Cervical spine anomalies in children and adolescents are rare. However, knowledge on how to recognize and treat cervical anomalies in the paediatric population is important to prevent possible neurologic complications. In addition, anatomic anomalies of the cervical spine in paediatric patients often coexist with skeletal dysplasias, connective tissue disorders and other genetically inherited metabolic disorders. These can be an indication for performing screening studies to rule out other organ system abnormalities such as renal or cardiac anomalies as well.
Due to the unique developmental anatomy of the upper cervical spine (i.e. C1, C2), knowledge on the development of the different ossification centres is important in order to effectively perform a radiographic evaluation.
The atlas develops from three ossification centres. The first ossification centre to appear is the body, which usually appears by 1 year . The posterior arches fuse by 3–4 years, and the body fuses to the lateral masses by 7 years. Thus, at 7 years of age, the atlas should be completely visible on cervical spine radiographs .
The axis develops from five ossification centres. The body fuses to the dens by age 6 and the dens fuses to the cranial tip (called ossiculum terminale) by age 12 [1,2].
The subaxial cervical spine (C3 and below) approaches adult morphology by age 7–8 [1,2]. Differences in the ossification centres and development of the upper cervical and subaxial cervical spine is the reason why the majority of cervical spine injuries in children under the age of 8 years are in the upper cervical spine (where ossification centres have not fused yet) and those who are over the age of 8 years exhibit more adult-type patterns of injury with trauma. Reasons for this include the hypermobility and ligamentous laxity seen in younger children, shallow and angled facet joints, incomplete ossification of the odontoid as well as weak neck muscles holding up a relatively large head [2–4].
Due to the developmental anatomy of the cervical spine, radiographic evaluation can be difficult. For example, if the odontoid has not completely fused to the body (which is the case in children under the age of 6 years), a radiograph might give the impression of a false odontoid fracture due to the synchondrosis. Therefore, general knowledge of the various ossification centres mentioned in the prior section is important to have in interpreting radiographs. In addition, in patients under the age of 7 years, the presence of the apophyses and incomplete ossification will make the cervical vertebra bodies appear oval or wedge-shaped (Fig. 1). Once patients are older (i.e. >8 years), the vertebral bodies will take a more rectangular shape similar to adults.
Some important things to recognize in the cervical spine are alignment of the spinous processes, spinolaminar line, posterior vertebral body line and the anterior vertebral body line all seen on the lateral view. All the lines should follow a smooth outline from one level to the next, and any nonharmonious transitions should increase suspicion for subluxations, congenital stenosis of C1 or other types of disease. In addition, the cervical spine rarely exhibits scoliosis and, if it does, may be a sign of early-onset scoliosis in more caudal regions of the spine. In this case, a thorough set of radiographs of the entire spine is necessary.
Sometimes, a pseudosubluxation of C2–C3 or of C3–C4 is seen in 20–46% of children under the age of 7 years [4,5]. This is of no clinical consequence, and a true injury can be ruled out by seeing the alignment of the anterior aspect of the spinous processes (Fig. 1). A line drawn should not have any spinous process more than 1 mm from the line connecting the spinous processes from C1 to C4 . In addition, the regional alignment of the cervical spine might be kyphotic in the paediatric patient before taking the normal cervical lordosis seen in adults. This can be seen in up to 15–40% of children less than 16 years of age [2,7▪].
If clinical suspicion is high or if cervical spine studies are being performed as a screening study for patients under the age of 7 years (i.e. patients with high risk for cervical spine anomalies such as Down's syndrome, Morquio's syndrome, juvenile rheumatoid arthritis, skeletal dysplasias, and so on) (Table 1), lateral cervical spine radiographs should also include flexion and extension radiographs, as this can help in assessing instability and for guiding the use of additional studies. MRI or computed tomography (CT) scans used to more closely evaluate the cervical spine are recommended. This is especially valuable for evaluating congenital abnormalities, basilar invagination as well as other diseases such as Chiari malformations. Although CT scans had traditionally been known to provide better detail on the bony anatomy, recent developments in MRI sequencing, although operator dependent, can provide excellent detail on bony anatomy without exposure to ionizing radiation, a concern amongst many who take care of paediatric patients.
For those paediatric patients in whom the osseous anatomy can be visualized on cervical spine radiographs (i.e. patients >8 years of age), a lateral image can be very informative for detecting abnormalities. In addition to the lines mentioned previously in the text, important relationships to visualize are the position of the odontoid in relation to the foramen magnum as well as the relationship of the axis to the atlas. Proximal invasion of the odontoid into the foramen magnum can be demonstrated by drawing a line from the basion to the opisthion, and if any portion of the odontoid invades this line it can be a sign of basilar invagination.
