plain spine films, tomography, and CT. Increasing recognition of this entity over the past decade has led to the accrual of a large pool of clinical data.^7,^14,^16,^18,^27,⁴⁷

Biomechanics and Mechanisms of Spinal Cord Injury

The pathogenetic concept of SCIWORA is based on the premise that the inherently elastic juvenile spine can accommodate considerable intersegmental displacement without fracture or ligamentous rupture, but at the expense of the underlying spinal cord. Four mechanisms may be involved in the pathogenesis: hyperextension, flexion, distraction, and spinal cord ischemia.

Hyperextension of the cervical spine forces the interlaminar ligaments to bulge forward into the spinal canal and may be responsible for up to 50% narrowing of the canal’s diameter.^55,⁵⁶ In addition, the cord thickens as it shortens during hyperextension.⁵⁷ Thus, the space available for the cervical cord within the canal is reduced during moderate hyperextension. During violent hyperextension, Taylor and Blackwood⁵⁶ and Bourmer⁵⁸ demonstrated rupture of the anterior longitudinal ligament, shearing of the intervertebral disk from the end plates, and retrodisplacement of the upper vertebrae. Dynamic radiography on fresh cadavers showed that elastic recoil of the displaced segment could result in perfect spontaneous reduction and give a normal radiographic appearance.⁵⁹ With its elastic constituents, the juvenile spine is especially susceptible to this sequence of momentary dislocation and spontaneous reduction. Intersegmental movement in children is further facilitated by their horizontal facet joints,^21,²³^–²⁶ ^,32 and the immature vertebral body splits readily from its end plate within the brittle growth zone and leaves no radiographic trace.³³ The elastic elements,^21,^32,⁶⁰ horizontal facets,^21,²⁴^–²⁶ wedge-shaped bodies,^21,²³ and absence of uncinate processes likewise predispose the juvenile spine to hyperflexion myelopathy.^31,³²

The spines of infants and young children are also uniquely vulnerable to distraction.^42,⁶¹ Leventhal found that although the elastic spinal column of neonatal cadavers could be stretched up to 2 inches without structural damage, the inelastic spinal cord ruptures if stretched more than 0.25 inch.⁶² The clinical counterpart of Leventhal’s study is the finding of frank rupture of the cord and meninges within a completely intact vertebral column in infants who had undergone forceful breech extraction.^24,⁶³ In nonobstetric SCIWORA, the best evidence of distraction injury is found in patients when the thoracic spine is forcefully distracted in lap belt injuries. Rupture of the dura and spinal cord in these patients is evidenced by the resultant cerebrospinal fluid–pleural fistula.⁶⁴ Finally, the precarious architecture of the neonatal atlanto-occipital articulations predisposes the upper cervical cord to ischemic necrosis from occlusion of the vertebral artery.

The Age Factor

As predicted by biomechanics, age influences SCIWORA in three ways. First, many studies have shown that the incidence of SCIWORA is higher than that of other injury types in young children (0 to 9 years) with traumatic myelopathy, and vice versa in older children (Fig. 224-1).^14,^44,^46,⁶⁵ Second, young patients with SCIWORA typically have more severe neurological injuries than do their older counterparts (Fig. 224-2).^5,⁴⁶ In our own series, 21 of 30 children younger than 8 years suffered complete or severe injuries as compared with only 1 of 25 children older than 8 years (P < .000001).²⁷ Similarly, Osenbach and Menezes noted severe injuries (Frankel grades B and C) in 21 of 22 patients younger than 9 years versus comparable injury severity in only 1 of 9 older children.¹⁸ Third, several studies have shown that young children are far more susceptible to upper cervical SCIWORA whereas lower cervical lesions occur more often in older children. In our series, 9 of 10 upper cervical injuries occurred in children younger than 8 years versus 21 of 33 lower cervical injuries in older children (Fig. 224-3).²⁷ In the series of Osenbach and Menezes, all 7 nonobstetric upper cervical injuries occurred in children younger than 9 years.¹⁸ Unlike cervical lesions, SCIWORA involving the thoracic cord is evenly distributed over the pediatric age range, with no age predilection.^18,^27,⁴⁶ Thus, because young children tend to have upper cord injuries and most of them are complete or nearly complete, the rehabilitation potential of this age group is very limited and the socioeconomic burden is accordingly prohibitive.

FIGURE 224-1 Incidence of spinal cord injury without radiographic abnormality versus overt spinal column injury in children with traumatic myelopathy as a function of age. “Young” children are those younger than 9 or 10 years.

(Data from references^14–18,34^,40 ^,44 ^,75 ^,83).

FIGURE 224-2 Severity of neurological injury in children with spinal cord injury without radiographic abnormality as a function of age. “Young” children are those younger than 9 years.

(Data from references^3,¹⁴^–¹⁶ ^,18 ^,44 ^,46 ^,75).

FIGURE 224-3 Correlation between patient age and level of neurological injury in spinal cord injury without radiographic abnormality. The vertical dashed line denotes the age (8 years) at which the physiologic properties of the juvenile spine change. The upper cervical spine was most prone to injury in infants and young children, whereas the lower cervical spine was at risk in all ages up to 16 years.

