Morphometric changes at the craniocervical junction during childhood

Jayapalli Rajiv Bapuraj Departments of Radiology and

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Amy K. Bruzek Neurosurgery, University of Michigan, Ann Arbor, Michigan;

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Jamaal K. Tarpeh Neurosurgery, University of Michigan, Ann Arbor, Michigan;

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Lindsey Pelissier Neurosurgery, University of Michigan, Ann Arbor, Michigan;

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Hugh J. L. Garton Neurosurgery, University of Michigan, Ann Arbor, Michigan;

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Richard C. E. Anderson Department of Neurosurgery, Columbia University College of Physicians and Surgeons, New York, New York;

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Bin Nan Department of Statistics, University of California, Irvine, California; and

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Tianwen Ma Department of Biostatistics, University of Michigan, Ann Arbor, Michigan

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Cormac O. Maher Neurosurgery, University of Michigan, Ann Arbor, Michigan;

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OBJECTIVE

Current understanding of how the pediatric craniocervical junction develops remains incomplete. Measurements of anatomical relationships at the craniocervical junction can influence clinical and surgical decision-making. The purpose of this analysis was to quantitatively define clinically relevant craniocervical junction measurements in a population of children with CT scans that show normal anatomy.

METHODS

A total of 1458 eligible patients were identified from children between 1 and 18 years of age who underwent cervical spine CT scanning at a single institution. Patients were separated by both sex and age in years into 34 groups. Following this, patients within each group were randomly selected for inclusion until a target of 15 patients in each group had been reached. Each patient underwent measurement of the occipital condyle–C1 interval (CCI), pB–C2, atlantodental interval (ADI), basion-dens interval (BDI), basion-opisthion diameter (BOD), basion-axial interval (BAI), dens angulation, and canal diameter at C1. Mean values were calculated in each group. Each measurement was performed by two teams and compared for intraclass correlation coefficient (ICC).

RESULTS

The data showed that CCI, ADI, BDI, and dens angulation decrease in magnitude throughout childhood, while pB–C2, PADI, BAI, and BOD increase throughout childhood, with an ICC of fair to good (range 0.413–0.912). Notably, CCI decreases continuously on coronal CT scans, whereas on parasagittal CT scans, CCI does not decrease until after age 9, when it shows a continuous decline similar to measurements on coronal CT scans.

CONCLUSIONS

These morphometric analyses establish parameters for normal pediatric craniocervical spine growth for each year of life up to 18 years. The data should be considered when evaluating children for potential surgical intervention.

ABBREVIATIONS

ADI = atlantodental interval; AOD = atlantooccipital dislocation; BAI = basion-axial interval; BDI = basion-dens interval; BOD = basion-opisthion diameter; CCI = occipital condyle–C1 interval; CM1 = Chiari malformation type I; ICC = intraclass correlation coefficient; Oc = occiput; PADI = posterior ADI; SAC = space available for the cord.

OBJECTIVE

Current understanding of how the pediatric craniocervical junction develops remains incomplete. Measurements of anatomical relationships at the craniocervical junction can influence clinical and surgical decision-making. The purpose of this analysis was to quantitatively define clinically relevant craniocervical junction measurements in a population of children with CT scans that show normal anatomy.

METHODS

A total of 1458 eligible patients were identified from children between 1 and 18 years of age who underwent cervical spine CT scanning at a single institution. Patients were separated by both sex and age in years into 34 groups. Following this, patients within each group were randomly selected for inclusion until a target of 15 patients in each group had been reached. Each patient underwent measurement of the occipital condyle–C1 interval (CCI), pB–C2, atlantodental interval (ADI), basion-dens interval (BDI), basion-opisthion diameter (BOD), basion-axial interval (BAI), dens angulation, and canal diameter at C1. Mean values were calculated in each group. Each measurement was performed by two teams and compared for intraclass correlation coefficient (ICC).

RESULTS

The data showed that CCI, ADI, BDI, and dens angulation decrease in magnitude throughout childhood, while pB–C2, PADI, BAI, and BOD increase throughout childhood, with an ICC of fair to good (range 0.413–0.912). Notably, CCI decreases continuously on coronal CT scans, whereas on parasagittal CT scans, CCI does not decrease until after age 9, when it shows a continuous decline similar to measurements on coronal CT scans.

CONCLUSIONS

These morphometric analyses establish parameters for normal pediatric craniocervical spine growth for each year of life up to 18 years. The data should be considered when evaluating children for potential surgical intervention.

In Brief

The purpose of this analysis was to quantitatively define clinically relevant craniocervical junction measurements in a population of normal children. Measurements of anatomical relationships at the craniocervical junction can influence clinical and surgical decision-making. Age-adjusted normal data will be useful when attempting to identify pathological conditions. The data showed that CCI, ADI, BDI, and dens angulation decrease in magnitude throughout childhood, while pB-C2, PADI, BAI, and BOD increase throughout childhood.

Our understanding of craniocervical junction development in children remains incomplete. Surgeons are frequently asked to evaluate children for craniocervical junction abnormalities. In many cases, treatment decisions may be influenced by an understanding of expected normal growth for each age group.1,2,9,16 Grabb et al.7 demonstrated that pB–C2 (the Grabb-Oakes line) correlated with ventral brainstem compression in patients with Chiari malformation and that halo traction and/or surgical decompression and fusion may be necessary to relieve ventral brainstem compression. However, the age-specific normal values for pB–C2 remain unknown.

Several previous studies have reported on craniovertebral junction measurements in children, although each has its own limitations.12,17,24 Lee et al.12 included 238 children divided into three age groups (< 2 years, 3–5 years, and > 5 years of age) and made 8 measurements of the craniovertebral junction. Although they additionally divided the measurements into individual age groups, the oldest age was 7 years, and sex-specific measurements were not determined.12 Vachhrajani et al.24 evaluated a small series of 42 pediatric patients and measured the basion-dens interval (BDI), atlantodental interval (ADI), posterior ADI (PADI, or the space available for the cord), lateral mass interval, and occipital condyle–C1 interval (CCI) in an effort to describe normal measurements for the craniovertebral junction in the pediatric population. Piatt and Grissom17 reviewed 841 pediatric CT studies to outline the postnatal development of the ossification centers (paired neural arch, basal central, dentate center, and apical center) and synchondroses (posterior midline and neurocentral) at each year of age from birth to 20 years. Previously, development of the atlas and axis was qualitative, but the timing of developmental changes and variations of such were unknown.17 While the Piatt and Grissom17 study was important for understanding normal closure of sutures of the atlas and axis, normal anatomical measurements were not evaluated.

