 CHILDREN’S ORTHOPAEDICS

New radiological parameters for the

assessment of atlantoaxial instability in
children with Down syndrome
THE NORMAL VALUES AND THE RISK OF SPINAL CORD INJURY
N. Nakamura, Aims
Y. Inaba, To determine the normal values and usefulness of the C1/4 space available for spinal cord
Y. Aota, (SAC) ratio and C1 inclination angle, which are new radiological parameters for assessing
M. Oba, atlantoaxial instability in children with Down syndrome.
J. Machida,
Patients and Methods
N. Aida, We recruited 272 children with Down syndrome (including 14 who underwent surgical
K. Kurosawa, treatment), and 141 children in the control group. All were aged between two and 11 years.
T. Saito The C1/4 SAC ratio, C1 inclination angle, atlas-dens interval (ADI), and SAC were measured
in those with Down syndrome, and the C1/4 SAC ratio and C1 inclination angle were
From Kanagawa measured in the control group.
Children’s Medical
Center, Yokohama Results
City, Japan The mean C1/4 SAC ratio in those requiring surgery with Down syndrome, those with Down
syndrome not requiring surgery and controls were 0.63 (standard deviation (SD) 0.1), 1.15 (SD
 N. Nakamura, MD, PhD, Vice- 0.13) and 1.29 (SD 0.14), respectively, and the mean C1 inclination angles were -3.1° (SD
Director, Department of Pediatric
Orthopedic Surgery 10.7°), 15.8° (SD 7.3) and 17.2° (SD 7.3), in these three groups, respectively. The mean ADI and
 J. Machida, MD, PhD,
President, Director of Pediatric SAC in those with Down syndrome requiring surgery and those with Down syndrome not
Orthopedic Surgery
 N. Aida, MD, PhD, Director of requiring surgery were 9.8 mm (SD 2.8) and 4.3 mm (SD 1.0), and 11.1 mm (SD 2.6) and 18.5
Department of Pediatric
Radiology
mm (SD 2.4), respectively.
 K. Kurosawa, MD, PhD, Director
of Department of Medical Conclusion
Genetics
Kanagawa Children’s Medical The normal values of the C1/4 SAC ratio and the C1 inclination angle were found to be
Center, 2-138-4 Mutsukawa,
Minami-ku, Yokohama city, about 1.2° and 15º, respectively.
Kanagawa, 232-8555, Japan.

 Y. Inaba, MD, PhD, Associate

Cite this article: Bone Joint J 2016;98-B:1704–10.
Professor, Department of
Orthopedic Surgery Children with Down syndrome frequently neutral position; the C1/4 SAC ratio (Fig. 1)
 T. Saito, MD, PhD, Vice-
president of University, Professor have atlantoaxial instability. The incidence and the C1 inclination angle (Figs 2 to 4),10
and Chairman of Department of
Orthopedic Surgery ranges from 20% to 30%. Neurological symp- and we investigated cut-off values to identify
Yokohama City University, 3-9
Fukuura, Kanazawa-ku,
toms may be present in about 1%1-3 and these an indication for surgery.
Yokohama city, Kanagawa, 236-
0004, Japan.
children may develop quadriplegia or respira- This study presents the normal values of
 Y. Aota, MD, PhD, Vice-
tory insufficiency. After the onset of quadriple- these parameters in a larger group of children
president of hospital, Director of gia, surgical treatment will often only prevent with Down syndrome, and in a control group
Department of Orthopedic
Surgery further exacerbation of neurological symp- of those without Down syndrome with a nor-
Yokohama Brain and Spine
Center, 1-2-1 Takigashira, Isogo- toms.4-6 The early identification of myelopathy mal cervical spine. We compare the differences
ku, Yokohama city, Kanagawa,
235-0012, Japan. is difficult because mental retardation may pre- in values between these two groups and com-
 M. Oba, MD, Staff, Department vent these children from expressing their symp- pare those children with Down syndrome who
of Orthopedic Surgery
Saiseikai Wakakusa Hospital, 12-1 toms clearly. require cervical spinal surgery with those who
Hiragatacho, Kanazawa-ku,
Yokohama city, Kanagawa, 236-
The commonly used radiological parameters do not.
8653, Japan. of the atlas-dens interval (ADI) and the space
Correspondence should be sent
to N. Nakamura; email:
available for the spinal cord (SAC) are associ- Patients and Methods
nnakamura@kcmc.jp ated with poor inter- and intra-observer relia- A total of 315 children with Down syndrome,
©2016 The British Editorial bility.7 They also risk causing neuropathy aged between 0 and 18 years, who were treated
Society of Bone & Joint Surgery
doi:10.1302/0301-620X.98B12.
because they require radiographs to be per- in our institution between August 2013 and
BJJ-2016-0018.R1 $2.00 formed with the cervical spine in flexion.8,9 In March 2015, were identified from our data-
Bone Joint J a previous study, we defined and proved the base. The control group was selected from 237
2016;98-B:1704–10.
Received 22 February 2016; reliability of two radiological parameters that children with a neutral position, lateral radio-
Accepted after revision 14 July
2016 can be measured with the cervical spine in the logical examination of the cervical region dur-

