Original Research
Neuroradiology/Head and Neck Imaging
January 2009

Evaluation of the Pediatric Craniocervical Junction on MDCT

Abstract

OBJECTIVE. The purpose of our study was to establish normal values on MDCT images for the measurement of various craniocervical junction relationships in children and to address discrepancies in the literature based on radiographic values.
MATERIALS AND METHODS. Accepted methods of evaluating the craniocervical junction were used to calculate normal values in 117 normal children on MDCT images with multiplanar reconstructions. The basion-axial interval, basion-dens interval, Powers ratio, atlantodental interval, and atlantooccipital interval were measured in each patient and compared with accepted data based on radiographs.
RESULTS. The basion-axial interval was difficult to reproduce on MDCT images. In 97.5% of patients, the basion-dens interval was less than 10.5 mm compared with 12 mm based on data from radiographs. Separating the patient population into those in whom the os terminale was ossified and those in whom it was not revealed a difference of 2 mm in the upper limit of normal (9.5 and 11.6 mm, respectively). The Powers ratio showed no significant difference compared with data obtained using radiographs. In 97.5% of the population, the atlantodental interval was less than 2.6 mm, compared with 4-5 mm measured on radiographs. The atlantooccipital interval showed 97.5% of the population falling below 2.5 mm at any point in the joint space, compared with the previously accepted value of 5 mm.
CONCLUSION. Normal values for the craniocervical junction articulations and relationships as seen on MDCT are different from the accepted ranges of normal based on radiographs. The values should be considered the normal values in the pediatric population on MDCT.

Introduction

Injuries to the pediatric cervical spine are significantly different from those encountered in the adult population. For the purposes of defining the pediatric population with respect to the cervical spine, it is known that by the time a child is 8-10 years old, the cervical spine reaches adult proportions [1-3]. Furthermore, after the age of 10-12 years, the clinical sequelae of adult and pediatric cervical spine trauma are similar [2, 4]. Children are more susceptible than adults to injuries at the craniocervical junction because of inherited anatomic differences in the cervical spine. In general, children have relatively weaker cervical musculature, a larger head size relative to the body, more ligamentous laxity, and a flatter contour of the occipital condyles than adults have [1, 2, 4-7]. These factors make children more predisposed to atlantooccipital dissociation injuries than their adult counterparts.
The craniocervical junction is defined by Harris [8] as the region extending from the basiocciput to the second cervical interspace. It is held in place by ligaments and articulations between the occiput, atlas, and axis. Unfortunately, this area is difficult to evaluate on radiographs because of multiple superimposed structures; therefore, authors have developed indirect methods to serve as indicators of injury. Harris et al. [9] proposed a method to evaluate for atlantooccipital dissociations on the contact lateral cervical spine radiograph using the basion-axial interval. All the children in their study population had a basion-axial interval between 0 and 12 mm. Several other authors have used the basiondens interval, as published in the Keats and Sistrom Atlas of Radiologic Measurement [10], to assess for atlantooccipital dissociation. The upper limits of normal range between 12 and 12.5 mm for this method based on radiographs [10]. In 1987, Kaufman et al. [11] measured the atlantooccipital joint space in 100 children and determined that the value should be less than 5 mm at any given point in the joint. This method is conceptually the most reliable method for detecting atlantooccipital dissociation; however, it is difficult to reproduce on radiographs.
Fig. 1 —Basion-axial interval (BAI). Midsagittal MDCT image of craniocervical junction in 5-year-old boy shows posterior axial line drawn along posterior cortex of body of axis and extended cranially. Basion-axial interval is distance between basion and this line.
Fig. 2A —Basion-dens interval (BDI). Midsagittal MDCT images of craniocervical junction show basion-dens interval as distance from most inferior portion of basion to closest point of superior aspect of dens. 5-year-old boy without ossification of os terminale and normal basion-dens interval measuring 10 mm.
Fig. 2B —Basion-dens interval (BDI). Midsagittal MDCT images of craniocervical junction show basion-dens interval as distance from most inferior portion of basion to closest point of superior aspect of dens. 7-year-old girl with ossified os terminale and normal basion-dens interval measuring 6 mm.
Other methods for detecting craniocervical junction injury using radiographs include the Powers ratio and the atlantodental interval. The Powers ratio has been used to evaluate for atlantooccipital dissociation and is considered normal when the value is less than 1 [12]. However, this method is sensitive only for evaluating anterior atlantooccipital dissociation. A posterior dissociation or vertical distraction injury could result in a normal value and consequently go undiagnosed. The atlantodental interval is a measurement used to evaluate the atlantoaxial relationship. This distance, described by Hinck and Hopkins [13], is conventionally held to be normal when it is 4-5 mm in children.
Currently, the approach to the acutely traumatized pediatric patient with a clinical suspicion of cervical spine injury varies from institution to institution. For reasons including radiation exposure, cost-effectiveness, and others, most protocols use conventional radiographs for the initial evaluation. However, others advocate the use of CT [14-16]. As technology advances, MDCT with multi-planar reconstructions (MPRs) has become, in many centers, the first step when evaluating the acute cervical spine [14-21]. For this reason, we want to objectively determine normal anatomic values of the craniocervical junction relationships based on MDCT reconstructed images.