The purpose of this study is to present a more complete and numerically robust understanding of the distribution of normal craniovertebral junction measurements in children at different stages of development in order to more accurately distinguish between normal and pathological findings on imaging studies and to facilitate treatment decision-making.

Methods

Study Population

This study was approved by the University of Michigan Institutional Review Board. Patients selected for this cross-sectional study were between 1 and 18 years of age at time of the scan. Each child underwent noncontrast CT scanning of the cervical spine at C.S. Mott Children’s Hospital. All included patients had imaging that included sagittal and coronal reformatted images reconstructed in 2-mm intervals, and the lower skull and upper cervical spine from at least the foramen magnum to the inferior endplate of C2. CT scans were read by pediatric radiologists. Only those patients classified as having a normal CT scan were included: no evidence of skull trauma, congenital anomaly of the skull, prior cranial surgery, congenital spine abnormality, prior spine surgery, or traumatic spine injury. Patients with inadequate imaging resolution or lacking visualization of the craniocervical junction were excluded.

A total of 1458 eligible patients were identified for potential inclusion. Patients were separated by both sex and age in years into 34 groups. We then used quota sampling as a form of nonprobability sampling to ensure equal representation of subjects per age group. To obtain this nonprobability sampling, the age groups were divided into 1-year intervals from ages 1 to 18. Patients within each age group were assigned a random number and then selected for inclusion until 15 patients in the group had been measured. Those who met the exclusion criteria were not measured. The largest group was 16-year-old males (107 patients) and the smallest group was 6-year-old females (15 patients). Due to the exclusion criteria, certain age and sex groups did not include 15 measured patients: 7-year-old females (14 patients), 6-year-old females (12 patients), 5-year-old females (12 patients), 4-year-old females (13 patients), and 2-year-old females (12 patients). Patient demographics, including race and ethnicity, are shown in Table 1. All inclusion criteria were met by the 498 patients studied.

TABLE 1.

Patient demographics

DemographicsNo. of PatientsPercentage of Total
Sex
 Male25551.2
 Female24348.8
Race
 Caucasian37374.9
 African American6312.7
 Other255.0
 Unknown193.8
 Asian183.6
Ethnicity
 Non-Hispanic32164.5
 Unknown16232.5
 Hispanic153.0

Measurements

Two teams of observers independently made the measurements. Both teams consisted of a board-certified faculty member in either neuroradiology (J.R.B.) or neurosurgery (C.O.M.) and one senior medical student (L.P., J.K.T.). Linear measurements were performed using the measurement program in the ImageCast radiology information system and picture archiving and communications system (better known as PACS) (IDX Systems Corp.). The resolution of the measurement program was 0.1 mm. The pB–C2 was measured according to the technique first described by Grabb et al.7 A line was drawn from the basion to the inferoposterior aspect of the C2 body. A second line was drawn perpendicularly from this line to the ventral dura, the measurement of which was considered the value for pB–C2. The ADI measurement extended from the posterior aspect of the anterior ring of C1 to the anterior aspect of the dens. The BDI was determined by measuring the shortest distance from the basion to the tip of the dens. For the basion-axial interval (BAI), a straight line was drawn along the posterior dens and extended through the foramen magnum past the basion. The BAI was then determined by measuring the shortest distance between that line and the basion in the sagittal plane. The basion-opisthion diameter (BOD) (McRae line) was determined by measuring the shortest distance between the basion and the opisthion. The dens angulation was determined by drawing a line along the base of C2 and a second line through C2 to the apex of the odontoid process and then calculating the posterior angle between the lines. The space available for the cord (SAC) or the canal diameter at the C1 level (PADI) was determined by drawing a line from the posterior aspect of the dens to the anterior aspect of the posterior arch of C1. The pB–C2, ADI, BDI, BOD, BAI, dens angulation, and PADI measurements were made on the midsagittal CT image of the cervical spine. The occipital CCI (occiput [Oc]–C1 joint or atlantooccipital joint) measurements were made on parasagittal and coronal slices through bilateral joints. On parasagittal slices through the atlantooccipital joint, the CCI was measured by drawing 4 perpendicular lines from the midpoint of the inferior aspect of the occipital condyle to the midpoint of the superior aspect of the articular surface of the lateral mass at C1 and averaging those 4 measurements (Fig. 1A and B).19 This measurement was similarly made on coronal CT scans (Fig. 1C).

FIG. 1.
FIG. 1.

CCI measurements made on bone window CT scans, showing 4 lines made perpendicular to the endplates of the occipital condyle and C1 lateral mass. These 4 lines were averaged for each joint. Right parasagittal Oc–C1 junction (A), left parasagittal Oc–C1 junction (B), and coronal view of the Oc–C1 junction (C).

Statistical Analysis

Means (± SD) were calculated for each of the measurements in each of the 34 groups. Intraclass correlation coefficients (ICCs) between the two measurement teams were calculated for each measurement.5,22 As described by Cicchetti,5 we considered an ICC of less than 0.40 to reflect a poor correlation; an ICC between 0.40 and 0.59 was considered fair; an ICC between 0.60 and 0.74 was considered good; and an ICC between 0.75 and 1.00 was considered excellent.

Results

Study Population

The patients included in this study had diverse indications for a cervical spine CT scan. A minor fall was reported by 139 patients (27.9%); 135 patients (27.1%) were involved in a motor vehicle collision; 120 patients (24.1%) were involved in accidental or unexplained trauma; 79 patients (15.9%) suffered a sports injury; 8 patients (1.6%) reported a near-drowning event; 6 patients (1.2%) presented with neck pain without a history of trauma; 4 patients (0.8%) presented following a seizure; 3 patients (0.6%) were evaluated following a suicide attempt; 3 patients (0.6%) presented with unexplained altered mental status; and 1 patient (0.2%) presented with a soft-tissue mass in the neck but not within the spine.