1704 THE BONE & JOINT JOURNAL

 NEW RADIOLOGICAL PARAMETERS FOR THE ASSESSMENT OF ATLANTOAXIAL INSTABILITY IN CHILDREN WITH DOWN SYNDROME
Fig. 1
Radiograph showing the C1/4 space available for the
spinal cord ratio, which is defined as the ratio of the
anteroposterior diameter of the spinal canal at the
level of C1 to that at the level of C4.
Fig. 2
Radiograph showing that the C1 inclination angle is
defined as the angle formed between the line perpen-
dicular to the tangent at the posterior surface of the
body of C2 and the line connecting the centres of the
anterior and posterior arches of C1. Cranial inclina-
tion, in which the anterior arch of C1 is elevated, is
considered positive and caudal inclination, in which
the anterior arch is lowered, is considered negative.
ing the same period, taken for other indications, and which
revealed no abnormality of the craniocervical region. In
order to reduce bias, we excluded children aged less than
two years or > 12 years of age, as there were few patients
with Down syndrome undergoing radiological examination
in the first two years, and few control patients aged > 12
years. The present study thus included those aged between
two and 11 years (Table I). After exclusions, there were 272
children with Down syndrome, including 156 boys and 116
girls with a mean age at presentation of 5.5 years (standard
deviation (SD) 2.4). Of these, 14, four boys and ten girls
with a mean age at the time of surgery of 10.9 years (2.0 to
17.9), underwent surgical treatment of the cervical spine.
For this group, we reviewed all radiographs and plotted the
longitudinal changes from the time of their initial visit or on
VOL. 98-B, No. 12, DECEMBER 2016
1705
Fig. 3
Lateral radiograph of a ten-year-old girl with Down
syndrome who was treated without surgery; the
C1/4 space available for the spinal cord ratio was
1.23 and C1 inclination angle was 18°.
reaching the age of 11 years, and the parameters were com-
pared with both the non-surgical group with Down syn-
drome and the control group.
The indications for surgery were neurological symptoms
with instability on lateral dynamic plain radiographs of the
cervical spine (ten children), and no symptoms but cord
atrophy and/or T2 high intensity of the cord at the C1 level
on MRI scans (four children).10
After exclusions, the control group consisted of 141 chil-
dren, 81 boys and 60 girls with a mean age at the time of
their radiograph of 6.6 years (SD 2.9). The indications for
the radiographs are shown alongside the online version of
this paper in supplementary material.
The C1/4 SAC ratio and C1 inclination angle were meas-
ured in all children in both groups from the neutral position
lateral radiographs, as previously described.10 We also
measured the ADI and SAC in those with Down syndrome
as they had undergone dynamic radiography. All images
and measurements (undertaken by NN, MO, JM) were
obtained from the picture archiving and communication
system (Rapid Eye; Toshiba Medical Systems, Tokyo,
Japan) in our institution.
Statistical analysis. Comparisons between the three groups
were performed using the Kruskal-Wallis test, and compar-
isons between two groups were performed using the Mann-
Whitney U test. In order to explore the changes with the
passage of time between the ages of two and 11 years, in
longitudinal data on C1 inclination angle and C1/4 SAC
ratio, we used a linear mixed-effects model designed to take
account of each child’s age as a fixed effect variable, and the
random effect of individual differences. A p-value < 0.05
was considered significant. The SPSS version 24 (IBM Cor-
poration, Armonk, New York) was used for the analyses.
1706 N. NAKAMURA, Y. INABA, Y. AOTA, M. OBA, J. MACHIDA, N. AIDA, K. KUROSAWA, T. SAITO

Fig. 4a Fig. 4b Fig. 4c

Lateral radiograph of ten-year-old boy with Down syndrome who was treated surgically. He presented with mild spinal symptoms, including limping
gait, shortened walking distance, and dropping cutlery; a) pre-operative C1/4 space available for spinal cord ratio was 0.76 and C1 inclination angle
was -3°; b) pre-operative MRI (T2-weighted image) reveals spinal cord compression with high intensity at the C1 level; c) C1-2 fixation using C1 Late-
mass screws and C2 Pars screws (Stryker OASYS, Mahwah, New Jersey) was performed.

