The pediatric cervical spine: Developmental anatomy and clinical aspects

The~oumalofEmergency

Med/one. Vol. 7,pp. 133-142, 1989

PrInted In the USA ??Copyright @I1989 Pergamon Press plc

THE PEDIATRIC CERVICAL SPINE: Developmental Anatomy and Clinical Aspects Francis M. Fesmire,

MD,*

and Robert C. Luten,

MD, FACEP,

Fhip*st

“Division of Emergency Medicine and tpediatric Emergency Services, University Hospital of Jacksonville/ University of Florida College of Medicine, 655 West 8th Street, Jacksonville, Florida Reprirft address: Francis M. Fesmire, MD, Emergency Medical Associates, P.O. Box 72538, Chattanooga, TN 37407

0 Abstract-The radiographic interpretation of the pediatric cervical spine can be a perplexing problem for the emergency physician. Given the wide range of variances in the ossification centers, the unfused synchondroses, and the relative hypermobility of the pediatric cervical spine, radiographs may be easily misread if one is not thoroughly familiar with the developmental anatomy and variants. This paper discusses those developmental aspects of the pediatric cervical spine that impact on emergency radiographic interpretation. Frequently encountered pediatric cervical spine fracture/dislocations are reviewed with an analysis of agerelated distributions. Finally, the syndrome of Spinal Cord Injury Without Radiographic Abnormality (SCIWORA) is discussed.

ANATOMIC DEVELOPMENT CERVICAL SPINE

The pediatric C-spine can best be understood by reviewing the anatomic development with increasing age (see Figure la-ld). The A tlas The first cervical vertebra (atlas) is formed from three primary ossification centers -the body and two neural arches (see Figure 2). The body of Cl is not ossified at birth, but becomes visible as one or two ossification centers during the first year of life. Rarely the ossification center fails to appear and the two neural arches extend forward. Failure of the neural arches to fuse in this instance results in a central cleft (l-6). The neural arches of Cl appear in utero at approximately the seventh fetal week. The synchondrosis of the posteriorly located spinous processes fuses around the third year of life. The synchondrosis about the body fuses approximately the seventh year. Prior to fusion, these synchondroses may be confused with fracture lines (l-5).

?? Keywords- pediatric cervical spine; cervical spine developmental anatomy; cervical spine fracture/ dislocations; spinal cord injuries, SCIWORA

INTRODUCTION

The emergency physician is frequently perplexed when interpreting radiographs of the pediatric cervical spine (C-spine). Given the unfused synchondroses, the incomplete ossifications, and the relative hypermobility of the C-spine of children, interpretation can be difficult. Even more perplexing is the fact that a significant percentage of pediatric cervical spinal cord injuries occur in the absence of C-spine fractures and dislocations. This paper discusses the developmental variations in the pediatric C-spine and reviews literature dealing with the incidence of pediatric C-spine fractures and spinal cord injuries.

v

OF THE

The Axis The second cervical vertebra (the axis) is the most confusing to the nonradiologist because there are four primary ossification centers -odontoid, body, and two neural arches (see Figure 3) (l-4). The odontoid forms in utero from two separate ossification centers that fuse in the midline by the

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Francis M. Fesmire and Robert C. Luten

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(4

Figure 1. The development of the pediatric cervical spine. (a) Six month old: The body of Cl has not yet appeared. The synchondrosis between the odontoid and the body of C2 is unfused. Note the widened soft tissue space anterior to the cervical spine which frequently is seen in the pediatric age group when the neck is held in mild fiexlon or with expiration. (b) Two year old: The body of Cl is now visible. Note the anterior wedging of C3 to C6 cervical vertebrae. (c) Four year old: The dens is fused to the body of Cl. The vertebral bodies are beginning to take on the rectangular shape of the adult vertebrae. (d) Ten year old: The cervical spine now resembles the adult spine. The inferior and superior epiphyseal rings have not yet appeared.