Among patients initially selected by randomization, 239 were subsequently excluded. Of these, 131 patients (54.8%) were excluded due to a condition affecting the cervical spine. Of the 34 different conditions that were noted, the most common were scoliosis, congenital cervical fusion, and torticollis. Other exclusions included 14 patients (5.9%) with a finding of an acute cervical spine fracture; 6 patients (2.5%) with an acute cervical subluxation; 9 patients (3.8%) with a history of cervical fracture or subluxation; 34 patients (14.2%) with poor sagittal alignment on CT scanning, precluding accurate measurements; 18 patients (7.5%) with significant motion artifact on the scan that limited our ability to make accurate measurements; 13 patients (5.4%) whose cervical spine CT scan did not include the entire cervical spine from the basion to C7; and 14 patients (5.9%) who lacked a complete set of images, including sagittal reconstruction in the image archive.

Morphometric Analysis

The pB–C2 (Grabb-Oakes line)

Using bony CT scan for measurement of pB–C2, we found that the pB–C2 line increases steadily until the age of 4 or 5 years in both boys and girls, then levels off to remain stable until age 18. In boys, the mean measurement was 3.8 mm (± 0.66 mm) between 1 and 2 years of age, with peaks of 6.71 mm (± 1.06 mm) and 6.62 mm (± 1.45 mm) at ages 10–11 and 17–18, respectively. In girls, the pB–C2 line was the smallest at 1–2 years of age at 3.13 mm (± 0.61), but it leveled out around 4–5 years of age, with a mean measurement of 5.41 mm (± 1.37 mm) by ages 17–18. The difference in pB–C2 distance was not statistically significant between boys and girls at any time point (Table 2, Fig. 2A).

TABLE 2.

Means and standard deviations of morphometric measurements of the craniocervical junction in males and females, stratified by age group