Materials and Methods

Our patient population consisted of 117 pediatric patients selected from a group of 179 patients who presented to our hospital emergency department between May 2004 and March 2007 and underwent MDCT of the head and cervical spine with MPRs as part of a trauma protocol. Conventional radiography of the cervical spine was not performed on patients in the study population. Patients were evaluated for cervical spine injury and were included in our study if no osseous or soft-tissue abnormality was detected on initial CT and if the patient was discharged from the hospital without a diagnosis of a cervical spine or head injury.
The subjects selected for our study ranged from 2 months to 10 years old (mean age, 4 years 8 months) and had no known prior cervical spine injury or anomaly. Because of the broad age range through which ossification of various landmarks at the cervicocranium occurs, the study population was not further subdivided on the basis of patient age. However, the study population was subdivided on the basis of ossification of bone structures that serve as anatomic landmarks for several of the measurements performed. Of the 117 patients, 67 patients were boys (57.3%) and 50 were girls (42.7%). Cervical spine imaging was performed with the patient in the neutral position without IV contrast material using a 16-MDCT scanner, with the following standard protocol: 16 × 0.75 mm collimation with 1-mm-thick sections, 0.5-mm overlap, and a pitch of 0.942. Axial images were reconstructed at 1 mm, and three contiguous sections were fused for review and storage on a PACS workstation. Reconstructions in both sagittal and coronal planes were obtained routinely from 1-mm axial reconstructions. MPRs were reformatted to 3-mm thickness every 3 mm through the entire spine. A 16-cm field of view, 512 × 512 matrix, 140 kV, and 100 mAs were generally used; however, these factors were sometimes altered to obtain the lowest achievable radiation dose. Examinations selected for inclusion in our study were free from motion artifacts. The images were analyzed using a preset bone window setting (level, 450 HU; width, 1,700 HU).
Using a PACS workstation, a total of 15 measurements were obtained in each patient, including the basion-axial interval, basion-dens interval, Powers ratio, atlantodental interval, and bilateral atlantooccipital interval. Although the in-plane resolution achievable using the technical parameters mentioned previously is 0.3125 mm, our workstation provided measurements to the nearest hundredth of a millimeter. These values were rounded to the nearest tenth of a millimeter.
The basion-axial interval was measured according to the method described by Harris et al. [9] as the perpendicular distance between the basion and the rostral extension of the posterior cortical margin of the body of the axis. The posterior axial line is a line drawn along the posterior cortex of the body of the axis and extended cranially. The basion-axial interval is the distance between the basion and this line; it was measured in the midsagittal plane [9] (Fig. 1).
The basion-dens interval was obtained by measuring the shortest distance from the most inferior portion of the basion to the closest ossified point of the superior aspect of the dens in the midsagittal plane. Patients were divided into two groups on the basis of the presence or absence of an ossified os terminale. If the os terminale was visualized (ossified), the basion-dens interval was drawn to the os terminale. If an os terminale could not be identified, the basion-dens interval was extended to the most superior aspect of the ossified dens [22] (Figs. 2A, and 2B).
Fig. 3 —Powers ratio. Midsagittal MDCT image of craniocervical junction in 5-year-old boy shows Powers ratio, which is calculated by dividing distance between tip of basion and spinolaminar line by distance from tip of opisthion to midpoint of posterior aspect of anterior arch of C1 vertebra.
Fig. 4 —Atlantodental interval (ADI). Midsagittal MDCT image of craniocervical junction in 5-year-old boy shows atlantodental interval, which is calculated by drawing a line from posterior aspect of anterior arch of C1 vertebra to most anterior aspect of dens at inferior margin of anterior arch of C1.
Fig. 5 —Atlantooccipital interval (AOI). Sagittal MDCT image of craniocervical junction in 5-year-old boy shows atlantooccipital interval, which is calculated by drawing a line perpendicular to articular surfaces of occipital condyle and lateral mass of C1 vertebra. Five evenly spaced measurements are performed from anterior to posterior in joint space.
The Powers ratio was calculated by dividing the distance between the tip of the basion and the spinolaminar line of the atlas by the distance between the tip of the opisthion and the midpoint of the posterior aspect of the anterior arch of the C1 vertebra [12] (Fig. 3). This measurement was not performed if the anterior or posterior arches of C1 were not visualized in the midsagittal plane either because of lack of ossification of the anterior arch of C1 or, less likely, because of incomplete fusion of the posterior neural arches.
The atlantodental interval was measured by drawing a line from the inferoposterior aspect of the anterior arch of C1 to the most anterior aspect of the dens. This measurement was performed in the midsagittal plane and was performed only when the anterior arch of C1 was ossified [13, 23] (Fig. 4).
The atlantooccipital interval was calculated by drawing a line perpendicular to the articular surfaces of the occipital condyle and the lateral mass of C1. A total of five evenly spaced measurements were performed from anterior to posterior in the joint space as described by Kaufman et al. [11]. Measurements of the atlantooccipital interval were performed bilaterally (Fig. 5).
For each of the methods used, a mean, SD, standard error of the mean (SEM), and range were calculated. Normal maximum values were defined as the value inclusive of 97.5% of the study population and were calculated as two SDs above the mean. After establishing normal values, we compared these values with previously accepted data from radiographs in the literature [10]. Finally, the data for boys and girls were separated and the calculations were again performed to evaluate for sex differences.