Radiographically Occult Instability

It is important to distinguish between the radiographically occult instability in SCIWORA and the overt instability seen in fracture-subluxation and subluxation without fracture (pure ligamentous injury). In SCIWORA, the spinal cord is injured without radiographic evidence of a fracture or subluxation that would indicate extensive ligamentous tearing and gross instability. Yet there had to have been sufficient bone displacement at impact to inflict damage to the cord. This implies that the stabilizing ligaments and fibrocartilaginous structures, although sufficiently elastic to stretch and recoil without rupturing, may have been severely sprained or even partially torn to render the involved vertebral segments vulnerable to repeated stress. The resulting instability or biomechanically precarious state is therefore “occult” rather than overt.^20,^21,²⁴^–²⁷ ^,33 The fact that flexion-extension radiographs fail to disclose abnormal movements in SCIWORA does not argue against the existence of occult instability because even gross instability can be masked by muscle spasm.³⁷ Moreover, motion studies executed with deliberate caution cannot compare with the random and unguarded neck movements in real-life activities. It is therefore not surprising that post-SCIWORA dynamic films do not reveal the precarious state of the injured segments.²⁷

Until the advent of MRI, the existence of occult instability in SCIWORA was unproved although strongly suggested by two phenomena: delayed neurological deterioration and recurrent SCIWORA. In a number of children with SCIWORA, neurological deficits are not detectable immediately after trauma but develop and worsen after a latent period of 30 minutes to 4 days, apparently in the absence of further trauma.^27,^40,^43,⁶⁶^–⁶⁸ The mechanism of this delayed deterioration remains speculative. A few cases may be due to posttraumatic occlusion of radicular arteries as a result of thrombosis or spasm, with subsequent delayed infarction of the cord,^43,⁶⁶ but this must be rare. The majority of cases probably result from repeated “punch-drunk” trauma to the cord during the latent period. This presumption is supported by two observations. First, many of these children recall transient neurological symptoms at the time of the initial trauma, such as subjective weakness, acroparesthesia, or Lhermitte’s phenomenon, thus indicating that the cord had been distracted or hit during the intersegmental displacement. This displacement may well have overstretched or partially torn crucial ligaments and rendered the segments susceptible to repeated shifts during otherwise innocuous neck movements. Second, the incidence of delayed deterioration at our institution has decreased dramatically (13 of 24 cases treated before 1982³⁴ versus 2 of 33 since 1982²⁷) because of the rigorous implementation of prompt neck immobilization and neurosurgical referral for any child with neck pain and transient neurological symptoms. Many of these children have been found to have subtle neurological deficits that could easily have been missed on cursory examination, or they show evidence of myelopathy on somatosensory evoked potential (SSEP) testing. Such patients would presumably have been at risk for reinjury if they had not been immobilized expeditiously.

The phenomenon of delayed neurological deterioration in SCIWORA suggests that the spinal column has been weakened temporarily by the impact, even if the initial neurological symptoms are mild. This concept of a postimpact period of vulnerability is supported by the phenomenon of recurrent SCIWORA, noted up to 10 weeks after initial SCIWORA in 8 of 42 children treated before 1986.⁶⁹ Before this time, it had been our practice to immobilize children in hard collars for 2 months after SCIWORA. Four of the children with recurrent SCIWORA had removed their hard collars and were reinjured while engaging in forbidden sports such as wrestling, gymnastics, or basketball. The others were reinjured while wearing their collars. The neurological deficits resulting from the recurrent SCIWORA were much worse than those of the initial trauma, which in all cases were mild.⁶⁹ It is noteworthy that none of these children had overt instability on dynamic radiographs either at the first SCIWORA or at the time of reinjury. These normal studies belie the precarious state of the “once touched” spinal cord when the unprotected neck is subjected to the erratic motions of a child at play.

Findings on Magnetic Resonance Imaging

The discovery of MRI abnormalities in the soft tissues of the spine represents the first direct evidence of occult ligament damage in SCIWORA.⁷⁰ These abnormalities are extraneural, involving mainly ligaments and intervertebral disks, and neural, involving the cord itself.

Extraneural Abnormalities

The extraneural soft tissue injury demonstrated on MRI is well correlated with the mechanism of injury.⁷⁰ For example, rupture of the anterior longitudinal ligament, seen as loss of continuity of the low-signal prevertebral line, widening of the anterior intervertebral space, and anterior disk herniation (Fig. 224-4), is found in cases of hyperextension. Rupture of the posterior longitudinal ligament, seen as loss of continuity of the retrovertebral line and small posterior disk herniation (Fig. 224-5), is correlated with hyperflexion. Intradiscal hemorrhages are seen when a translational interbody shearing mechanism is suspected. Hemorrhage of the tectorial membrane (tear) has been associated with the violent shaking of child abuse (Fig. 224-6), and hemorrhages in the interspinous and interlaminar ligaments are seen with distraction injury (Fig. 224-7). Furthermore, the level of these soft tissue injuries corresponds exactly to the level of the neurological lesion.¹⁹

FIGURE 224-4 Thirteen-year-old girl who had mild partial C7 myelopathy after a hyperextension injury. Left, Plain film revealing slight separation of the disk space at C6-7. Right, Sagittal magnetic resonance image (TR, 2200; TE, 30) obtained 3 days after injury showing discontinuity of the prevertebral line of signal void, a finding suggestive of a tear in the anterior longitudinal ligament, anterior C6-7 disk herniation (large arrowhead), and possible end-plate separation (small arrowhead).

FIGURE 224-5 A 9-year-old boy sustained a lateral flexion injury and had complete Brown-Séquard syndrome at initial evaluation. A sagittal long TR (TR, 4000; TE, 18) magnetic resonance image shows interruption of the retrovertebral line of the signal void, consistent with a disrupted posterior longitudinal ligament and C2-3 disk herniation (arrow).

FIGURE 224-6 Sagittal magnetic resonance image in an infant with a tear of the tectorial membrane resulting from whiplash-shake syndrome. It is seen as a subacute hemorrhage (hyperintense on short TR) within the soft tissue behind the odontoid process.

FIGURE 224-7 T2-weighted magnetic resonance image in a 6-year-old child with hyperflexion and mild cord syndrome. Widespread edema (arrows) is evident in the interspinous ligaments and muscles of the upper five cervical levels.

These extraneural MRI findings strongly support the hypothesis that SCIWORA is associated with spraining or partial tearing of crucial stabilizing structures of the vertebral column.^19,²⁷ For years, these ligamentous and disk injuries, which are responsible for the post-SCIWORA vulnerable period, had escaped detection by conventional radiology but are now “exposed” by MRI. The continued use of MRI is expected to reveal more information about SCIWORA.