Sex & Age GrouppB–C2 in mm (SD)ADI in mm (SD)PADI in mm (SD)BDI in mm (SD)BAI in mm (SD)BOD in mm (SD)Dens Angulation in mm (SD)Oc–C1 (para; lt) in mm (SD)Oc–C1 (para; rt) in mm (SD)Oc–C1 (cor; lt) in mm (SD)Oc–C1 (cor; rt) in mm (SD)
Males
 Age (yrs)
  1–23.80 (0.66)2.43 (0.54)16.61 (1.74)8.48 (1.78)4.04 (0.87)32.07 (3.70)81.27 (4.21)2.73 (0.40)2.78 (0.46)3.15 (0.50)3.27 (0.48)
  2–34.04 (0.96)2.04 (0.52)18.44 (1.20)8.14 (0.82)3.76 (1.92)32.49 (2.99)79.34 (3.93)3.06 (0.65)2.93 (0.69)2.64 (0.68)2.70 (0.67)
  3–44.41 (0.95)2.38 (0.79)18.20 (1.70)8.19 (1.75)4.53 (1.69)34.20 (2.99)79.01 (4.47)2.99 (0.75)3.07 (0.79)2.73 (0.72)2.78 (0.75)
  4–55.26 (1.29)2.33 (0.55)19.34 (1.60)7.59 (1.47)6.26 (2.27)35.12 (2.79)77.09 (3.87)3.43 (0.91)3.40 (0.75)2.93 (0.65)2.79 (0.48)
  5–65.17 (1.11)2.46 (0.46)20.44 (2.33)7.81 (1.29)5.64 (1.90)36.84 (3.85)76.72 (3.63)3.18 (0.56)3.35 (0.72)2.66 (0.75)2.80 (0.69)
  6–75.56 (1.03)2.39 (0.81)19.19 (1.71)7.11 (1.50)6.45 (1.77)35.32 (2.86)78.70 (2.56)3.36 (0.80)3.42 (0.73)2.68 (0.60)2.87 (0.77)
  7–85.69 (0.96)2.48 (0.84)19.76 (1.95)7.02 (1.71)6.54 (1.54)36.14 (2.48)74.33 (3.46)3.48 (1.26)3.54 (1.04)2.70 (0.46)2.75 (0.68)
  8–95.63 (1.30)2.59 (0.57)19.92 (1.67)6.94 (1.59)7.02 (2.20)36.49 (2.99)73.18 (3.92)3.10 (1.07)3.26 (0.92)2.54 (0.59)2.38 (0.42)
  9–105.77 (1.41)2.55 (0.56)18.96 (2.09)7.20 (1.98)6.95 (2.46)36.90 (3.24)72.71 (4.21)4.05 (1.21)3.61 (1.14)3.10 (0.82)3.22 (1.10)
  10–116.71 (1.06)2.36 (0.39)19.08 (1.77)5.70 (1.31)8.02 (1.40)36.28 (1.86)73.49 (3.34)2.70 (0.68)2.91 (0.88)2.35 (0.55)2.29 (0.46)
  11–125.06 (0.99)2.27 (0.29)20.90 (3.04)5.98 (1.02)7.66 (1.98)39.01 (3.00)75.18 (3.33)2.60 (1.02)2.39 (0.77)2.22 (0.67)2.23 (0.72)
  12–135.54 (1.45)2.26 (0.47)19.77 (2.20)5.61 (0.91)7.85 (2.09)36.38 (3.58)74.00 (3.18)2.50 (0.76)2.51 (0.92)2.33 (0.74)2.27 (0.61)
  13–145.70 (1.47)2.24 (0.33)21.02 (2.71)5.51 (1.08)8.42 (2.38)37.85 (2.59)72.79 (4.81)1.94 (0.63)2.14 (0.98)1.83 (0.46)1.86 (0.53)
  14–155.30 (1.49)2.25 (0.50)20.91 (2.44)5.33 (1.25)8.25 (2.05)37.90 (3.53)72.56 (2.91)2.38 (0.89)2.23 (0.92)1.92 (0.50)1.97 (0.61)
  15–164.98 (1.36)1.81 (0.30)18.80 (1.45)5.27 (1.41)8.04 (1.88)36.40 (1.76)72.62 (3.23)1.81 (0.64)1.90 (1.14)1.73 (0.49)1.70 (0.49)
  16–175.54 (0.88)1.75 (0.33)20.27 (1.53)5.22 (1.52)8.76 (1.25)38.00 (1.83)68.88 (2.52)1.77 (0.36)1.88 (0.45)1.60 (0.30)1.62 (0.29)
  17–186.62 (1.45)1.52 (0.27)21.50 (2.27)5.06 (1.49)8.06 (2.62)38.22 (2.56)71.85 (8.69)1.47 (0.30)1.40 (0.23)1.38 (0.30)1.36 (0.29)
Females
 Age (yrs)
  1–23.13 (0.61)1.84 (0.53)16.12 (1.66)8.82 (1.39)2.42 (1.45)29.71 (2.41)81.81 (2.72)2.72 (0.44)2.68 (0.55)2.73 (0.58)2.88 (0.53)
  2–33.75 (0.75)1.75 (0.46)17.21 (1.33)7.89 (1.15)3.86 (1.87)31.75 (2.02)78.83 (2.77)2.79 (0.61)3.04 (0.70)2.73 (0.80)2.8 (0.64)
  3–44.42 (1.06)2.10 (0.51)17.75 (1.81)7.59 (2.01)4.96 (1.55)32.98 (3.79)79.21 (3.15)2.74 (0.57)2.79 (0.59)2.43 (0.49)2.62 (0.68)
  4–55.10 (1.32)2.21 (0.76)19.09 (1.73)6.93 (1.61)6.24 (1.92)34.60 (2.83)77.36 (5.52)3.12 (0.82)2.94 (0.73)2.78 (0.88)2.63 (0.73)
  5–65.32 (0.97)2.40 (0.78)18.80 (2.26)6.18 (1.72)6.13 (1.51)34.45 (1.93)75.73 (3.36)2.94 (0.93)3.03 (0.43)2.34 (0.45)2.44 (0.53)
  6–75.24 (1.48)2.18 (0.42)17.43 (0.98)6.34 (1.35)6.50 (2.14)32.52 (2.91)73.92 (2.96)3.54 (0.66)3.25 (0.79)2.52 (0.34)2.75 (0.60)
  7–85.97 (1.31)2.28 (0.31)18.99 (1.98)6.12 (1.58)6.91 (1.74)35.19 (2.75)75.76 (5.59)3.47 (0.88)3.39 (1.14)2.64 (0.72)2.23 (0.37)
  8–95.96 (0.95)2.18 (0.58)17.87 (1.71)6.03 (1.32)7.53 (1.12)34.38 (2.14)73.18 (3.93)3.23 (1.09)3.57 (1.10)2.67 (0.63)2.53 (0.60)
  9–105.52 (1.49)1.97 (0.43)18.11 (2.65)6.43 (1.20)6.58 (2.26)34.28 (2.44)74.10 (3.54)2.60 (0.99)2.46 (0.95)2.31 (0.83)2.15 (0.83)
  10–115.88 (1.30)1.83 (0.45)17.82 (2.21)5.24 (1.45)7.18 (1.20)34.51 (2.74)74.14 (3.86)1.86 (0.74)1.99 (0.86)1.72 (0.46)1.71 (0.59)
  11–125.30 (1.35)2.09 (0.46)19.13 (1.43)5.60 (1.51)7.58 (1.92)36.36 (2.01)74.34 (5.62)2.40 (1.08)2.23 (0.93)2.02 (0.83)1.92 (1.03)
  12–135.65 (1.20)1.91 (0.41)18.78 (1.76)4.51 (1.19)8.01 (1.66)35.05 (2.05)71.50 (4.22)1.43 (0.62)1.52 (0.65)1.43 (0.51)1.38 (0.54)
  13–144.96 (1.64)1.58 (0.35)18.71 (2.25)4.98 (1.52)7.86 (2.11)34.79 (2.58)71.87 (5.56)1.30 (0.19)1.39 (0.28)1.23 (0.16)1.22 (0.18)
  14–155.17 (1.38)1.67 (0.30)18.89 (2.56)5.10 (1.96)8.12 (2.09)36.19 (2.15)69.36 (2.99)1.69 (0.59)1.54 (0.50)1.37 (0.32)1.29 (0.22)
  15–164.78 (0.97)1.56 (0.20)19.23 (1.72)4.99 (0.84)7.62 (1.06)34.99 (2.31)68.97 (4.35)1.42 (0.49)1.27 (0.16)1.31 (0.16)1.31 (0.17)
  16–175.29 (0.82)1.46 (0.32)19.52 (1.41)5.16 (1.17)7.77 (1.50)35.53 (2.33)69.79 (3.35)1.48 (0.22)1.51 (0.21)1.65 (0.39)1.62 (0.36)
  17–185.41 (1.37)1.30 (0.25)18.44 (1.36)5.06 (1.56)7.00 (2.06)34.20 (2.58)69.28 (3.90)1.23 (0.34)1.24 (0.33)1.21 (0.22)1.24 (0.24)

cor = coronal; para = parasagittal.

FIG. 2.
FIG. 2.

Mean morphometric measurements with standard deviations by age for female (dotted line) and male (solid line) patients. The pB-C2 (A), ADI (B), PADI (canal diameter at C1) (C), BDI (D), BAI (E), (F) BOD (F), dens angulation (G), Oc–C1 measured on parasagittal CT scans (H), and Oc–C1 measured on coronal CT scans (I).

ADI

Unlike pB–C2, the ADI decreased throughout childhood, from a mean of 2.43 mm (± 0.54 mm) to a mean of 1.52 mm (± 0.27 mm) for boys and from a mean of 1.84 mm (± 0.53 mm) to a mean of 1.3 mm (± 0.25 mm) for girls. Girls had an increase in ADI between the ages of 2 and 5 years, with a peak value of 2.40 mm (± 0.78 mm) before slowly declining. In boys, the ADI stayed approximately stable throughout childhood before making a significant decline after the age of 14 years (Table 2, Fig. 2B).

PADI and SAC (canal diameter at the C1 level)

The canal diameter at the C1 level (PADI or SAC) had a mild increase throughout childhood in both males and females. In males, PADI started at 16.61 mm (± 1.74 mm) between 1 and 2 years, rose steadily to the age of 5, and then stayed about steady except for a decline at age 14 years (21.02 mm, ± 2.71 mm), with a final mean of 21.50 mm (± 2.27 mm). Female patients had a mean of 16.12 mm (± 1.66 mm) between 1 and 2 years and a final mean of 18.44 mm (± 1.36 mm) between ages 17 and 18 (Table 2, Fig. 2C).