Results

There are differences between previously published normal values based on radiographs for several of the methods and data based on MDCT images for the study population (Table 1). The basion-axial interval has been found to be difficult to reproduce on MDCT images in the past [24]. Analysis of the pediatric patient population indicates similar limitations when using this method. The basion-axial interval was also found to have a large SEM. Furthermore, a number of individuals were found to have basion-axial interval measurements greater than the upper accepted norm of 12 mm [9], and others were found to have negative basion-axial interval values. Both of these scenarios are contrary to the report by Harris et al. [9] of measurements in the pediatric population using radiographs.
TABLE 1 : Normal Anatomic Relationships of Craniocervical Junction on MDCT Images in 117 Children and Comparison with Accepted Values on Radiographs
MDCT ValueMDCT Normal ValueaRadiography Normal Value [9, 11, 12, 23, 25, 26]
RelationshipMeanSDRange
Basion-axial interval2.93.28−5.2 to 14.0Not reliable>0 to <12.0
Basion-dens interval     
    With ossification6.21.661.3-9.9<9.5<12, <12.5
    Without ossification7.81.903.6-11.0<11.6<12, <12.5
Powers ratio0.70.080.6-1.0<0.9<1.0
Atlantodental interval1.40.590.4-3.2<2.6<4.0-5.0
Atlantooccipital interval     
    Left1.60.490.4-3.1<2.5<5.0
    Right
1.6
0.45
0.5-3.3
<2.5
<5.0
Note—Except for the Powers ratio, results are given in millimeters.
a
Normal value = maximum value for 97.5% of the population.
The commonly accepted normative upper limit of the basion-dens interval in children—12-12.5 mm [25, 26]—was found to be excessive as the maximum distance recorded in the study population was 11 mm, and a distance of 10.5 mm would be inclusive of 97.5% of patients. By separating the patient population into those in whom the os terminale is present and those in whom it is absent, more precise results are obtained. The age range of patients with ossification of the os terminale was between 21 months and 10 years (n = 81), whereas the age range of patients without ossification was between 6 months and 4 years (n = 36). In patients with ossification of the os terminale, the maximum value obtained was 9.9 mm, and a value of 9.5 mm would be inclusive of 97.5% of the population. In those patients in whom the os terminale is not yet ossified, the maximum value obtained in this study was 11 mm, and a value of 11.6 mm would be inclusive of 97.5% of the population.
Analysis of the Powers ratio showed 97.5% of the population to have a ratio of < 0.9, which corresponds with the currently accepted norm [12]. However, the Powers ratio was obtained in only 99 of the 117 patients included in the study because either the anterior arch of C1 was not yet ossified or the posterior neural arches of C1 were not yet fused.
Although the normal maximal atlantodental interval using radiographs is thought to be between 4 and 5 mm in children [23], the maximum value obtained in the study population was 3.2 mm; 97.5% of patients should have a value less than 2.6 mm. The atlantodental interval was calculable in only 110 patients of the 117 patients in the study group.
The atlantooccipital interval was calculated on both atlantooccipital joints in all 117 patients in the study group. The calculated normal values for the atlantooccipital interval were significantly smaller than those pertaining to data obtained from radiographs, in which a value of less than 5 mm is considered normal [11]. The maximum measured distance for any point in the joint space on the right side was 3.3 mm, and the calculated upper limit of normal inclusive of 97.5% of patients was 2.5 mm. Similar values were obtained on the left side, with a maximum measured distance of 3.1 mm and an upper limit of normal calculated to be 2.5 mm. These measurements were found to be easily reproducible and had a small SEM.
Comparisons of the individual means and upper limits of normal revealed no differences in any of the measured values when comparing boys and girls for any of the methods used.