Pediatric Cervical Spine

135

g-A

Neural arch

.>:.I h:k. \

d

Figure 2. The first cervical vertebra (atlas). a. Body: ossification center becomes visible during the first year of life. b. Neural arches: ossification center appears in utero at approximately the 7th fetal week. c. Synchondrosis of spinous process: fuses at approximately the third year of life. d. Synchondrosis about the body (neurocentral synchondrosis): fuses at approximately the seventh year of life. e. Ligament surrounding the superior vertebral notch: may ossify later in life. Reprinted with permission from Fielding JW. Cervical spine injuries in children. In: The Cervical Spine Research Society (eds): The cervical spine. Philadelphia, PA: JB Lippincott; 1983:288-81.

seventh fetal month. A secondary ossification center appears at the apex of the odontoid between 3 and 6 years and fuses with the odontoid by 12 years of age (l-5). The body of C2 develops from a single ossification center (rarely two), which appears by the 5th fetal month. The synchondrosis between the body and the odontoid fuses by 3 to 6 years of age. The fusion line commonly remains visible until age 11 and frequently is confused with a fracture. One-third of individuals will have a visible fusion line throughout life (l-5). The neural arches of C2 appear bilaterally by the 7th fetal month. They fuse posteriorly by 2 to 3 years. The synchondroses between the neural arches and the body/odontoid fuse between 3 and 6 years (l-5).

Figure 3. The second cervical vertebra (axis). a. Body: ossification center appears by the fifth fetal month. b. Neural arches: appear by the seventh fetal month. c. Synchondrosis of spinous process: fuses by the thlrd to sixth year of life. e. and i. Neurocentml synchondrosis: fuses by the third to sixth year. f. and G. Inferior eplphyseal ring: appears at puberty and fuses to body at approximately twenty-five years of life. g. Summit ossification center for odontoid: appears at approximately the third to the sixth years and fuses with the odontoid by the twelfth year of life. h. Odontoid: develops from two ossification centers which fuse by the seventh fetal month. j. Synchondrosis between the odontoid and body: fuses at approximately the third to sixth year of life. Reprinted with permission from Fielding JW: Cervical spine injuries in children. In: The Cervical Spine Research Society (eds). The cervical spine. Philadelphia, PA: JB Lippincott; 1983:288-81.

c3 to c7 The remaining cervical vertebrae (C3 to C7) can be discussed as a unit (see Figure 4). The body arises from a single ossification center (rarely two) by the fifth fetal month. The neural arches appear bilaterally by the 7th to 9th fetal week and fuse posteriorly by the 2nd to 3rd year. The anterior portion of the transverse process may develop from a separate ossification center and fuse with the neural arch by the 6th year. The synchondrosis between the neural arches and body fuse between 3 and 6 years (see Figure 5). A secondary ossification center appears at the tips of

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b

Figure 5. The neurocentral synchondroses (arrow) are frequently visible in young children (fuse by the third to sixth year) and may be confused with fracture lines.

changes as they pertain to the radiographic interpretation of the pediatric C-spine.

NORMAL VARIANTS

Figure 4. Typical cervical vertebra (C3-C7). a. Anterior portion of transverse process: may develop from a separate ossification center which fuses by the sixth year. b. Synchondrosis between the spinous processes: fuse by the third year. c. Secondary centers for bifid spinous processes: appear at puberty and fuse by the twenty-fifth year. d. Neurocentral synchondrosis: fuses at approximately the third to sixth year of life. e. Superior and inferior epiphyseal rings: appear at puberty and fuse with body by the twentyfifth year. Reprinted with permission from Fielding JW. Cervical spine injuries in children. In: The Cervical Spine Research Society (eds): The Cervical Spine. Philadelphia, PA: JB Lippincott; 1983:288-81.

the C3 to C7 cervical vertebrae at puberty and fuses with the spinous process at about age 25. Prior to ossification, this secondary center is frequently confused with a spinous process fracture (l-6). Secondary ossification centers also appear at puberty along the superior and inferior aspects of the cervical bodies (superior and inferior epiphyseal rings). These ossification centers fuse with the main body by age 25 and may be confused with chip fractures (see Figure 6). Table 1 demonstrates these major age-related