BDI

The BDI decreased steadily throughout childhood in both males and females. Males had a mean BDI of 8.48 mm (± 1.78 mm) around the 1st year of life, which decreased to a mean of 5.06 mm (± 1.49) by age 18. In females, the mean BDI was 8.82 mm (± 1.39), and it declined to 5.06 mm (± 1.56 mm) by age 18 (Table 2, Fig. 2D).

BAI

The BAI increased overall from age 1 to 18 years, with the most significant increase during the first 4 years and only a slight rise after that. Males started at a mean 4.04 mm (± 0.87 mm) and had a mean of 8.06 mm (± 2.62 mm) by age 18. There were small, insignificant decreases and increases throughout childhood. In females, the mean BAI was 2.42 mm (± 1.45 mm) in the youngest age group, 1–2 years, and 7.00 mm (± 2.06 mm) by 18 years of age (Table 2, Fig. 2E).

BOD

Overall, in males the BOD, also known as the McRae line, stays approximately stable after an increase in the first 5 years of life. The mean BOD in males was 32.07 mm (± 3.70 mm) at about 1 year of age, increased to 35.12 mm (± 2.79 mm) by age 5, and then slowly increased overall to 38.22 mm (± 2.56 mm) by age 18. Females had a similar steady increase to the age of 4, then a sharp decline by the age of 6 (although not below the starting mean), and overall a return to a steady state with the exception of a sudden and nonsustained increase around age 11. The mean BOD in females was 29.71 mm (± 2.41 mm) at age 1 year, with a steady rise to 34.6 mm (± 2.83 mm) between ages 4 and 5, and a mean of 34.2 mm (± 2.58 mm) by age 18 (Table 2, Fig. 2F).

Dens Angulation

The dens angulation was approximately equal between males and females, with a steady decline for both throughout childhood. At age 1 year, males had a mean dens angulation of 81.27° (± 4.21°), and females had a mean dens angulation of 81.81° (± 2.72°). By 18 years of age, males had a mean dens angulation of 71.85° (± 8.69°), and females had a mean of 69.28° (± 3.90°) (Table 2, Fig. 2G).

CCI

The Oc–C1 joint space decreases during childhood. The pattern of decrease differed according to the image that was used (coronal or parasagittal). The CCI decreases continuously throughout childhood when measured on coronal CT scans (Table 2, Fig. 2H and I). Specifically, in males on coronal CT scans, the measurement started off at just over 3 mm and ended at just over 1 mm by age 18. In females, the joint space started off at just under 3 mm and was slightly over 1 mm by age 18. When measured on parasagittal CT images, the CCI did not decrease before age 9 years, after which it showed a continuous decline similar to that seen on coronal CT scans.

Interrater Correlation

No measurements had poor correlation between raters. The pB–C2 (0.413) and sagittal Oc–C1 (left 0.509 and right 0.563) had only fair ICC.5,22 Coronal measurements of the Oc–C1 joint spaces (left 0.618 and right 0.610), dens angulation (0.633), and ADI (0.702) had good correlation. PADI (0.882), BDI (0.841), BAI (0.912), and BOD (0.793) had ICCs in the excellent range.

Discussion

Most of the age-related differences in this study have not been previously reported, with some notable exceptions. Ravindra et al.18 studied age-related changes in CCI in a large cohort of individuals without atlantooccipital dislocation (AOD). Lee et al.12 reported on age-related changes in 238 patients divided into 3 pediatric age groups (< 2 years, 2–5 years, and > 5 years). That analysis focused on measurements of the axis and atlas within these age groups but did also examine pB–C2, BOD, and BDI differences. Similar to the previous report of Lee et al.,12 we found a significant increase in spinal canal diameter in children less than 5 years of age. Vachhrajani et al.24 found upper limits of normal of 2.76 mm for ADI, 7.49 mm for BDI, and 3.24 mm for CCI, with an average of 1.28 mm for all children. Our upper limit findings, similar to those of Vachhrajani et al., were 2.59 mm (± 0.57 mm) for ADI, 8.82 mm (± 1.39 mm) for BDI, and 3.27 mm (± 0.48 mm) for CCI. Like Vachhrajani et al.,24 our values were much different than accepted adult values, emphasizing the need for pediatric-specific studies such as ours.

BOD

Previous reports of BOD in adults have found a mean between 35 and 36 mm.4,25 In contrast, Tubbs et al.23 calculated a mean BOD of 31 mm in a cadaveric study of 72 dry skulls of older adults. Schmeltzler et al.21 measured the BOD on radiographs acquired in children and adults and reported data very similar to the present study, finding that BOD increased throughout childhood, especially during the first 5 years. Lee et al.12 demonstrated enlargement of the BOD when comparing infants to older children. Our data confirmed an increase in the BOD in early childhood and indicated that this size increase slows but continues with advancing age during childhood (Fig. 2F).

BDI

Lee et al.12 found a slight decrease in BDI when comparing measurements in young children according to 3 age groups. We confirmed this finding and showed that this decrease continues at a slower rate throughout childhood (Fig. 2D). As stated, our results were similar to those of Vachhrajani et al.24 in that the upper limit of normal was less than 9 mm in our study and less than 8 mm in the study of Vachhrajani et al. Piatt and Grissom17 have outlined normal ossification of the atlas and axis and variations of each. They showed that in the atlas, while ossification of the neural arches begins in the prenatal period, ossification of the anterior arch begins postnatally between 1 and 22 months of age.17 The median age at the start of ossification of both synchondroses of the atlas was 5.2 years, the median age at complete ossification was 8.5 years, and all patients had complete ossification by about 7 years of age.17 Asymmetrical ossification of the neurocentral synchondroses of the atlas occurred in about 7% of patients.17 In the axis, the median age at initial ossification of the neurocentral synchondrosis was 3.8 years, with the latest occurring prior to 6 years of age. The posterior midline synchondrosis of the axis is closed by age 3 years. Unlike the atlas, it was uncommon (0.4%) to have anomalous ossification centers in the axis.17 Piatt and Grissom17 focused on the ossification of the atlas and the axis rather than describing morphometric measurements. However, relevant to this analysis, they observed that the median age at ossification of the apical ossification center of the dens was 2.7 years (IQR 1.9–3.6). Because we measured bony distance to the dens for BDI, the ossification of the apical dens would have an impact on this measurement. Specifically, at least some of the reduction in BDI that we observed may have been due to this ossification. This could account for the relatively rapid decline in BDI between ages 8 and 10 (Fig. 2D). Vachhrajani et al.24 made a similar observation. However, we would draw the distinction that given that apical ossification has largely concluded by age 8 and we continued to observe a reduction in BDI throughout childhood, joint-space narrowing of the Oc–C1 joint, in addition to ossification of the dens, is involved.