Discussion

Accurate methods of evaluating the craniocervical junction are of utmost importance in assessing for atlantooccipital dissociation injuries in the setting of acute cervical spine trauma. Furthermore, measurements of the normal anatomic relationships of the craniocervical junction on MDCT images are different from those published in the literature that are based on radiographs. Although the published measurements of these relationships on radiographs likely remain valid for radiographs, they should not be applied when assessing the cervical spine on MDCT images. For each method of measurement, the published radiographic normal value is larger than the value obtained for MDCT images. Thus, use of radiographic normal values could result in failure to identify pathologically increased measurements and subsequently missed injuries. Magnification in standard radiographic technique and limitations in accuracy of radiographic measurements are probably the causes of the bulk of the differences between the two techniques.
Atlantooccipital dissociation injuries include both atlantooccipital dislocations and atlantooccipital subluxations. Although dislocations are usually fatal, subluxations are rarely fatal but occur with less frequency than dislocations [8]. For this reason, much attention has been paid to this region to identify patients who have had subluxation injuries so that they may be appropriately managed. Harris et al. [9] described a method using the relationship between the basion and the posterior axial line; they calculated the normal value for this technique in 50 pediatric patients on radiographs. However, this method has been shown to be difficult to translate to MDCT images when evaluating the adult craniocervical junction because of inconsistencies in selecting the posterior axial line [24]. Similarly, when evaluating the pediatric craniocervical junction on MDCT images, this method was found to be difficult to perform and to have a broad range of normal values. For these reasons, this method is not thought to be a useful tool to assess for atlantooccipital dissociation on MDCT images.
Several authors have used radiographs to assess the normal space between the tip of the basion and the tip of the dens in children [12, 22, 25, 26]. However, no data at this time apply this method to MDCT images in children. The basion-dens interval has been shown to be an easily performed and reproducible method of assessing the craniocervical junction when using both radiographs and MDCT images; however, the results of this study show that the normal values are quite different when comparing the two imaging techniques. Pang et al. [27] assessed the sensitivity of the basion-dens interval in 16 patients with known atlantooccipital dissociation and reported a low sensitivity of 50%. However, those authors used the published radiographic upper limit of normal (12 mm) as the threshold for atlantooccipital dissociation and applied this value to MDCT images. Although the basion-dens interval is an indirect method of assessing for atlantooccipital dissociation, it is likely to be made more sensitive by applying the normal upper limits based on MDCT as opposed to using the radiographic data as the benchmark. Furthermore, the length of the basion-dens interval is greatly affected by ossification of the os terminale. When subdividing the study population into patients in whom the os terminale had already ossified and those in whom it had not, a 2-mm difference in the mean value was obtained. Attention to visualization of the os terminale is likely to affect the sensitivity of this method for detecting atlantooccipital dissociation.
The Powers ratio is limited to the detection of anterior atlantooccipital dissociation and requires the identification of the anterior arch of C1 and the spinolaminar line at the C1 level on the midsagittal image. In pediatric patients, the anterior arch of C1 may not yet have ossified or the posterior neural arches of C1 may not have fused in the midline, depending on the maturation level of these structures. In a young patient in whom these structures are not seen (15% of the patients in the study population), the Powers ratio cannot be performed. Because this value is a ratio, no significant difference was found when comparing our results based on MDCT images with the established normal values in the literature based on radiographs.