The signal characteristics of hemorrhage within non-neural tissues are detectable within hours of the injury on T1-weighted images as lines of hyperintensity because extravasated blood is converted within hours to methemoglobin (MHb) in non-neural tissues versus days to weeks in neural tissues (see later).^4,^30,^71,⁷² Extraneural injuries in SCIWORA can thus be diagnosed by MRI within hours after the injury. The problem is that the adjacent fascial, muscular, and fat planes also produce high signal and can overwhelm the small streaks of MHb. The use of fat suppression sequences reduces the high signal of fat but not that of blood on short relaxation time (TR) (T1-weighted) images and is effective in highlighting the soft tissue hemorrhages in SCIWORA.

Neural Abnormalities

The MRI abnormalities seen within the traumatized spinal cord correspond to the signal characteristics of the various metabolized forms of extravasated hemoglobin (Table 224-4). Fresh blood from spinal cord hemorrhage contains intracellular oxyhemoglobin, which is rapidly converted to deoxyhemoglobin (DHb) within 3 hours. DHb is a stable intracellular compound and appears hypointense on long TR (T2-weighted) images.^4,^10,^30,^71,⁷³ Gradient echo techniques, which are particularly sensitive to paramagnetic substances such as DHb, detect acute hemorrhage even better than do standard long TR sequences.^12,^30,^71,^73,⁷⁴ Oxidation of intracellular DHb to MHb begins after approximately 3 days, although DHb may still be detectable up to 8 days after injury, especially with larger hematomas. Intracellular MHb is hyperintense on short TR images but hypointense on long TR images, whereas extracellular MHb appears hyperintense on both short and long TR images. Subsequent hemolysis around day 7 liberates MHb into extracellular tissues, where it may persist for months. Extracellular MHb is finally converted to hemosiderin after phagocytosis; this substance, which may persist for life, is markedly hypointense on long TR images and slightly hypointense on short TR images.⁷³ The larger the hemorrhage, the longer it takes for all the DHb to be converted to MHb and ultimately for MHb to become hemosiderin. The signal characteristics are thus dependent not only on the time elapsed since injury but also on hematoma size.

TABLE 224-4 Magnetic Resonance Imaging Signal Alterations in Spinal Cord Injury As a Function of the Chemical State of Blood

Five patterns of parenchymal (cord) findings are seen on the post-SCIWORA MRI scan.⁷⁰ (1) Complete disruption of the spinal cord is seen with severe distraction injuries in very young children (Fig. 224-8). This is usually accompanied by hypointensities on gradient echo sequences (DHb) of the rostral cord stump. The common sites of cord disruption are the upper cervical and upper thoracic levels. Severe flexion injury occasionally produces a similar picture. (2) Major cord hemorrhage has occurred when more than 50% of the cross-sectional area of the cord on axial MRI shows evidence of extravasated hemoglobin (Fig. 224-9). Depending on the timing of MRI, the signal characteristics may be those of DHb, intracellular or extracellular MHb, or hemosiderin. This pattern is associated with severe neural deficits and a dismal prognosis. (3) Minor cord hemorrhage has occurred when less than 50% of the cross-sectional area of the cord shows evidence of hemorrhage. It is associated with moderately severe initial deficits but a decent chance for recovery. (4) Edema only, without hemorrhage, is noted if the T1-weighted image shows isointensity or slight hypointensity but the T2-weighted image is intensely bright. No stage of hemoglobin metabolism produces this pattern of signal characteristics. Edema is predictive of a good outcome. (5) Approximately 35% of patients with clinically proven SCIWORA do not have MRI abnormalities in their spinal cords. These patients have an excellent prognosis for complete recovery.⁷⁵

FIGURE 224-8 Two-month-old with a complete C6 injury subsequent to a motor vehicle accident. A sagittal short TR (TR, 800; TE, 30) magnetic resonance image obtained 6 days after injury shows loss of cord continuity consistent with cord transection.

FIGURE 224-9 Twenty-one-month-old boy with a complete C3 injury after suffering physical abuse. A, Computed tomographic myelography performed 15 days after injury shows marked enlargement of the cord; the cause (hemorrhage or edema) could not be discerned. B, Axial short TR (TR, 600; TE, 20) magnetic resonance imaging (MRI) performed 16 days after injury shows intraparenchymal hyperintensity expanding and replacing the cord substance, consistent with methemoglobin. C, Sagittal short TR (TR, 600; TE, 20) MRI at day 16 shows the methemoglobin-suffused segment of the cord extending from C2 to T1. D, Sagittal short TR (TR, 600; TE, 20) MRI performed 3 months after injury shows marked cervical cord atrophy.

It is our policy to repeat the MRI study on days 6 to 9 after the injury, regardless of whether the acute MRI (on days 0 to 3) showed abnormal findings. Edema takes 3 to 4 hours to develop, and small dots of DHb may not be easily detectable until it is converted to MHb, at which point contrast between the spinal cord and hemoglobin is greater. If the initial MRI findings are abnormal, a later study at 3 to 6 months is performed to detect syrinx formation and marked atrophy of the cord.

Thoracolumbar SCIWORA

About 13% of cases of SCIWORA involve the thoracic cord. SCIWORA of the thoracic spine is typically due to violent trauma, such as high-speed automobile accidents or crushing injuries.* Accordingly, these patients have a high incidence of associated thoracic, abdominal, and pelvic injuries. Three discrete subgroups of patients with thoracic SCIWORA are encountered. One consists of children who sustain severe distraction injuries related to lap seat belts and high-speed vehicular collisions.⁶⁴ CT myelography typically shows spinal cord and dural rupture and free flow of contrast material into the mediastinum.^25,^42,^76,⁷⁷ The splinting effect of the rib cage normally protects the thoracic spine against horizontal displacement as a result of flexion and extension forces. However, because the sternocostal joints permit a fair amount of “bucket handle” movements, the rib cage provides little protection against longitudinal distraction. In lap belt injuries, there is always a component of forceful distraction caused by forward propulsion of the upper part of the chest while the pelvis is harnessed by the lap belt. The elastic juvenile spinal column then recoils like a spring to restore normal configuration after having stretched enough to rupture the cord and dura. As with upper cervical SCIWORA, thoracic SCIWORA secondary to distraction occurs almost exclusively in children younger than 8 years.