pB–C2

The pB–C2 line has been used as a determinant of the degree of ventral compression in patients with Chiari malformation type I (CM1) and associated conditions. In their initial description of this measurement, Grabb and colleagues7 found that no patients with a pB–C2 less than 9 mm in their cohort of 40 CM patients required ventral decompression or fusion. The utility of the pB–C2 measurement in the evaluation of CM patients has been noted by several groups, but some disagreement remains regarding the determination of abnormality of this measurement.2,3,11,20 We found that in males, the largest pB–C2 distance was a mean of 6.71 mm (± 1.06 mm) in the 10- to 11-year-old age group, and in females the upper limit for pB–C2 was a mean of 5.97 mm (± 1.31 mm) in the 7- to 8-year-old age group. Although we used bony CT images to measure pB–C2, whereas Grabb et al.7 used MRI, our findings are similar to those of a recent prior study that measured pB–C2 in a cohort of male and female patients with CM1:10 At a mean age of nearly 8 years, pB–C2 was 5.9 mm for symptomatic CM1 patients and 7.0 mm for asymptomatic patients, which was not statistically significant. These normal values should be considered when determining the relevance of pB–C2 values for the treatment of patients with Chiari malformations.

CCI

CT-based CCI measurements have been used to diagnose AOD since the seminal work of Pang et al.14,15 Although these initial analyses of the CCI in children were not able to identify trends in CCI with advancing age in childhood, Martinez-Del-Campo et al.13 found that their adult CCI measurements were less than those of children in previous reports.14,15 Ravindra et al.18 performed a detailed analysis of 578 patients without AOD and found a decreasing trend line for CCI in these subjects throughout childhood, a finding confirmed by our data (Fig. 2H and I). Of interest, in our assessment, we reported the average of 4 measurements across the joints in both coronal and sagittal planes, while Ravindra et al.18 used the maximum of 3 measurements in coronal and sagittal planes to determine their clinical decision rule.

These changes with advancing age should be considered in a diagnosis of AOD. Pang et al.14,15 proposed that CCI greater than 4 mm may indicate AOD. Based on adult data, some have proposed that AOD should be considered if the CCI is greater than 2.5 mm.6 We agree with Ravindra et al.18 that higher thresholds could be considered for younger patients. Furthermore, given the changes in CCI that are noted throughout childhood, especially on coronal imaging, we believe that the diagnosis of AOD should take these age-specific normal measurements into account, especially when evaluating young children for possible AOD.

ICCs

When evaluating measurements made by humans, error can affect statistical significance and subsequent reliability of the measurements.22 A commonly used method of determining reliability of measurements made by humans is to calculate the ICC.5,22 We calculated ICC, and used excellent, good, fair, and poor to describe the quality of the ICC based on numerical ICC values.5,22 In general, correlations for all measurements were good, except for a fair ICC for pB–C2. Hankinson et al.8 have previously demonstrated good ICC for pB–C2 measurements. In using our measurements to consider whether or not the values can be generalized, one should consider the fair ICC and use the trend of pB–C2 more than exact values. The simpler measurements had the better ICC values, which intuitively makes sense because the likelihood of encountering error and lack of correlation between observers is less when there are fewer measurements. Vachhrajani et al.24 reported poor agreement for ADI (0.457) but otherwise similar values for PADI, BDI, and CCI.

Limitations

Our data were derived from patients undergoing CT scanning at a referral center. Although we attempted to exclude patients with known spinal abnormalities, the included patients may not be representative of healthy volunteers. However, given the risk of radiation exposure with CT scans and radiographs, and the need for sedation in young children undergoing MRI, it is unlikely that any study of normal pediatric volunteers will ever be completed. The analysis of growth was determined by comparing different patients at different ages, rather than the same patients followed longitudinally. The study was performed in the Midwestern United States, and our population is likely more homogeneous than that of other geographic regions; therefore, it is difficult to make a generalized statement, as there are no data on the differences between varying racial or ethnic groups. Caucasian and non-Hispanic were the majority race and ethnicity, respectively. Additionally, with 30 patients per age group, comparison to the general population is limited. With regard to random sampling, because the population as a whole cannot be studied, one relies on sampling methods. True random sampling is difficult to achieve. To obtain a set number of patients per group, we employed quota sampling to generate our groups. Because of this method, generalization is difficult, as an unknown proportion was not sampled and measured.

Another limitation of the study is the inability to directly compare our measurements with other studies. In particular, Grabb et al.7 used MRI to measure pB–C2, while we used CT. The numerical values, therefore, could understandably differ, and overall trends rather than exact values should be used when comparing our study to others that used MRI. We used bony CT rather than MRI because patients who have experienced trauma usually first or only undergo CT scanning rather than MRI. Importantly, any morphometric study based on imaging must acknowledge the possibility of measurement errors. In this study, measurements were performed by two groups, and in general all measurements had a good ICC except for pB–C2, which had a fair ICC. Hankinson et al. have previously demonstrated a good ICC for pB–C2 measurements.8 Finally, differences in ossification in young children, especially of the dens, may contribute to measurement error.

Future Directions

Our study performed multiple measurements, not all of which are routinely made in patients with suspected traumatic injuries. As such, a study that focuses on clinically relevant measurements, such as atlantoaxial interval, would be extremely useful for patients who are being evaluated for trauma.

The CT scans in the present study were static rather than dynamic images, which allows for variability in measurements when one considers that, in young children in particular, many tissues (muscles, intervertebral discs, ligaments, etc.) are not fixed. A study that may attempt to correct for the variability would include dynamic images such as flexion-extension plain radiographs that may help to adjust or average the measurements.