There are several normal anatomic variants seen in the radiologic interpretation of the pediatric C-spine as compared to the adult spine which can be confusing if not fully appreciated. Absent Lordosis In children up to age 16, absent lordosis of the lateral C-spine when the neck is held in the neutral position is a frequent finding (1,7). In the adult, this finding may be a sign of ligamentous injury. Cattell and Filtzer (7) found a rate of absent lordosis of 14% in the lateral roentgenogram of 160 normal children ranging in age from 1 to 16 years. Anterior Wedging In very young children, normal anterior wedging of the immature vertebral bodies as they ossify can produce the appearance of a compression fracture (see Figure 1B) (2). The fact that this variant is seen in several adjacent vertebral bodies suggests a normal variant as opposed to a compression fracture.

Pediatric Cervical Spine

137 Table 1. Radiographic Development of the Pediatric Cervical Spine Age 6 months

body of Cl not visible; all synchondroses

1 year

body Cl now visible

3 years

synchondroses of posteriorly processes fuse

3-6 years

neurocentral synchondroses fuse; synchrondrosis between odontoid and body of C2 fuses; summit ossification center appears at superior aspect of odontoid; anterior wedging of vertebral bodies resolve

6 years

pseudosubluxation and widening of predental space resolve; spine assumes a more lordotic appearance

puberty

secondary ossification centers appear at the tips of the spinous processes; superior and inferior epiphyseal rings appear; summit ossificaiton center of odontoid fuses secondary ossification centers at tips of spinous processes fuse; superior and inferior epiphyseal rings fuse to the main body

25 years

Figure 6. Fifteen year old: The superior and inferior epiphy seal rings are clearly visible. These ossification centers may be confused with chip fractures. The secondary ossification centers of the spinous processes are present but not visible in the photo.

Developmental Change open

located spinous

on 160 normal children in the age range 1 to 16 years. He found that 46% of children less than 8 years old (32 out of 70) demonstrated anterior pseudosubluxation of C-2 on C-3 of 3 millimeters (mm) or more. As an aid in distinguishing pseudosubluxation from true subluxation, Swischuk (10,ll) has developed the concept of the posterior cervical line (see Figure 8). This line is drawn from the anterior aspect of the spinous process of Cl to the anterior aspect of the spinous process of C3. If the posterior cervical line misses the anterior aspect of C2 spinous process by greater than or equal to 2 mm (1.5 mm is borderline), this finding is suggestive of hangman’s fracture or true subluxation. However, this concept of the posterior cervical line should only be applied to radiographs in which C2 is displaced anteriorly on C3. In normal pediatric individuals not exhibiting C2 on C3 displacement, the posterior cervical line will commonly miss the anterior aspect of C2 spinous process by 2 mm or more.

Widening of Predental Space Pseudosubluxation

When the neck is held in mild flexion in infants and small children, there may be an anterior pseudosubluxation between adjacent vertebrae (see Figure 7). This finding is due to the extreme laxity of the surrounding ligaments and is most marked at the level of C2 to C3 (1,2,7-g). Cattell and Filtzer (7) performed flexion and extension lateral roentgenograms

Another common variant found in the roentgenograms of children is an increase in the distance between the odontoid process and the anterior arch of the atlas (predental space) (see Figure 7) (3,7). This finding is due to the laxity of the transverse ligament. Cattell and Filtzer (7) found a distance of greater than 3 mm in 20% of patients less than 8 years old. In the adult, a distance of greater than 2.5 mm to 3 mm

Francis M. Fesmire and Robert C. Luten

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tissue density less than 7 mm anterior to C2 or less than three-quarters of the adjacent vertebral body’s width (14). However, these norms are extremely unreliable in small children as there are marked increases in prevertebral soft tissue width in small children when the neck is held in mild flexion or if the radiograph is taken during expiration (see Figures 1 and 7) (11).

CONGENITAL ANOMALIES Excluding major congenital malformations, there are two major congenital anomalies other than those mentioned in the developmental anatomy section that deserve mention.

OS Odontoideum OS odontoideum is a failure of the odontoid to fuse with the body of C2 (2,15,16). The odontoid is separated from the atlas by a thin layer of hyaline cartilage. Fairly insignificant flexion injury can result in odontoid subluxation with resulting quadriplegia or death (15). OS odontoideum can also be an acquired condition resulting from a failure of an odontoid fracture to heal (15,16).