A second subgroup of thoracic SCIWORA includes children who are crushed by slow-moving vehicles.^3,²⁷ In these cases, tire marks are clearly imprinted on the body, so the body position and exact site of crushing can be determined. All thoracic SCIWORA victims injured by crushing were lying prone when run over by the cars that left tire marks on their backs. In contrast, children with tire marks on the abdomen or anterior chest region typically suffer intraperitoneal injuries but rarely SCI. In the group with ventral tire marks, the gentle S curve of the thoracic spinal column, being solidly buttressed by the ground, merely straightens out and is thus protected against excessive intersegmental displacement; the abdominal viscera bear the brunt of the injury. In the group with dorsal tire marks, the spinal column is hyperextended into the softness of the chest and abdominal cavities, thereby resulting in hyperextension cord injury and rupture of retroperitoneal organs while sparing the well-protected intraperitoneal contents.

The last subgroup of thoracic SCIWORA involves a direct hit on a standing child by a high-speed vehicle. These children all had severe or complete cord lesions, and all sustained severe or even fatal extraneural injuries. The presumed mechanism is an egregious self-reducing deformity of the thoracic spine caused by an extreme force that has overcome the protective splinting of the rib cage, which explains the high fatality. Ironically, because attention is often focused on the other life-threatening injuries during initial resuscitation, the paraplegia is not infrequently missed until the child’s condition stabilizes and survival ensured, thereby affording a perversely fertile field for litigation.

Management

The initial management of a child with a presumed SCI begins in the field (Fig. 224-10). Patients with symptoms or mechanism of injury compatible with SCI should be immobilized supine in a hard collar on a fracture board. If the child’s head is large, the body from the shoulders down is propped up with folded blankets or foam sheets to prevent forced flexion of the neck.

FIGURE 224-10 Management algorithm for the evaluation and treatment of children with spinal cord injuries. The main focus is on recommendations for patients with possible spinal cord injury without radiographic abnormality (SCIWORA). ER, emergency room; CT, computed tomography; MRI, magnetic resonance imaging.

When possible, a careful history is obtained from the patient or eyewitnesses to determine the cause and mechanism of injury. In addition, interpretation of the associated non-neural injuries frequently gives clues to the mechanism of the spinal injury. All patients undergo complete cervical spine radiography, and a full spine survey is performed on patients with presumed thoracic cord lesions or severe multisystem trauma. Patients with SCI but without abnormalities on plain films undergo thin-section axial CT with bone algorithms to rule out an occult fracture at the level of the neurological lesion, followed by MRI. The radiographic evaluation is not complete until good-quality flexion and extension films of the affected area of the spine are obtained to rule out overt ligamentous instability. In many patients, severe spasm of the paraspinal muscles precludes adequate flexion for several days; the dynamic study must be repeated a few days later.

In children with severe cord injuries diagnosed within 8 hours of the injury, a 24-hour course of high-dose corticosteroids is initiated. This recommendation is based on the beneficial effects of high-dose methylprednisolone in adult patients reported by the National Acute Spinal Cord Injury Study (NASCIS III).⁸⁰^–⁸² There are no equivalent data for children, and our endorsement of corticosteroids for SCIWORA must be understood to be “empirical” rather than evidence-based. Patients with cervical cord injuries are immobilized in a Guilford brace (B.A. Guilford and Sons Orthotic Laboratory Ltd., Cleveland, OH) or other cervical-thoracic brace for 3 months. Mid to low thoracic lesions are treated with a thoracolumbar orthosis (TLSO), and children with upper thoracic lesions are fitted with a TLSO with added chin and occiput supports. Physical and occupational therapies are begun in the intensive care unit (ICU). Those with severe residual deficits are transported to a rehabilitation facility when clinically stable. Patients with mild residual weakness are enrolled in an outpatient physical therapy program. Bracing is maintained for 3 months, during which time both contact and noncontact sports are strictly prohibited. The brace is favored over a hard collar for several reasons: (1) it can be tailored to fit children as young as 1 year; (2) it imparts greater limitation of motion; (3) it produces less skin irritation and chafing than a collar; and most importantly, (4) a child cannot easily remove the brace, which also interferes with play activity, both helping to enforce compliance. It may be helpful to embellish with graphic details the estates of paralysis, wheelchair existence, decubitus ulcers, impotence, and so on to older children and their families as a warning of the dire consequences of protocol violation.

Our decision to immobilize for 3 months is based anecdotally on the fact that one patient treated with just 2 months of wearing a hard collar suffered recurrent SCI with trivial trauma 10 weeks after the initial SCIWORA. Since changing from our old protocol of using just a hard collar for 2 months,³⁴ no recurrent SCIWORA has been reported.⁶⁴ The improved outcome may just as well be due to switching of the collar to bracing as to switching from 2 months to 3 months. Currently, there are institutions that favor the 2-month protocol, and unless adverse results are reported with the shorter immobilization, the choice of 2 versus 3 months must be left to the individual belief of the treating physician. After 3 months, flexion-extension radiographs are obtained with the child out of the brace to check for late instability. In our experience, this is rarely a problem with SCIWORA, nor is late deformity such as kyphosis or scoliosis.^19,^20,⁸³

SCIWORA in the Comatose Child

The question is often asked how to “clear the neck” of a comatose child. A normal spine film and CT scan rule out most cases of gross fracture and dislocation, but not SCIWORA. In some ICUs, a comatose child is kept on a hard collar and flat log-rolling regimen as long as the child is unresponsive or being maintained on mechanical ventilation, but this could last weeks and skin breakdown around the chin and occiput can become troublesome long before a valid neurological examination is feasible. In this setting we suggest performing MRI and using SSEPs to detect spinal cord conduction block.⁷⁵ If both MRI and SSEPs are normal, the spinal precautions are removed. If either the SSEPs or MRI is abnormal, strict spine precautions are observed until the patient is able to mobilize, at which time a proper brace is fitted.