Conclusions

Our study provides a comprehensive description of normal measurements for the pediatric population by both age and sex, with a large number of pediatric patients. Overall, CCI, ADI, and BDI decrease in size throughout childhood, while pB–C2, PADI, BAI, and BOD increase. Furthermore, the dens becomes more retroflexed with increasing age. These age-specific normal measurements may be helpful in clinical decision-making.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Maher, Bapuraj, Anderson. Acquisition of data: Maher, Bapuraj, Tarpeh, Pelissier. Analysis and interpretation of data: Maher, Bapuraj, Bruzek, Tarpeh, Pelissier. Drafting the article: Maher, Bapuraj, Bruzek, Garton, Anderson. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Maher. Statistical analysis: Nan, Ma. Administrative/technical/material support: Maher, Bapuraj. Study supervision: Maher, Bapuraj.

References

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    Bollo RJ, Riva-Cambrin J, Brockmeyer MM, Brockmeyer DL: Complex Chiari malformations in children: an analysis of preoperative risk factors for occipitocervical fusion. J Neurosurg Pediatr 10:134141, 2012

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    Bonney PA, Maurer AJ, Cheema AA, Duong Q, Glenn CA, Safavi-Abbasi S, et al.: Clinical significance of changes in pB-C2 distance in patients with Chiari Type I malformations following posterior fossa decompression: a single-institution experience. J Neurosurg Pediatr 17:336342, 2016

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    Catalina-Herrera CJ: Study of the anatomic metric values of the foramen magnum and its relation to sex. Acta Anat (Basel) 130:344347, 1987

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    Cicchetti DV: Guidelines, criteria, and rules of thumb for evaluating normed and standardized assessment instruments in psychology. Psychol Assess 6:284290, 1994

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    Gire JD, Roberto RF, Bobinski M, Klineberg EO, Durbin-Johnson B: The utility and accuracy of computed tomography in the diagnosis of occipitocervical dissociation. Spine J 13:510519, 2013

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    Grabb PA, Mapstone TB, Oakes WJ: Ventral brain stem compression in pediatric and young adult patients with Chiari I malformations. Neurosurgery 44:520528, 1999

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    Hankinson TC, Tuite GF, Moscoso DI, Robinson LC, Torner JC, Limbrick DD Jr, et al.: Analysis and interrater reliability of pB-C2 using MRI and CT: data from the Park-Reeves Syringomyelia Research Consortium on behalf of the Pediatric Craniocervical Society. J Neurosurg Pediatr 20:170175, 2017

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    Kennedy BC, D’Amico RS, Youngerman BE, McDowell MM, Hooten KG, Couture D, et al.: Long-term growth and alignment after occipitocervical and atlantoaxial fusion with rigid internal fixation in young children. J Neurosurg Pediatr 17:94102, 2016

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    Khalsa SSS, Geh N, Martin BA, Allen PA, Strahle J, Loth F, et al.: Morphometric and volumetric comparison of 102 children with symptomatic and asymptomatic Chiari malformation Type I. J Neurosurg Pediatr 21:6571, 2018

    • Crossref
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    Ladner TR, Dewan MC, Day MA, Shannon CN, Tomycz L, Tulipan N, et al.: Evaluating the relationship of the pB-C2 line to clinical outcomes in a 15-year single-center cohort of pediatric Chiari I malformation. J Neurosurg Pediatr 15:178188, 2015

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    Lee HJ, Kim JT, Shin MH, Choi DY, Hong JT: Quantification of pediatric cervical spine growth at the cranio-vertebral junction. J Korean Neurosurg Soc 57:276282, 2015

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    Martinez-Del-Campo E, Kalb S, Soriano-Baron H, Turner JD, Neal MT, Uschold T, et al.: Computed tomography parameters for atlantooccipital dislocation in adult patients: the occipital condyle-C1 interval. J Neurosurg Spine 24:535545, 2016

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    Pang D, Nemzek WR, Zovickian J: Atlanto-occipital dislocation: part 1—normal occipital condyle–C1 interval in 89 children. Neurosurgery 61:514521, 2007

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    Pang D, Nemzek WR, Zovickian J: Atlanto-occipital dislocation—part 2: The clinical use of (occipital) condyle–C1 interval, comparison with other diagnostic methods, and the manifestation, management, and outcome of atlanto-occipital dislocation in children. Neurosurgery 61:9951015, 2007

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    Phuntsok R, Mazur MD, Ellis BJ, Ravindra VM, Brockmeyer DL: Development and initial evaluation of a finite element model of the pediatric craniocervical junction. J Neurosurg Pediatr 17:497503, 2016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Piatt JH Jr, Grissom LE: Developmental anatomy of the atlas and axis in childhood by computed tomography. J Neurosurg Pediatr 8:235243, 2011

  • 18

    Ravindra VM, Riva-Cambrin J, Horn KP, Ginos J, Brockmeyer R, Guan J, et al.: A 2D threshold of the condylar-C1 interval to maximize identification of patients at high risk for atlantooccipital dislocation using computed tomography. J Neurosurg Pediatr 19:458463, 2017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Riascos R, Bonfante E, Cotes C, Guirguis M, Hakimelahi R, West C: Imaging of atlanto-occipital and atlantoaxial traumatic injuries: What the radiologist needs to know. Radiographics 35:21212134, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Ridder T, Anderson RCE, Hankinson TC: Ventral decompression in Chiari malformation, basilar invagination, and related disorders. Neurosurg Clin N Am 26:571578, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Schmeltzler A, Babin E, Wenger JJ: Measurement of the foramen magnum in children and adults. Neuroradiology 2:162163, 1971

  • 22

    Shrout PE, Fleiss JL: Intraclass correlations: uses in assessing rater reliability. Psychol Bull 86:420428, 1979

  • 23

    Tubbs RS, Griessenauer CJ, Loukas M, Shoja MM, Cohen-Gadol AA: Morphometric analysis of the foramen magnum: an anatomic study. Neurosurgery 66:385388, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Vachhrajani S, Sen AN, Satyan K, Kulkarni AV, Birchansky SB, Jea A: Estimation of normal computed tomography measurements for the upper cervical spine in the pediatric age group. J Neurosurg Pediatr 14:425433, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Wanebo JE, Chicoine MR: Quantitative analysis of the transcondylar approach to the foramen magnum. Neurosurgery 49:934943, 2001

  • Collapse
  • Expand
  • CCI measurements made on bone window CT scans, showing 4 lines made perpendicular to the endplates of the occipital condyle and C1 lateral mass. These 4 lines were averaged for each joint. Right parasagittal Oc–C1 junction (A), left parasagittal Oc–C1 junction (B), and coronal view of the Oc–C1 junction (C).