The atlantoaxial relationship is evaluated on the lateral radiographs by the use of the atlantodens interval (ADI). Typically, an ADI less than 5 mm in young children (<8 years old) is normal and this decreases to 3 mm in patients more skeletally mature. Increased ADI can be a sign of C1–C2 instability. The space available for the chord (SAC) is also an important radiographic parameter for evaluating C1–C2 instability. The typical SAC follows Steel's rule of thirds. Specifically, at the level of the odontoid, the spinal cord, free space and the bone of the odontoid should each occupy one-third of space within the ring of C1.
On an open-mouth odontoid view, an overhang of the lateral masses of C1 on C2 can be seen and mistaken for a fracture or atlantoaxial rotatory subluxation (AARS). In children, this has been called the pseudo-Jefferson fracture and is common in patients up to 4 years old and may be seen in patients up to 7 years old . An overhang of approximately 6 mm is normal between the lateral masses relative to the lateral aspect of C2 in these children.
Another anomaly that should be recognized is the recent description of spondylolysis or incomplete/delayed ossification of the posterior arch of C2 in patients with Menkes disease. This can give the appearance of nonaccident trauma (i.e. child abuse), but was seen in 11% of patients with Menkes disease [9▪,10].
TYPES OF CERVICAL SPINE ANOMALIES IN CHILDREN
Various cervical spine anomalies exist in paediatric patients. A thorough understanding of the anatomy is critical to arriving at the correct diagnosis. Often, plain radiographs can lead to the diagnosis. If the anatomy is difficult to discern, an MRI can be used. In these patients, a CT scan can be performed for patients who are surgical candidates in order to prevent exposure to radiation unnecessarily.
Basilar impression (a.k.a. basilar invagination) occurs when the upper cervical spine is invaginated upward into the foramen magnum. This results in a compression of the contents of the posterior cranial fossa (often the cerebellum, midbrain and the spinal cord) because the contents of the posterior fossa are bounded by the tentorium above. On the basis of the severity of this compression, patients can be asymptomatic or can exhibit symptoms consistent with compression in this region. Specifically, there can be a compromise of the circulation along the posterior inferior cerebellar artery as well as impingement of the cisternae resulting in a block to the normal flow of cerebrospinal fluid. Therefore, the diagnosis can often be confused with syringomyelia, amyotrophic lateral sclerosis and multiple sclerosis. Motor or sensory symptoms can be seen in up to 85% of patients .
It is commonly associated with systemic disorders such as achondroplasia, osteogenesis imperfecta, Morquio syndrome, and cleidocranial dysplasia as well as spondyloepiphyseal dysplasia. It can also be associated with other anomalies such as Klippel–Feil syndrome, hypoplasia of the atlas and occipitocervical synostosis.
Its diagnosis is primarily made by radiographic criteria. On a lateral radiograph, the odontoid will be displaced much more cranially than normal and many times can be seen abutting the clivus (basion). Normally, the odontoid should be caudal to the foramen magnum.
In the paediatric population, the diagnosis can be made with lateral radiographs or MRI. Contrast is not needed to make the diagnosis unless it is caused by tumours in the posterior fossa or suspicion for an oncologic or infectious process is high. CT scans are not necessary initial studies and can usually be performed to aid in surgical planning if needed.
C1–C2 INSTABILITY (ATLANTOAXIAL INSTABILITY)
The diagnosis for C1–C2 instability is made by radiographic criteria. On flexion and extension lateral radiographs of the cervical spine, the ADI should never exceed 5 mm, and, if so, the diagnosis of C1–C2 instability is made.
In the paediatric population, this can be caused by ligamentous laxity (i.e. Down's syndrome), hypoplasia of the odontoid (in Morquio syndrome and spondyloepiphyseal dysplasia) or inflammation of the C1–C2 articulation at the odontoid and anterior arch of C1 (as seen in juvenile rheumatoid arthritis) [2,3].
All patients should have a thorough neurologic examination. Those who exhibit signs of myelopathy should be evaluated by a spine surgeon for possible surgical stabilization. Usually, those who are symptomatic will need to undergo surgical fusion. Some asymptomatic patients may also need surgical stabilization if there are coexistent anatomic abnormalities in the cervical spine. One example is when C1–C2 instability coexists with a hypoplastic posterior arch of C1. This will result in a decreased SAC, and therefore these patients will be at a high risk for neurologic injury. Some recommend prophylactic surgical stabilization of these patients to prevent possible catastrophic neurologic injury. In cases of Morquio syndrome or spondyloepiphyseal dysplasia, surgical stabilization is indicated under the setting of C1–C2 instability even if the patient is asymptomatic.
ATLANTOAXIAL ROTATORY SUBLUXATION
AARS is a radiographic diagnosis made on the basis of an open mouth odontoid view. On this radiograph, attention is paid to the lateral masses. The size of the lateral masses should be symmetric on C2. If one side is larger than the other, or if there is a greater amount of lateral mass overhang on one side than the other, there should be a high suspicion for AARS. Subsequently, a CT scan can help in aiding the diagnosis, especially in mild cases, and a dynamic CT study can help in distinguishing fixed from flexible deformities. Usually, patients with AARS will clinically present with torticollis; so, the combination of radiographs and CT scans can help in distinguishing AARS from the clinically similar presentations seen in congenital muscular torticollis. Neurologic symptoms are rare, and therefore surgical management can proceed on an elective basis.