Outcome

Several studies,^5,¹⁸ including our own from 1989,²⁷ have shown that the main predictor of long-term outcome in children with SCIWORA is the admission neurological status. Children with complete lesions rarely improve. Those with severe but incomplete lesions often improve with time but seldom regain normal function. Only patients with mild to moderate initial deficits can hope for a full recovery (Fig. 224-11). Thus, the overall outcome for SCIWORA can best be improved by preventing serious neurological damage. Primary prevention programs within the community such as ThinkFirst have lowered the overall incidence of SCI in children. Once SCIWORA has occurred, the pediatric neurosurgeon’s responsibility would be to minimize the extent of neuronal damage through three avenues: (1) rule out other (non-SCIWORA) categories of SCI, (2) anticipate and prevent delayed neurological deterioration, and (3) prevent recurrent injury. This means that occult fractures, disk herniation, epidural hematoma, and overt ligament instability must be excluded with dynamic radiographs, CT, and MRI before the diagnosis of SCIWORA can be established because each of these entities mandates more than simple bracing. The results reported by Pang and Pollack²⁷ and Pollack and colleagues⁶⁹ suggest that the incidence of delayed neurological deterioration and recurrent SCIWORA can be lowered by compulsive prehospital care and a low threshold for the use of spinal immobilization in any injured child meeting our diagnostic criteria for SCIWORA.

FIGURE 224-11 Long-term neurological outcome in children with spinal cord injury without radiographic abnormality as a function of initial neurological status.

Prognostic Value of Magnetic Resonance Imaging in SCIWORA

Although preventive measures are still paramount in improving outcome, recent MRI data ⁷⁵ suggest that our earlier outcome predictions made without MRI²⁷ have become somewhat obsolete. In our recent series,⁷⁵ we correlated the five neural MRI abnormalities (really four abnormalities plus “normal”) with the four grades of neurological deficit (complete, severe, mild, and normal) at initial evaluation and 6 months later in a much larger population (Fig. 224-12). We found instead that although the general conclusions from the original outcome analysis²⁷ stand, in specific cases MRI surpasses the initial neurological examination in predicting outcome. The implication of cord disruption, once clearly portrayed on MRI, is self-evident. In all patients with this finding, who invariably have complete sensorimotor paralysis, the deficits remain complete. Major hemorrhage is also associated with complete or severe deficits (Frankel grades B and C) at initial evaluation, as well as with very poor long-term outcome.^71,⁸⁴ Patients with this finding either remain profoundly impaired or achieve only minimal recovery. No one in our series ever ascended from severe to the mild or moderate category (Frankel grade D) of cord syndromes, although two patients initially found to be complete were raised to the severe grade. In short, cord disruption and major hemorrhage are no better predicators of outcome than the admission neurological examination.

FIGURE 224-12 Correlation of findings on magnetic resonance imaging (MRI) with neurologic syndromes at initial evaluation and at 6 months’ follow-up in 50 patients in the authors’ updated series. The numbers in each box correspond to numbers of patients in a syndrome category. The fate of cord disruption or pulping is obvious. All patients with major hemorrhage have complete syndromes, but only a few improved to the severe grade. All minor hemorrhage was associated with either complete or severe grades, but a significant number improved to a mild grade at 6 months. An even larger percentage of patients with edema only improved to the mild grade. Most patients with normal cord findings have mild injuries and improve to normal status at 6 months. The 2 patients who had complete syndrome but became normal within 2 days (cord concussion) had normal findings on MRI.

The situation is different with the other categories of neural MRI findings. All patients with minor hemorrhage have severe initial deficits (Frankel grades B and C) at initial evaluation, but only 60% remained in this grade at 6 months and 40% ultimately recovered to the mild grade (Frankel grade D). Furthermore, about 44% of the patients with edema only on MRI initially had moderate to severe deficits (Frankel grade B and C), yet none of them remained in the severe grades; overall, 75% improved to the mild grade and 25% became normal. Thus, in patients with minor hemorrhage and edema only, the MRI finding is a better predictor of outcome than the initial neurological examination. By and large, edema only and minor hemorrhage, in that order, are associated with a much better prognosis than major hemorrhage, even though the initial deficits may be equally severe in the three groups. Among the four types of neural abnormalities on post-SCIWORA MRI, edema-only remains the best indicator for good recovery.

All patients with no cord abnormality on post-SCIWORA MRI, except two, had mild initial deficits, and all made a complete recovery. The two exceptions initially had complete sensorimotor paralysis but within 2 days had also made a complete recovery.⁷⁰ This phenomenon of “cord concussion” had been described by Quencer, who thought that the “chemical alterations” within the cord that led to the initial paralysis did not generate abnormal MRI signals.⁸⁵ Thus, normal MRI findings always presage an excellent prognosis regardless of the initial neurological grading.