Table I. Age and gender of the children with Down syndrome and the control group

Frequency
Down syndrome Control
Entire cohort Girls Boys Entire cohort Girls Boys
Age (yrs) n %* n n n %* n n
2 28 10.3 9 19 20 14.2 9 11
3 71 26.1 29 42 15 10.6 6 9
4 31 11.4 9 22 13 9.2 3 10
5 28 10.3 16 12 14 9.9 5 9
6 42 15.4 22 20 16 11.3 8 8
7 28 10.3 9 19 17 12.1 9 8
8 11 4.0 6 5 12 8.5 8 4
9 11 4.0 5 6 9 6.4 3 6
10 12 4.4 5 7 10 7.1 4 6
11 10 3.7 6 4 15 10.6 5 10
Total 272 100 116 156 141 100.0 60 81
* contribution to the cohort

Results also statistically significant (p < 0.01). The estimated

C1/4 SAC ratio. The mean C1/4 SAC ratios were 0.63 (SD
0.1) in the surgical group with Down syndrome, 1.15 (SD
0.13) in the non-surgical group with Down syndrome, and
1.29 (SD 0.14) in the control group. These differences were
statistically significant (p < 0.01) (Fig. 5). The linear mixed-
effects model was applied to estimate the underlying trend in
the longitudinal data for the surgical group. The estimated
fixed effect of age on the C1/4 SAC ratio was -0.039/yr
(p < 0.01) (95% confidence interval (CI) -0.074 to -0.013).
Thus, this ratio was negatively correlated with age in this
group, which was consistent with the downward trend of
the ratio shown in Figure 5.
C1 inclination angle. The mean C1 inclination angle was -3.1
(SD 10.7) in the surgical group with Down syndrome, 15.8
(SD 7.3) in the non-surgical group with Down syndrome, and
17.2 (SD 7.3) in the control group. These differences were
fixed effect of age on the C1 inclination angle in the linear
mixed-effects model was -2.16°/yr (p < 0.01; 95% CI -2.92
to -1.46) in the surgical group. Although the distribution of
the angles was wider than the distribution of the C1/4 SAC
ratios, a downward trend for the C1 inclination angle was
also seen in the surgical group (Fig. 6).
ADI. The mean ADI was 9.8 mm (SD 2.8) in the surgical
group with Down syndrome and 4.3 mm (SD 1.0) in the
non-surgical group with Down syndrome. In 11 children, in
the surgical group (78.6%) and 207 in the non-surgical
group (76.1%), it was highest with the cervical spine in
flexion. The differences between these two groups were sta-
tistically significant (p < 0.01) (Fig. 7).
SAC. The mean SAC was 11.1 mm (SD 2.6) in the surgical
group with Down syndrome and 18.5 mm (SD 2.4) in the
non-surgical group with Down syndrome. In the latter

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 NEW RADIOLOGICAL PARAMETERS FOR THE ASSESSMENT OF ATLANTOAXIAL INSTABILITY IN CHILDREN WITH DOWN SYNDROME 1707

1.6
Control
1.4 Nonsurgical down
1
1.2 2
3
CI/14 SAC ratio 1 4
5
0.8 6
7
Surgical down
0.6 8
9
0.4 10
11
0.2 12
13
0 14
2 3 4 5 6 7 8 9 10 11
Age (yrs)
Fig. 5

Graph showing mean values for the C1/4 space available for the spinal cord (SAC) of ratio in the
control and non-surgical Down syndrome groups compared with the linear results the children
with Down syndrome who were treated surgically. The C1/4 SAC ratios were approximately 1.3
in the control group and approximately 1.2 in the non-surgical group with Down syndrome. The
ratios in the surgical group with Down syndrome deviated greatly from both other groups and
deteriorated over time. The ratios exceeded 1 standard deviation from the age of five years in all
children treated surgically. The whisker stands for 1 standard deviation.