The atlantodental interval, also known as the predental space, is maintained by the presence of the atlantodental ligament, alar ligaments, and transverse atlantal ligament. Thus, an abnormally widened predental space is an indirect indicator of craniocervical junction ligamentous injury, and specifically, injury to the transverse atlantal ligament [28]. However, this space varies in flexion and extension [23]. The study population showed smaller values for the width of this space on MDCT images compared with the values accepted as normal for radiographs and similar to data published on MDCT in adults. Again, ossification of the anterior arch of C1 must be complete in the midsagittal plane to perform this measurement. In the study population, this method could not be performed in 6% of the group.
In 1987, Kaufman et al. [11] measured the atlantooccipital joint space in 100 normal children at five evenly spaced points on the cross-table lateral radiograph of the skull. This space was reported to be congruent throughout, and at no point should it measure more than 5 mm. Although examination of the joint space on MDCT images does show that it is congruent throughout, a wedge-shaped depression is often seen in the articular surface of the condyle at the midpoint on sagittal images, which has been previously described [29, 30]. This structure represents normal synchondrosis in the developing skull base and is termed “synchondrosis intraoccipitalis anterior,” which is usually no longer seen by the time the child is 10-12 years old [29, 30] (Fig. 6). It is important to note this structure and refrain from including this depression in measurements of the atlantooccipital interval because doing so would falsely increase the value obtained. In our experience, the synchondrosis intraoccipitalis anterior is seen in the medial aspects of the joint space and can often be avoided by selecting a more lateral image to perform measurements.
Fig. 6 —Synchondrosis intraoccipitalis anterior in 7-year-old girl. Wedge-shaped depression in articular surface of condyle at midpoint on sagittal image is normal synchondrosis in developing skull base, which is termed “synchondrosis intraoccipitalis anterior.”
Pang et al. [6] have also evaluated the atlantooccipital interval on CT images in 89 healthy patients between 6 months and 17 years old and obtained similar results with regard to normal values despite differences in methods of measurement and patient population. In addition, those authors have calculated the sensitivity of this method for detecting atlantooccipital dissociation injuries to be 100% based on a group of 16 patients [27].
Calculations of interexaminer and intraexaminer variability were not performed in this study, which is a limitation of the study. However, we have shown that, except for the basion-axial interval, these methods of assessing the craniocervical junction have low variability when performed repeatedly by the same examiner or by different examiners [24].
Ideally, the patient population would have included only healthy volunteers or children undergoing MDCT of the cervical spine for an indication other than trauma. Unfortunately, this is not practically feasible, and children have been included who sustained some form of trauma as an indication for evaluation of the cervical spine. Although this is a limitation of the study, we believe that the strict criteria for inclusion in our patient population markedly limit the possibility that a child with a true cervical spine abnormality was included. Although age-specific normal values would be useful, the broad range of normal ages at which various components of the cervical spine mature in children would probably make such a study practically unfeasible. Nonetheless, the lack of age-specific results limits our examination.