Ossiculum Terminale

Figure 7. Three year old with a 4 mm anterior pseudosubluxation of C2 on C3 and a nonpathologic widened predental space of 4 mm. Note that the anterior aspect of the spinous processes of Cl through C3 lie on a straight line. This line would be broken in a true subluxation or a hangman’s fracture. The synchondrosis between the dens and body of C2 is unfused. Also note the normal anterior wedging of the vertebral bodies as well as the increased soft tissue space anterior to the cervical spine.

is felt to indicate a torn transverse ligament or a subluxation of Cl on C2 (12). In children less than 8 years, a distance greater than 3.5 mm is considered abnormal. However, distances up to 5 mm may be seen in normal children (13).

Prevertebral Soft Tissue Widening Prevertebral soft tissue widening due to edema and hemorrhage is an important radiographic finding in the interpretation of the adult C-spine. In the pediatric age groups, suggested norms have included soft

Ossiculum terminale is a failure of fusion of the apical segments of the dens (15). This condition is usually benign. However, there is one case of this anomaly leading to progressive atlanto-axial dislocation, quadriplegia, and death (17).

PEDIATRIC CERVICAL SPINE FRACTURES AND DISLOCATIONS Cervical spine injury is an extremely rare occurrence in children. Approximately 2% of all cervical spine fracture/dislocations occur in children less than 15 years old (18). The age distribution for pediatric cervical spine fractures is approximately 10% to 15% for age < 8 years, 20% to 25% for age 8 to 12 years, and 60% to 70% for age > 12 years (18-20). In one study, only 1.2% of all C-spine radiographs performed in children for evaluation of possible fractures revealed radiographic abnormalities (21). Even more rare is cervical spine fracture/dislocation in children less than 16 months if one excludes birth trauma. A re-

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139

A

C

B

Figure 8. The posterior cervical line (PCL) is drawn by connecting the anterior aspect of the spinous processes of Cl and C3. The concept of the posterior can only be applied to radiographs in which C2 Is displaced anteriorly on C3 (panels B and C). A. Subluxationlpseudosubluxation is absent: the anterior aspect of the spinous process of C2 will commonly miss the PCL by 2 mm-NORMAL or ABNORMAL (PCL cannot be applied). B. Pseudosubluxation is present: the anterior aspect of the spinous process of C2 lies on the PCL-NORMAL. C. Subluxation is present: the anterior aspect of the spinous process of C2 misses the PCL by 2 mm. This finding is suggestive of a Hangman’s fracture of the neural arches of CS-ABNORMAL.

view of several large pediatric series (147 patients total) reveals no cases of fracture/dislocation in children less than 16 months old except for 3 cases associated with birth trauma (18-21). The etiology of cervical spine fracture/dislocations is broad, but motor vehicle accidents and diving accidents/falls account for approximately 75% of the fracture/dislocations in the pediatric age group (Table 2) (18-22). The types of pediatric cervical spine injuries seen can be divided into those of the upper cervical spine (Cl to C2) and those of the lower cervical spine (C3 to C7). The two most common upper cervical fractures encountered are fracturekynchondral separation of odontoid with atlantoaxial dislocation, and the hangman’s fracture of the neural arches of C2 (2, 18-22,23,24). Other fractures commonly described in the upper cervical region are atlanto-occipital subluxation, rotary atlanto-axial subluxation, and C2 on C3 subluxation (18-22,25-29). Disruption of the transverse ligament with atlanto-axial subluxation is extremely rare in the pediatric age group due to the relative strength of the ligaments as compared to bone (2,25). Abnormalities of the lower cervical spine most commonly described are anterior subluxation/ dislocation, compression fractures, teardrop fractures, and spinous process fractures (2,18-21,25). The literature commonly states that for children less than 8 years old, cervical spinal fractures are con-

Table 2. Etiology of Cervical FractureslDislocations

MVA Diving/falls Sports injuries

Henrys

Hill

Racheschy

(16)