group it tended to increase with the passage of time. In ten
patients in the surgical group (71.4%) and 201 in the non-
surgical group (73.9%), it was lowest with the cervical
spine in flexion. The differences between these two groups
were statistically significant (p < 0.01) (Fig. 8).
Surgical group. No children with normal anatomy under-
went surgery. Only three children did not have an os odon-
toideum, and in these the SAC was narrow while the ADI
was wide, indicating severe hypoplasia of C1. We assume
that the ligamentous laxity associated with Down syn-
drome becomes problematic in children with such a hypo-
plastic C1.
Discussion
The ADI and SAC are commonly used for the assessment of
atlantoaxial stability, and clinically critical values have been
estimated. However, assessment is often difficult and con-
troversial because of changes in values due to growth,3,11,12
poor inter- and intra-observer reproducibility13 and a poten-
tial risk of neuropathy due to flexion of the cervical
spine.8,9,14
The recently developed and reported the C1/4 SAC ratio
and the C1 inclination angle10 are expressed as a ratio and
an angle and are less likely to be affected by age and
growth. Moreover, their reproducibility and reliability were
found to be high in paediatric spinal surgeons and ortho-
paedic residents. The receiver operating characteristic
(ROC) curve analysis showed that both of these indices,
measured in the neutral position, had a diagnostic ability
comparable with the conventional ADI and SAC. In partic-
ular, the discriminatory ability of the C1/4 SAC ratio was
high. We concluded that children with a ratio of < 0.86, a
C1 inclination angle of < 10°, and an os odontoideum, were
likely to require surgery, and justified additional MR imag-
ing and/or referral to a spinal surgeon.10,15,16
The present study involved more children in order to
explore the normal values and to analyse measurements in
patients undergoing surgery. Both the non-surgical group
with Down syndrome and the control group had a C1/4
SAC ratio which was nearly constant. The difference in the
ratio between the surgical and non-surgical groups was
more obvious than other measurements, indicating that this
ratio would enable the early identification of patients who
would likely need surgery.
Based on analysis using the generalised linear mixed-
effects model, the C1/4 SAC ratio in the surgical group
tended to decrease with age. Although this trend was statis-
tically significant, the small number of observation points
limits the reliability of this finding. The distribution of age-
specific C1/4 SAC ratios in the surgical group tended to dif-
fer from the corresponding distributions in the other two
groups, possibly indicating a time-dependent change.
Although the C1 inclination angle also remained nearly
constant, the measurements were widely dispersed. As pre-
viously reported,10 the C1/4 SAC ratio is more reliable than
the C1 inclination angle. However, because the differences
between the surgical and non-surgical groups with Down
syndrome were significant, and as both measurements are

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1708 N. NAKAMURA, Y. INABA, Y. AOTA, M. OBA, J. MACHIDA, N. AIDA, K. KUROSAWA, T. SAITO

40
Control

Nonsurgical down
30
1

20 3
C1 inclination angle (º)

5
10
6

7
0 Surgical down
8
2 3 4 5 6 7 8 9 10 11
9

-10 10

11

12
-20
13

14
Age (yrs)
-30
Fig. 6

Graph showing the mean C1 inclination angle in children with Down syndrome who were treated without surgery and controls, com-
pared with the linear results over time for the children who were treated surgically. Although there were statistically significant differ-
ences in the C1 inclination angle between the three groups, the differences were not as clear as for the C1/4 space available for the spinal
cord ratio. The C1 inclination angle alone was inadequate as a parameter for the determination of indications for surgery.

obtained from lateral imaging of the spine in the neutral
position, we consider the C1 inclination angle to be a useful
supplementary measurement to the C1/4 SAC ratio.
All the children with Down syndrome underwent
dynamic radiography. However, as we found, surgery can
be indicated based on the evaluation of images taken in the
neutral position alone. Although each measurement
changed with the passage of time in the surgical group (the
C1/4 SAC ratio, C1 inclination angle, and SAC decreased
over time, whereas the ADI increased), this does not imply
changes in cut-off values for the indications for surgery
with age. Instead, this indicates a progression towards
advanced subluxation of C1 and local kyphosis,17-19 at
which time it is too late to make the diagnosis.
ADI was associated with a wide variation of data in the
surgical group with Down syndrome, suggesting that the
assessment of risk based on numerical values would be dif-
ficult. This is comparable with previously reported find-
ings.20 The SAC in the surgical group with Down syndrome
increased with age, reflecting the increase in the diameter of
the spinal canal3,11,12 with growth. If the SAC remains
unchanged during follow-up, this may indicate a relative
deterioration of stenosis supporting the use of the C1/4
SAC ratio, instead of absolute numbers.
Regarding C1, the patients with Down syndrome who
did not need surgery still had significantly more severe
hypoplasia than the normal control group (Fig. 5). Those
who needed surgery, however, had much more severe hypo-
plasia of C1 than those who did not need surgery. Compres-
sion of the spinal cord causing myelopathy is further likely
in children with additional ligamentous laxity and an os
odontoideum. Measuring the maximal ADI and minimal
SAC in a risky forward flexion position is unnecessary, as
the os odontoideum is readily observed in lateral images
taken in the neutral position. One of the children who
underwent surgery (patient 2, supplementary material)
experienced worsening of paralysis and respiratory insuffi-
ciency during pre-operative radiography in flexion.
The rate of surgery in children with Down syndrome
reflects the published rate of those with neurological symp-
toms of about 1%. We identified 14 surgical cases during a
period when 1542 children with Down syndrome aged < 18
years registered in our hospital. With different surgical indi-
cations. However, the measurements would vary. As there