The accuracy of measurements could theoretically be limited by the fact that the data were collected using measurements to the nearest tenth of a millimeter, whereas the true in-plane resolution of the examinations performed is 0.3125 mm. The technical parameters of cervical spine trauma scanning protocols using MDCT are fairly standardized and result in similar in-plane resolution [24]. Furthermore, most radiologists obtain these measurements with workstations similar to the ones used in our study. Therefore, it is not likely that this discrepancy will alter the validity of the data.
Practically speaking, the landmarks used to perform the methods discussed herein are difficult to precisely localize on radiographs and are subject to inherent radiographic magnification. Furthermore, the Powers ratio and the basion-axial interval involve drawing multiple lines and, in the case of the Powers ratio, performing a calculation. An effective method of evaluating for atlantooccipital dissociation should be simple, accurate, easily reproducible, and able to be performed rapidly by the busy radiologist evaluating the traumatized child in the emergency department.
On MDCT MPR images, magnification is negligible, and direct visualization of the joint spaces can be performed. Specifically, on MPRs, direct evaluation of the atlantooccipital joint is possible. Therefore, the relationship between the occipital condyle and the lateral mass of the atlas becomes the single most important method for detecting atlantooccipital dissociation. Conceptually, any separation between the cranium and the cervical spine would be seen as an increase in this space. Other authors have also suggested that the relationship between the lateral masses of the atlas and axis is also important to assess when evaluating for craniocervical junction injuries. Widening of the joint space between the articular facets of C1 and C2 has been described in the setting of atlantooccipital dissociation [31, 32]; and the atlantoaxial interval should also be assessed when suspicion for atlantooccipital dissociation exists. There are no data in the literature of the pediatric population regarding the normal value for this space on MDCT; however, a review of the normal values on MDCT for the atlantoaxial interval in both adults and children is now under way.
In summary, defining the normal relationships of the craniocervical junction is of particular clinical importance in children because of their propensity for injuries in this region in the setting of trauma. However, normal values in children for the craniocervical junction articulations as seen on MDCT are different from the accepted ranges of normal based on radiographs. These differences are likely due to multiple factors, including magnification, lack of certainty in identifying osseous landmarks, and patient positioning. By establishing the normal relationships between the atlas, the axis, and the occiput, the sensitivity of MDCT for detecting ligamentous injuries and subtle bone injuries will likely be increased. We suggest that these new values be considered the normal ranges in children on MDCT.

Footnotes

Address correspondence to J. C. Bertozzi, 1513 S Georgia Ave., Tampa, FL 33629 ([email protected]).
CME This article is available for CME credit. See www.arrs.org for more information.
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This article is available for CME credit. See www.arrs.org for more information.

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Information & Authors

Information

Published In

American Journal of Roentgenology
Pages: 26 - 31
PubMed: 19098175

History

Submitted: April 11, 2008
Accepted: June 13, 2008

Keywords

  1. atlantooccipital dissociation
  2. atlantooccipital interval
  3. children
  4. craniocervical junction
  5. pediatric imaging

Authors

Affiliations

John Christopher Bertozzi
Department of Radiology, University of South Florida College of Medicine, 12901 Bruce B. Downs Blvd., MDC 17, Tampa, FL 33612.
Carlos Andres Rojas
Department of Radiology, University of South Florida College of Medicine, 12901 Bruce B. Downs Blvd., MDC 17, Tampa, FL 33612.
Carlos Rodrigo Martinez
Department of Radiology, University of South Florida College of Medicine, 12901 Bruce B. Downs Blvd., MDC 17, Tampa, FL 33612.

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