Pure Ligamentous Injuries (Subluxation without Fracture)

Unlike the case with SCIWORA, the diagnostic criteria and management guidelines for overt instability in children are not well defined. Certainly, if the radiograph shows extensive bone fractures or subluxation, the implication of gross instability is obvious. However, the biomechanics of many subtler kinds of ligamentous instability in children has not been studied as intensely as it has been in adults, and recommendations for children are often extrapolated from adult data. For example, cadaver studies by Fielding and coworkers regarding stability of the atlantoaxial joint showed that (1) the atlantodental interval (ADI) in normal adults seldom exceeds 3 mm, (2) an ADI of 3 to 5 mm implies rupture of the transverse ligament, (3) an ADI of 5 to 10 mm suggests additional incompetence of the alar ligaments, and (4) an ADI greater than 10 mm exists only if all other accessory odontoid ligaments are also ruptured.^86,⁸⁷ Thus, an ADI greater than 3 mm in adults is considered unstable.⁸⁸ Equivalent scientific data are unavailable in children. From purely empirical observations and taking into account the elasticity of the juvenile ligaments, an ADI of 4 mm has been regarded as the upper limit of normal in children younger than 8 years.^86,⁸⁹ Other studies have also shown that 20% to 30% of children with trisomy 21 and an ADI greater than 6 mm deteriorate with time, thus suggesting that 6 mm should be used as the threshold for treatment in children with Down syndrome.⁹⁰^–⁹³

Similar biomechanical studies of the subaxial spine by White and Panjabi and their associates showed that the angle between adjacent vertebrae in normal adults is always less than 11 degrees and that deformities greater than 11 degrees in adults are considered unstable.^88,⁹⁴^–⁹⁸ For children, however, the upper limit of normal should be less than 11 degrees. The reason is as follows: because the juvenile spine is so elastic and apt to recoil, the final resting position of the displaced segment may lie well short of its actual maximal excursion at the time of impact. The initial angle of displacement on the lateral radiograph is thus deceptively small, but the actual ligamentous disruption may have been profound. This scenario is illustrated by the case of a 10-year-old boy who suffered a flexion injury and was found to have an asymmetric central cord syndrome with a radiograph showing a kyphotic deformity of 8 degrees and horizontal displacement of 2 mm at C4-5. No dynamic radiographs were obtained for fear of aggravating the neurological deficits, but because the angulation did not satisfy the 11-degreee adult rule, he was initially treated with a halo vest and not surgical fusion. When the halo was removed 3 months later, his kyphosis progressed rapidly and he ultimately required a posterior fusion (Fig. 224-13).

FIGURE 224-13 Flexion injury in a 10-year-old boy with an asymmetric central cord syndrome. A, Lateral radiograph showing a kyphotic deformity of 8 degrees at C4 and C5, horizontal displacement of less than 2 mm, slight widening of the C4-5 interspinous space, and compression fractures of the C5 and C6 vertebral bodies. He was treated with a halo for 3 months. B, Immediately after removal of the halo, a lateral radiograph showed angulation of 13 degrees. C, One week after removal of the halo, the angulation increased to 33 degrees. Horizontal displacement increased to 3.5 mm.

This case illustrates the dilemma when the neutral radiograph does not meet the 11-degree instability rule yet the neural deficits suggest ligamentous damage but also preclude a flexion study. In retrospect, this boy’s instability was obviously present despite the 8-degree angulation on the initial film. Such examples are common in pediatric neck injury. To avoid underdiagnosis, we recommend the following algorithm for children with angular deformities in the subaxial cervical spine (Fig. 224-14):

1 If the neutral radiograph shows more than 11 degrees of angulation, with or without neurological deficits, overt instability is assumed. No flexion-extension study is obtained, and surgical fusion is performed.

2 If the neutral radiograph shows an angulation greater than 7 degrees but less than 11 degrees and a neurological deficit is present, the injury is considered unstable based on the assumption that the actual displacement must have been greater to cause myelopathy. No dynamic study is performed.

3 If the neutral radiograph shows an angulation greater than 7 degrees but less than 11 degrees and the child is neurologically normal, flexion-extension studies are obtained. If the angulation increases to 11 degrees or greater, surgical fusion is performed. If the angulation is unchanged, the dynamic study is repeated in 3 to 5 days to eliminate the effect of spasm. If the angle is again less than 11 degrees, the child is fitted with a cervicothoracic brace for 2 months, after which dynamic radiographs are obtained to confirm solid ligamentous healing.

4 If the initial angulation is less than 7 degrees but the patient has severe pain and spasm, a collar is worn until dynamic studies can be repeated in a few days to rule out instability.

FIGURE 224-14 Management algorithm for ligamentous instability in children if the lateral radiograph shows a kyphotic deformity.

Another case illustrates the importance of flexion studies (Fig. 224-15). A 12-year-old girl suffered a flexion injury and had a painful stiff neck, a normal neurological examination, and a neutral film that showed an angulation of 9 degrees at C4 and C5. A flexion study showed that the angle increased to 12 degrees. Nonetheless, the child was immobilized in a Philadelphia collar for only 14 days, at which time a repeat radiograph showed that the kyphosis had increased to 17 degrees. Under the present guidelines, this patient would have undergone surgical fusion after the flexion study.

FIGURE 224-15 Flexion injury in a 12-year-old girl with a painful stiff neck and normal neurological status. A, Lateral radiograph showing angulation of 9 degrees between C4 and C5. B, Flexion study showing an increase in angulation to 12 degrees. The child was immobilized in a Philadelphia collar. C, Fourteen days after injury, the angulation between C4 and C5 increased to 17 degrees, a finding indicative of overt instability.

Besides the 11-degree rule, the studies of White and Panjabi showed that horizontal interbody displacement of greater than 3.5 mm in adults implies significant ligamentous rupture that will result in delayed instability.^88,⁹⁶^–⁹⁸ The juvenile spine, however, exhibits much greater physiologic horizontal movement than the adult spine, and displacement greater than 3.5 mm may be considered normal. Sullivan and coworkers noted forward glide of 3.5 to 4 mm between C2 and C3 in 13 of 100 normal children.²³ Cattell and Filtzer observed similar findings in 19% of normal children younger than 8 years.²⁶ In all probability, this “pseudosubluxation” between C2 and C3 and, to a lesser extent, between C3 and C4 is due to the elastic supporting soft tissues. The following recommendations are helpful in distinguishing clinical instability from physiologic hypermobility in the subaxial segments of children:

1 Children older than 8 years are similar to adults, and horizontal displacement greater than 3.5 mm at any level should be considered unstable.