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 NEW RADIOLOGICAL PARAMETERS FOR THE ASSESSMENT OF ATLANTOAXIAL INSTABILITY IN CHILDREN WITH DOWN SYNDROME 1709

14
Nonsurgical down
12 1
2
10 3

ADI (mm)
4
5
8
6
7
6 Surgical down
8
9
4 10
11
2 12
13
0 14
2 3 4 5 6 7 8 9 10 11
Age (yrs)
Fig. 7

Graph showing the mean atlas-dens index (ADI) for children with Down syndrome who
were treated without surgery compared with the linear results over time for those treated
surgically. In some children with a more severe condition, when the atlantal anterior arch
was anteriorly and inferiorly displaced to the greatest extent, the ADI decreased.

30
Nonsurgical down
1
25
2
3
20 4
SAC (mm)

5
6
15 7
Surgical down
8
10 9
10
11
5
12
13
0 14
2 3 4 5 6 7 8 9 10 11
Age (yrs)

Fig. 8

Graph showing the mean space available for the spinal cord (SAC) for those with Down syn-
drome who were treated without surgery compared with the linear results over time for those
treated surgically. The SAC was relatively effective in distinguishing between surgical and
non-surgical cases. However, enlargement of the spinal canal with growth was linked with a
longitudinal increase in the baseline SAC. As a result, there were children in whom there was
little change in values despite deterioration of their condition.

were few children undergoing surgery for analysis of the
data on C1/4 SAC ratio and C1 inclination angle, the linear
mixed-effects model may not be accurate. Nonetheless, we
suggest that the downward trend of these parameters is
characteristic of the surgical group.
A further limitation is the retrospective nature of the
study. Although those children in the control group were
reported to have no abnormality in either the spine or spi-
nal cord, it is debatable whether they can be classed
‘normal’.

VOL. 98-B, No. 12, DECEMBER 2016

1710 N. NAKAMURA, Y. INABA, Y. AOTA, M. OBA, J. MACHIDA, N. AIDA, K. KUROSAWA, T. SAITO
In conclusion, for atlantoaxial instability in children
with Down syndrome, our proposed C1/4 SAC ratio and
C1 inclination angle can be determined from lateral images
of the cervical spine in the safe, neutral position. These
parameters are comparable with the conventionally used
ADI and SAC in their ability to identify severe cases. We
would recommend that paediatricians not specialised in the
cervical spine use these new parameters.
The normal values for the C1/4 SAC ratio and inclina-
tion angle were found to be about 1.2 and 15º, respectively.
Children with a C1/4 SAC ratio of < 0.8 have a high risk of
developing neurological symptoms or signs and referral to
paediatric spinal surgeons is recommended.
Take home message:
The risk of developing myelopathy is especially high in chil-
dren with a C1/4 SAC ratio of < 0.8.
Supplementary material
Tables showing the symptoms and pathology neces-
sitating radiographs of the cervical spine in the con-
trol group without Down syndrome and details of the
children with Down syndrome who underwent surgery can
be found alongside this article online at http://
www.bjj.boneandjoint.org.uk
Author contributions:
N. Nakamura: Designed the study, Interpreted the data, Wrote the initial manu-
script, Approved the final manuscript as submitted.
Y. Inaba: Designed the data collection, Reviewed and revised the manuscript,
Approved the final manuscript as submitted.
Y. Aota: Designed the data collection, Reviewed and revised the manuscript,
Approved the final manuscript as submitted.
M. Oba: Supported statistical analysis, Approved the final manuscript as sub-
mitted.
J. Machida: Collected the data, Carried out initial analyses, Reviewed the man-
uscript, Approved the final manuscript as submitted.
N. Aida: Designed the data collection, Reviewed and revised the manuscript,
Approved the final manuscript as submitted.
K. Kurosawa: Collected the data, Carried out initial analyses, Reviewed the man-
uscript, Approved the final manuscript as submitted.
T. Saito: Designed the data collection, Reviewed and revised the manuscript,
Approved the final manuscript as submitted.
No benefits in any form have been received or will be received from a commer-
cial party related directly or indirectly to the subject of this article.
This article was primary edited by E. Moulder and first proof edited by J. Scott.
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