Those deformities that are fixed on dynamic CT studies will fail nonsurgical measures for management. Mobile subluxations can undergo a trial of nonsteroidal anti-inflammatory medication, as, in the absence of trauma, the cause is thought to be a postinflammatory reaction to an upper respiratory tract infection (i.e Grisel syndrome) [2,3]. In some cases, halo traction can also be used to aid in the reduction of AARS. If the subluxation is able to be reduced via closed methods, a trial of rigid collar immobilization can be used. Usually, a Miami J collar for 2–3 months is trialled, and, if there is persistent subluxation or a fixed deformity, surgery can be explored. The purpose of surgical intervention is to prevent a fix deformity rather than to decompress the spinal cord.
Congenital anomalies of the paediatric cervical spine include congenital occipitocervical synostosis, congenital unilateral absence of C1, odontoid anomalies and Klippel–Feil syndrome. These congenital anomalies are very rare.
In congenital occipitocervical synostosis, the occiput is partially or completely fused to C1. This results in excessive motion at the C1–C2 joint and therefore can lead to subsequent C1–C2 instability that is seen in as many as 50% of patients [2–4]. Patients can be asymptomatic throughout life or develop symptoms after mild trauma. Physical examination findings that may lead to a heightened suspicion for this are a short broad neck, low hairline, torticollis, a high riding scapula or limited range of motion of the neck [2–4]. Klippel–Feil syndrome is a congenital fusion of the cervical spine that can range from one motion segment to all. Therefore, occipitocervical synostosis can be considered to be a type of Klippel–Feil syndrome. If this is seen on radiographs, there should be a high suspicion for ruling out other disorders such as Sprengel's deformity, renal anomalies, and congenital heart disease as well as impairments in hearing [2–4,11]. Patients with this condition can develop hypermobility at mobile segments adjacent to the congenitally fused segment, resulting in early development of degenerative arthritis (Fig. 2).
Congenital unilateral absence of C1 is very rare. It is also associated with other systemic anomalies such as tracheoesophageal fistula. As a result of the congenital absence, patients develop different degrees of torticollis, which can start at birth or develop later . Surgery is necessary in these patients to prevent progression and neurologic compromise. Ideally, the fusion is performed between the ages of 5 and 8 years .
Odontoid anomalies can range from a complete absence to varying degrees of hypoplasia. This can lead to varying degrees of C1–C2 instability. Surgical intervention is necessary for symptomatic patients or those who are asymptomatic but demonstrate an ADI greater than 10 mm.
IATROGENIC CERVICAL ANOMALIES
Paediatric patients can also develop iatrogenic deformities after prior surgery. Usually, patients whom we have seen are those who have had tumours of the spine that necessitated laminectomies in the past. These patients develop postlaminectomy kyphosis, which may initially be cosmetically displeasing; however, in the future they can develop myelopathy and neurologic compromise. Usually, after a period of surveillance, surgical correction of the kyphosis can help to maintain forward gaze and fix the deformity. I personally do not recommend the surgical management of these patients until they have been disease free for at least 5 years. Clear radiographic visualization is imperative for ruling out recurrent disease and this can be difficult when spinal instrumentation is in place. Paediatric patients who have had prior laminectomies for oncologic reasons should be followed by a spine surgeon annually to follow the development of kyphotic deformities.
Cervical spine anomalies in the paediatric patient need to be recognized as early as possible to prevent permanent neurologic injury. Often, the developmental anatomy of the paediatric cervical spine makes it difficult to recognize the anomalies. However, familiarity with the ossification centres and normal radiographic appearance of the cervical spine in children can optimize correct image interpretation and diagnosis in these patients. In addition, high suspicion for patients with various genetic and metabolic syndromes who are at a high risk for cervical spine anomalies is important to maximize function in these patients. Referral to a spine surgeon is recommended in order to deliver comprehensive care to paediatric patients with cervical spine anomalies.
Conflicts of interest
Han Jo Kim MD is on the Spinal Innovation Advisory Board for Medtronic, Inc.
REFERENCES AND RECOMMENDED READING
Papers of particular interest, published within the annual period of review, have been highlighted as:
- ▪ of special interest
- ▪▪ of outstanding interest
Additional references related to this topic can also be found in the Current World Literature section in this issue (pp. 151–152).
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This study reviewed 35 patients with Menkes disease from the National Institutes of Health (NIH) database and found that 11% of patients had either spondylolysis or incomplete ossification of the posterior arches of C2, giving the appearance of a Hangman's fracture that is associated with child abuse in paediatric patients.
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