2 Children younger than 8 years have increased physiologic mobility at the C2-3 and C3-4 joints, but horizontal displacement at these levels greater than 4.5 mm should be considered unstable.

3 In children younger than 8 years, if horizontal displacement of 3.5 mm at the upper levels is accompanied by muscle spasm, pain, neurological findings, or additional abnormalities, such as an avulsed spinous process or widened interspinous space, clinical instability is assumed.

4 Even in children younger than 8 years, the physiologic mobility below C4 is not significantly different from that in adults; therefore, horizontal displacement greater than 3.5 mm suggests instability.

Atlanto-occipital Dislocation

Traumatic AOD is one of the most common fatal cervical spine injuries. Autopsy and postmortem radiographic examination of traffic fatalities revealed a 20% to 35% incidence of AOD.⁹⁹^–¹⁰¹ Improvements in emergency resuscitation and prehospital care have increased survival in patients with this previously almost invariably fatal injury. AOD is a particularly important entity in pediatric spine trauma, not only because it occurs more than twice as frequently in children as in adults¹⁰² but also because children who survive the initial crisis often make good recoveries despite the severe initial neurological deficits.^103,¹⁰⁴

Anatomy and Biomechanics

The occipitoatlantoaxial (O-C1-C2) articulations function as a single unit that procures movements of the head about the spine. The atlas works as a biconcave washer between two spheres of motion. The upper articulation, between the occipital condyles and the atlas, is cup shaped in the sagittal plane and medially tilted in the coronal plane. This orientation allows flexion, extension, and some lateral bending, but minimal rotation. In contrast, the biconvex and laterally tilted facet articulation between the atlas and axis allows a large degree of rotation centered about the dens. Sagittal movement of the anterior arch of the atlas along the slightly pointed dens provides additional flexion and extension.

Movements within the O-C1-C2 unit are facilitated by the redundant articular capsules and thin occipitoatlantal and atlantoaxial membranes, which in turn impart minimal stability.⁹⁸ Rather, stability is provided by the strong internal ligaments between C2 and the occiput, chiefly the tectorial membrane, a well-developed continuation of the posterior longitudinal ligament that straps the body of C2 to the clivus; by the paired alar ligaments that connect the dens to the occipital condyles; by the cruciate ligament; and by the apical dental ligament (Fig. 224-16). Flexion of the basion beyond the tip of the dens is limited by the tectorial membrane, whereas extension is checked by the tectorial membrane and by bony contact between the opisthion and the arch of C1. Lateral bending and rotation are controlled by the alar ligaments.¹⁰⁵ The importance of the tectorial membrane and the alar ligaments was demonstrated by Werne, who found that sectioning of the former results in excessive flexion and extension, as well as vertical separation of the basion from the dens beyond the normal range of 1 cm, whereas sectioning of the latter results in increased lateral bending and rotation.¹⁰⁶ When both the alar ligaments and tectorial membrane are cut, complete occipitoaxial dissociation occurs. The remainder of the internal ligaments—namely, the ascending band of the cruciate ligament and the apical ligament—are ineffectual in limiting motion. Finally, cadaver studies have shown that paraspinal muscle action also contributes to stability of the O-C1-C2 unit.^107,¹⁰⁸

FIGURE 224-16 The joints and ligaments of the craniovertebral junction. Top, Posterior view. Bottom, Lateral view. Lig, ligament.

(From Wolf JW, Johnson RM. Cervical orthoses. In: Bailey DW, Sherk HH, eds. The Cervical Spine. Philadelphia: JB Lippincott; 1983:54-61.)

Pathology and Pathogenesis

Traumatic AOD results from high-energy impacts that cause rupture of the tectorial membrane and alar ligaments.^65,^99,^101,^102,¹⁰⁹^–¹¹¹ Pedestrian-vehicle accidents are the most common cause. Three factors make children more vulnerable to AOD than adults. First, children are more frequently involved in pedestrian-vehicle accidents.¹¹² Second, the relatively larger head in children in comparison to the torso generates a greater shearing moment. Third, the occipitoatlantal joint is inherently more unstable in children.¹¹³

The force vectors involved in AOD may be reconstructed by circumstantial evidence. Adams’ study revealed a high incidence of associated submental lacerations and mandibular fractures,⁹⁹ and others have reported posterior atlas fractures,¹¹⁴ both of which point to a hyperextension mechanism. Furthermore, 9 of Adams’ 12 subjects had pontomedullary lacerations,⁹⁹ a lesion that is characteristic of hyperextension and rotation.¹¹⁵^–¹¹⁷ However, approximately 25% of patients with AOD have coexistent anterior atlantoaxial subluxation, and other patients are seen with spinomedullary transection by a posteriorly pointing dens.^99,¹¹⁰ These findings suggest a hyperflexion mechanism.¹¹⁸ Because the alar ligaments—the check ligaments for rotation—are also ruptured in AOD, the forces must be directed obliquely to the head.^105,¹¹⁹^–¹²¹ Thus, AOD is most often caused by hyperextension-distraction forces directed obliquely to the chin, but hyperflexion-distraction forces to the occiput are involved in some cases.