  • Mean morphometric measurements with standard deviations by age for female (dotted line) and male (solid line) patients. The pB-C2 (A), ADI (B), PADI (canal diameter at C1) (C), BDI (D), BAI (E), (F) BOD (F), dens angulation (G), Oc–C1 measured on parasagittal CT scans (H), and Oc–C1 measured on coronal CT scans (I).

  • 1

    Anderson RC, Ragel BT, Mocco J, Bohman LE, Brockmeyer DL: Selection of a rigid internal fixation construct for stabilization at the craniovertebral junction in pediatric patients. J Neurosurg 107 (1 Suppl):3642, 2007

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Bollo RJ, Riva-Cambrin J, Brockmeyer MM, Brockmeyer DL: Complex Chiari malformations in children: an analysis of preoperative risk factors for occipitocervical fusion. J Neurosurg Pediatr 10:134141, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Bonney PA, Maurer AJ, Cheema AA, Duong Q, Glenn CA, Safavi-Abbasi S, et al.: Clinical significance of changes in pB-C2 distance in patients with Chiari Type I malformations following posterior fossa decompression: a single-institution experience. J Neurosurg Pediatr 17:336342, 2016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Catalina-Herrera CJ: Study of the anatomic metric values of the foramen magnum and its relation to sex. Acta Anat (Basel) 130:344347, 1987

  • 5

    Cicchetti DV: Guidelines, criteria, and rules of thumb for evaluating normed and standardized assessment instruments in psychology. Psychol Assess 6:284290, 1994

  • 6

    Gire JD, Roberto RF, Bobinski M, Klineberg EO, Durbin-Johnson B: The utility and accuracy of computed tomography in the diagnosis of occipitocervical dissociation. Spine J 13:510519, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Grabb PA, Mapstone TB, Oakes WJ: Ventral brain stem compression in pediatric and young adult patients with Chiari I malformations. Neurosurgery 44:520528, 1999

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Hankinson TC, Tuite GF, Moscoso DI, Robinson LC, Torner JC, Limbrick DD Jr, et al.: Analysis and interrater reliability of pB-C2 using MRI and CT: data from the Park-Reeves Syringomyelia Research Consortium on behalf of the Pediatric Craniocervical Society. J Neurosurg Pediatr 20:170175, 2017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Kennedy BC, D’Amico RS, Youngerman BE, McDowell MM, Hooten KG, Couture D, et al.: Long-term growth and alignment after occipitocervical and atlantoaxial fusion with rigid internal fixation in young children. J Neurosurg Pediatr 17:94102, 2016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Khalsa SSS, Geh N, Martin BA, Allen PA, Strahle J, Loth F, et al.: Morphometric and volumetric comparison of 102 children with symptomatic and asymptomatic Chiari malformation Type I. J Neurosurg Pediatr 21:6571, 2018

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Ladner TR, Dewan MC, Day MA, Shannon CN, Tomycz L, Tulipan N, et al.: Evaluating the relationship of the pB-C2 line to clinical outcomes in a 15-year single-center cohort of pediatric Chiari I malformation. J Neurosurg Pediatr 15:178188, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Lee HJ, Kim JT, Shin MH, Choi DY, Hong JT: Quantification of pediatric cervical spine growth at the cranio-vertebral junction. J Korean Neurosurg Soc 57:276282, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Martinez-Del-Campo E, Kalb S, Soriano-Baron H, Turner JD, Neal MT, Uschold T, et al.: Computed tomography parameters for atlantooccipital dislocation in adult patients: the occipital condyle-C1 interval. J Neurosurg Spine 24:535545, 2016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Pang D, Nemzek WR, Zovickian J: Atlanto-occipital dislocation: part 1—normal occipital condyle–C1 interval in 89 children. Neurosurgery 61:514521, 2007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Pang D, Nemzek WR, Zovickian J: Atlanto-occipital dislocation—part 2: The clinical use of (occipital) condyle–C1 interval, comparison with other diagnostic methods, and the manifestation, management, and outcome of atlanto-occipital dislocation in children. Neurosurgery 61:9951015, 2007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Phuntsok R, Mazur MD, Ellis BJ, Ravindra VM, Brockmeyer DL: Development and initial evaluation of a finite element model of the pediatric craniocervical junction. J Neurosurg Pediatr 17:497503, 2016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Piatt JH Jr, Grissom LE: Developmental anatomy of the atlas and axis in childhood by computed tomography. J Neurosurg Pediatr 8:235243, 2011

  • 18

    Ravindra VM, Riva-Cambrin J, Horn KP, Ginos J, Brockmeyer R, Guan J, et al.: A 2D threshold of the condylar-C1 interval to maximize identification of patients at high risk for atlantooccipital dislocation using computed tomography. J Neurosurg Pediatr 19:458463, 2017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Riascos R, Bonfante E, Cotes C, Guirguis M, Hakimelahi R, West C: Imaging of atlanto-occipital and atlantoaxial traumatic injuries: What the radiologist needs to know. Radiographics 35:21212134, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Ridder T, Anderson RCE, Hankinson TC: Ventral decompression in Chiari malformation, basilar invagination, and related disorders. Neurosurg Clin N Am 26:571578, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Schmeltzler A, Babin E, Wenger JJ: Measurement of the foramen magnum in children and adults. Neuroradiology 2:162163, 1971

  • 22

    Shrout PE, Fleiss JL: Intraclass correlations: uses in assessing rater reliability. Psychol Bull 86:420428, 1979

  • 23

    Tubbs RS, Griessenauer CJ, Loukas M, Shoja MM, Cohen-Gadol AA: Morphometric analysis of the foramen magnum: an anatomic study. Neurosurgery 66:385388, 2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Vachhrajani S, Sen AN, Satyan K, Kulkarni AV, Birchansky SB, Jea A: Estimation of normal computed tomography measurements for the upper cervical spine in the pediatric age group. J Neurosurg Pediatr 14:425433, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Wanebo JE, Chicoine MR: Quantitative analysis of the transcondylar approach to the foramen magnum. Neurosurgery 49:934943, 2001

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