(19)

(21)

44% 27% 16%

31% 40% 29%

36% 40% 16%

fined mainly to the Cl to C2 regions and that for children greater than 8 years old, fractures occur in a distribution resembling adult fractures (approximately 75% of adult fractures occur in the lower cervical spine (2,18,19,25,30). An analysis of the literature (18-20) reveals that a more accurate statement may be that children greater than age 12 resemble adults in their distribution of fractures and that children ages 8 to 12 years are in a transition state between preponderance of high cervical lesions to low cervical lesions (Table 3). Reasons given for this tendency of young children to have a preponderance of Cl to C2 lesions relate to the developmental anatomy of the spine. Infants and young children have a relatively heavy head compared to their body. This fact coupled with the laxity of ligaments and nearly horizontal facet joints in the upper cervical vertebrae during the first years of life results in high torques and shear forces being applied to the Cl to C2 region (2,7,19). The prognosis for pediatric patients with cervical

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Table 3. Correlation of Level of Cervical Fractures/ Dislocations with Age (excluding birth trauma)

Hill Apple (19) (20)

Percent Cl-C2

fracture

Age

Henrys (18)

Cl-C2 c3-c7

<8 <8

4 1

8 0

6 0

14 1

Cl-C2 c3-c7

8-12 8-12

5 0

6 6

5 2

16 8

67%

Cl-C2 c3-c7

>12 >12

4 2

13 41

4 13

21 56

27%

Level of

Total

#Patients Henrys (18) Hill (19) Apple (20) Total

is relatively optimistic. The incidence of death is largely unknown as most studies exclude those patients arriving with a fatal injury. The reported incidence of spinal cord deficits resulting from cervical spine fracture/dislocations ranges from 24% to 36% with 11% to 13 % of those with spinal cord injury being rendered quadriplegic (1820). This incidence of cord deficit increases with age (Table 4).

SPINAL

< 8 years

93%

fracture/dislocation

PEDIATRIC

Table 4. Incidence of Neurological Deficit With Cervical Spine Fractures/Dislocations (excluding birth trauma)

CORD INJURIES

Acute spinal cord injuries are rare in the pediatric population. Approximately 1% to 3.3% of all spinal injuries occur in the age group less than 16 years (3133). Kewalramani and coworkers (34), conducted an exhaustive epidemiologic analysis of all spinal cord injuries in an 18-county region of California and discovered that 9.4% of the spinal injuries occurred in children less than 16 years old with an injury rate of 18.2 cases per million. In this study, 44 of 58 cord lesions were cervical (76%) and 14 of 58 were thoracic or lumbar (24%). The etiology of acute spinal cord injuries closely parallels the etiology of cervical spine fractures with motor vehicle accidents and diving accidents/falls accounting for approximately 75% of cord injuries (35,36). Neurologic examination of patients with spinal cord deficits reveal four distinct syndromes: complete cord transection, central cord syndrome, Brown-Sequard syndrome, and anterior cord syndrome. A complete cord transection is defined as total loss of motor and sensory modalities distal to the site of the lesion and carries a dismal prognosis. A central cord syndrome results from damage to the central gray matter and most central regions of the pyramidal and spinothalamic tracts. The pathophysiology of cord damage is felt to be secondary to contusion produced by the ligamentum flavum buckling into the cord dur-

9 7 5 21

Deficit 2 0 2 4 (19%)

8-l 8 years # Patients 9 67 24 100

Deficit 5 27 9 41 (41%)