Recently, Sun and colleagues ¹²² used high-resolution MRI to reveal a progressive pattern of disruption of the structures responsible for the stability of the O-C2 joint. Progressing from minor to severe injuries, the sequence of successive and additive involvement of structures is as follows: suboccipital musculature, atlanto-occipital and atlantoaxial membranes, apical and alar ligaments, tectorial membrane, and bilateral atlanto-occipital joint capsules. These authors postulated that involvement of the tectorial membrane is a critical threshold for instability at the O-C2 joint. Tectorial membrane damage can consist of frank rupture (Fig. 224-17) or stripping of the membrane from the clival or C2 attachments (Fig. 224-18). In both cases, the mechanical advantage of the membrane’s stabilizing function is rendered ineffective. Weakening of this membrane appears to “expose” the O-C1 joint capsules to overt disruption, the denouement of the AOD scenario, with the cord being left vulnerable to traction and crushing injuries. In our recent series of AOD in which 14 children underwent MRI,¹²³ seven tectorial membranes had ruptured, three had been stripped off the clivus, and only four had remained intact.

FIGURE 224-17 Sagittal T2-weighted magnetic resonance image in a 7-year-old child with atlanto-occipital dislocation. The tectorial membrane is completely disrupted. The upper stump (arrow) is still attached to the clivus. The alar ligaments are not visualized above the tip of the dens, thus suggesting that they have also ruptured.

FIGURE 224-18 Sagittal T2-weighted magnetic resonance image in a 9-year-old child with atlanto-occipital dislocation. The tectorial membrane (arrow) is lifted off the clivus. The clival-dens space contains blood or edema fluid.

Traynelis and coworkers classified AOD into three types.¹¹⁸ Type I, the most common, is characterized by anterior displacement of the occiput on the atlas. Type II is a longitudinal separation of the two structures, and type III is posterior displacement of the occiput. The prevalence of anterior AOD seems contradictory to the postulated hyperextension vector, but given the highly unstable nature of this injury, the location of the head relative to C1 may be more a function of postimpact positioning than the dynamics of the impact. As an example, when an injured child lies on a flat board, the occipital prominence of the large head forces the neck into flexion, thereby artificially creating an anterior displacement pattern. Rigid classification of AOD according to the relative position of the head therefore carries no correlative value with regard to mechanism and should be discouraged. Isolated examples of pure lateral dislocation,¹²⁴ as well as pure rotatory subluxation, further attest to the extreme looseness of the disrupted O-C1 joint.^125,¹²⁶

Clinical Findings

Children with traumatic AOD have signs of brainstem, spinal cord, and cranial nerve injury. Thirty percent of children who survive AOD are apneic or in full cardiorespiratory arrest at the scene of the accident.^47,¹²⁷^–¹³³ Other brainstem findings include pupillary abnormalities, rotatory nystagmus, ocular bobbing, decerebrate posturing, and variable alterations in consciousness.¹²³ The motor deficits include quadriparesis, cruciate paralysis, crossed hemiplegia, or hemiparesis, depending on the level of the pyramidal tract lesions. Brainstem injury in AOD is due to a combination of actual disruption of tissues, spinal medullary compression by bony structures or epidural hematoma, and ischemia secondary to vertebral artery spasm or thrombosis.¹³⁴ Thrombosis of the anterior spinal artery produces the unique syndrome of ipsilateral hypoglossal palsy and crossed hemiplegia.¹³⁵ The caudal six pairs of cranial nerves may also be injured from downward traction of the medulla against the fixed points at their exit foramina.¹³⁶ However, the most common cranial neuropathy in AOD, sixth nerve palsy, is probably caused by the concomitant head injury. Posttraumatic hydrocephalus must be ruled out if the abducens palsy persists.

The true mortality rate associated with AOD is unknown. Of 35 nonfatal cases of pediatric AOD reported in the literature,^104,^111,^122,^{129–133,136–145} only 5 had no initial deficits except for neck pain and torticollis. Of the 30 patients with deficits, 12 recovered fully; 3 remained quadriplegic and ventilator dependent, 2 of whom died 8 months after injury. The remaining 15 patients experienced various intermediate recoveries. Thus, children with AOD who have incomplete initial paralysis often make significant improvements, but in isolated cases, even initially flaccid paralysis does not preclude a good recovery.

Radiographic Diagnosis

The diagnosis of AOD is contingent on a high level of suspicion in trauma victims, especially those with mandibular and facial fractures or with instantaneous cardiorespiratory instability. Casting of the brainstem with subarachnoid blood, seen on 25% of head CT scans in patients with AOD, should immediately suggest a distraction injury at the atlanto-occipital junction. The radiographic “chase” for the diagnosis should be relentless because survival depends on recognition. Although gross separation of the occiput and atlas is obvious on plain x-ray films, horizontal luxations are much harder to diagnose. The literature is replete with imperfect diagnostic criteria. A critical review of these criteria allows the clinician to use multiple methods to augment the positive yield.

One of the oldest criteria is the interval between the tip of the dens and the basion (DB interval) (Fig. 224-19). Wholey and associates examined 480 adult and 120 pediatric cervical spine radiographs and determined that the upper limit of the DB interval is 5 mm in adults and 10 mm in children, the age difference being attributed to incomplete summit ossification of the dens in children.¹⁴⁶ Earlier application of the DB interval revealed considerable overlap between normal subjects and patients with AOD, possibly because of the mixed age groups.¹¹⁰ The most recent use of the DB interval exclusively in children showed that the value in normal children is less than 12.5 mm; the values in 11 children with proven AOD were all greater than 14 mm.¹³⁸ However, several problems are inherent in this method. First, as with any absolute radiographic measurement, the number depends on the target-film distance. Wholey’s original measurements were done on an upright film at a target-film distance of 6 ft. When the DB intervals in 400 subjects were measured on supine films taken at 40 inches, Harris and colleagues found the upper limit to be 12 mm in adults.¹⁴⁷ Second, the variable ossification of the odontoid summit in children makes universal application of a maximal DB interval unreliable. Third, the measurement varies with flexion, extension, and axial traction in normal subjects. Nevertheless, a DB interval greater than 14 mm in a child is almost certainly indicative of AOD, but values between 10 and 14 mm still defy precise designation.