ing severe hyperextension of the neck. These patients have a greater neurologic deficit in the upper extremities as compared to the lower extremities and frequently have near full recovery of neurologic function as edema and cord contusion resolve. The Brown-Sequard syndrome results from hemisection of the spinal cord with patients demonstrating ipsilateral motor deficit and contralateral sensory dysfunction. Prognosis is good due to the unilateral nature of the deficits, and most retain bowel and bladder control. The anterior cord syndrome results from injuries producing either contusion to the anterior cord or laceration or thrombosis of the anterior spinal artery. These patients exhibit various degrees of paralysis and sensory loss below the level of injury with preservation of posterior column functions (36,37). As stated earlier, the incidence of cervical spinal cord injuries with cervical spinal fracture/dislocations ranges from 29% to 36% with 11% to 13% of those with spinal cord injury being rendered quadriplegic (1 S-20). Even more perplexing to the emergency physician is the syndrome of Spinal Cord Injury Without Radiographic Abnormalities (SCIWORA) in children. The reported incidence of SCIWORA ranges from 4% to 67% of all pediatric spinal injuries in series to date (Table 5) (19,33-36,38-40). However, most of these series data are derived from rehabilitation facilities and are not representative of true incidences. Kewalramani and coworkers (34) in their epidemiologic analysis of 16 California counties found an incidence of 20% of all pediatric spinal injuries, which probably most accurately reflects true incidence of this syndrome. Pang and Wilberger (36) conducted a detailed study of SCIWORA in 24 children (aged 6 months to 16 years). Eighty-three percent of the lesions involved the cervical cord. Fifty-eight percent of the lesions involved children less than 8 years, and 42% involved children 8 years or older. There were 7 cases of complete cord transection and 10 cases of central cord syndrome. All patients with complete cord syndrome were less than eight years old. Interestingly, 13 pa-

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Table 5. Incidencee of SCIWORA (Spinal Cord Injury Without Rediographic Abnormality) in Pediatric Patients With Spinal Cord Injury Melzak (1969) (33) Burke (1971) (36) Hachen (1977) (39) Andrews & Jung (1979) (40) Anderson & Schutt (1960) (35) Kewalramani et al (1960) (34) Pang & Wilberger (1962) (36) Hill et al (1964) (19)

16 (55%) 12 (50%) 6 (44%) 7 (47%) 2 (4.5%) 5 (20%) 24 (67%) 1 (4%)

tients in this series (54%) had a delayed onset of neurologic deficit (range, 30 minutes to 4 days; mean, 1.2 days). The nature of cord injuries in this subset with delayed onset of neurologic deficit consisted of 2 complete cord, 7 central cord, and 4 partial cord. Seven of these 13 patients later recalled transient paresthesias at the time of the injury. The authors were unable to detect any unique clues in age distribution or mechanisms of injury to distinguish this subgroup of patients from those patients with immediate cord deficits. Pang and Wilberger conclude that all pediatric patients with a history of significant neck trauma who give a history of paresthesias should receive a full investigative work-up. The pathophysiology of SCIWORA is thought to result from a diverse multitude of mechanisms all resulting in a disruption of microvascular blood supply. Mechanisms proposed include hyperextension with inward bulging of interlaminar ligaments, reversible disc prolapse, flexion compression of the cord, longitudinal distraction of cord, and vertebral artery spasm or thrombosis (20,36). Doubtless, several of these mechanisms work in combination to produce SCIWORA depending on the mechnism of neck injury.

The diagnosis of SCIWORA should only be made after occult fractures and ligament/disk damage have been ruled out by CT scanning, flexion-extension films under fluoroscopy, and myelography. Prognosis in SCIWORA depends on the extent of spinal cord abnormality. Those with severe cervical cord abnormalities do poorly while those with partial cord deficits usually recover to some degree and do quite well. Physicians should be alert to the possiblity of SCIWORA. All children with significant mechanism of injury to the neck and normal cervical spine by radiograph should be questioned specifically for transient paresthesias at the time of the accident. If present, these children should be considered to have a spinal cord injury until proven otherwise.

SUMMARY The evaluation of the pediatric cervical spine can be a perplexing problem for the emergency physician. Given the wide range of variances in the ossification centers, the unfused synchondroses, and the relative hypermobility of the pediatric C-spine, radiographs may easily be misread if one is not thoroughly familiar with these developmental aspects. Even more perplexing is the fact that if one correctly interprets a radiograph as normal, a small percentage of these children may still have a spinal cord abnormality which may not manifest itself in the immediate postinjury period. All children with a history of significant neck trauma and a normal neurologic exam should be questioned specifically regarding paresthesias at the time of the accident. If present, these children should be considered to have a cervical spine injury until proven otherwise.

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