Advertisement

Child's Nervous System

, Volume 34, Issue 9, pp 1725–1733 | Cite as

Quantitative analysis of cranial-orbital changes in infants with anterior synostotic plagiocephaly

  • Rosalinda Calandrelli
  • Fabio Pilato
  • Luca Massimi
  • Marco Panfili
  • Concezio Di Rocco
  • Cesare Colosimo
Original Paper

Abstract

Purpose

The effects of premature fusion of one coronal suture cause skull and orbital alterations in term of side-to-side asymmetry. This study aimed to quantify the cranio-orbital complex changes related to the severity of skull base dysmorphology in patients with unicoronal synostosis.

Methods

Twenty-four infants affected by unicoronal synostosis were subdivided in three subgroups according to the severity of skull base deformity and their high-resolution CT images were quantitatively analyzed (groups IIa, IIb, III). Dimensions of cranial fossae, intracranial volume (ICV), ICV synostotic and ICV non synostotic side, whole brain volume (WBV), orbital volumes (OV), ICV/WBV, ICVsynostotic/ICVnon-synostotic, and OVsynostotic/OVnon-synostotic were evaluated.

Results

Asymmetry and reduction in the growth of the anterior and middle fossae were found in all groups while asymmetry of the posterior cranial fossa was found only in IIb and III groups. In all groups, ICV, WBV, and ICV/WBV were not significantly different while ICVsynostotic/ICVnon-synostotic and OVsynostotic/OVnon-synostotic resulted significant difference (p < 0.05). ICVsynostotic side resulted reduction only in group III. OV on the synostotic side was not significantly reduced although a trend in progressively reducing volumes was noted according to the severity of the group.

Conclusion

Skull and orbital changes revealed a side-to-side asymmetry but the effects of the premature synostosis were more severe in group III suggesting an earlier timing of premature unicoronal synostosis in group III with respect to the other groups. The assessment of the skull base deformity might be an indirect parameter of severity of skull orbital changes and it might be useful for surgical planning.

Keywords

High-resolution CT Craniosynostosis Skull base Intracranial volume Orbital volume 

Introduction

Anterior synostotic plagiocephaly (ASP) is the third most common type of unisutural craniosynostosis following scaphocephaly and trigonocephaly, accounting for 13–16% of all craniosynostoses [12, 19, 30]. Up to 40% of affected subjects are syndromic patients (mainly because of occurrence of Muenke syndrome) [16, 20]. ASP is characterized by the premature fusion of the coronal suture on one side [4, 13] but it can occur also in association with synostosis of other parts of the coronal ring such as the frontosphenoidal or frontoethmoidal sutures [13, 29]. Rarely, the picture is characterized by the fusion of the frontosphenoidal suture or the frontozygomatic suture alone [8, 14].

In ASP, high-resolution CT scan with 3-D reconstruction is accepted as a diagnostic tool to preoperatively assess the minor and the major sutures of the skull but it is not advisable for the postoperative follow-up because of the radiation dose and the possible need of sedation [18, 21, 22, 28].

In 1988, Di Rocco and Velardi proposed a classification scheme of ASP based on clinical observation and basicranium analysis using CT scan. According to this classification, the patients can be divided into three groups: group I: frontal bone flattening ipsilateral to the affected suture and elevation of the orbital roof without nasal pyramid deviation. In these children, axial CT scans show normopositioned vomer and petrous bone. Group II: frontal and orbital abnormalities with a contralateral deviation of the nasal pyramid and variable anterior displacement of the external ear of the synostotic side. This group is further divided in two subgroups: IIA and IIB, according to the severity of petrous bone anterior displacement and the presence of vomer bone deviation. Group IIA includes patients with normal positioning of the vomer with a mild or absent anterior displacement of the petrous bone on the affected side. Group IIB includes patients with a moderate degree of vomer deviation and severe displacement of the petrous bone, resulting in a reduced size of the middle cranial fossa; Group III: severe nasal deviation associated with ipsilateral deviation of the vomer and anterior displacement of the petrous bone in addition to frontal bone flattening and orbital bone anomalies with secondary asymmetry of the craniovertebral junction [11, 12, 26]. To explain the different degrees of severity of clinical and radiological phenotypes, the authors assumed that group I is the result of early fusion of one coronal suture, whereas the other two groups result from a progressive extension of sutural synostosis of the skull base sutures [11, 26]. Afterwards, previous reports, analyzing the “minor” sutures of the coronal arch by high-resolution CT, reported a different severity of skull base facial distortion also in infant with exclusive involvement of one coronal suture and suggested that the severity of cranio-facial deformity is probably related to the timing of unicoronal suture synostosis [5].

Currently, the assessment of the effects of ASP on the orbital and cranial cavities remains of special concern in considering the prognosis as well as the decision to proceed with surgical intervention [1, 2, 17]. Previous studies have quantified intracranial and orbital volumes in ASP but a univocal conclusion was not reached [15, 17, 25, 27, 31]. This is probably related to differences in the techniques of computed tomographic volumetry; heterogeneous or small samples; variable surgical intervention timing, procedures, or computed tomographic scan protocols; and inappropriate normative control data [7, 24, 32]. Moreover, these previous volumetric studies did not quantify intracranial and orbit volumes according to the severity of skull base phenotype in ASP infants.

The present study evaluates intracranial and orbital volumes in the different subgroups of patients with ASP according to the severity of skull base deformity with the goal to help to plan the best timing of fronto-orbital advancement in order to minimize the possible recurrence of the craniosynostosis.

Material and methods

Patients

We retrospectively reviewed the multiplanar high-resolution 3D-CT images of 26 infants with ASP (mean age 162.26 days, range 90–256 days). Twenty-four out of 26 children (mean age 163.91 days, range 100–256 days) were divided into three subgroups according to Di Rocco and Velardi classification [11, 12, 26]: group IIA, (n.7), mean age 167 days; group IIB, (n.10), mean age 168.5 days; and group III, (n.7), mean age 154.2 days. Two children with early frontosphenoidal synostosis were not included in this classification due to the absence of a corresponding clinical and radiological phenotype (Fig. 1). Twenty-four age-matched healthy subjects (mean age 161.33; range 81–255 days) who underwent CT examinations for cranio-facial trauma were enrolled as controls. The study was approved by the local Institutional Review Board.
Fig. 1

Classification scheme of anterior synostotic plagiocephaly based on cranio-facial dysmorphology. 3D-CT (a, b, c, e, f, g, i, j, k) and coronal 2D-CT (d, h, l). Vertex (a, e, i) and endocranial (c, g, k) 3D views have been rotated. Angles and lines on the synostotic side are shown in red while angles and line on the unaffected side are shown in black. Group IIA (ad); Note frontal bone flattening ipsilaterally to the affected suture (arrows, a), as well as elevation of the orbital roof (arrow, b), normal positioning of the vomer, mild or absent anterior displacement of the petrous bone on the affected side (c), and symmetry of the craniovertebral junction (d). Group IIB (eh); Note frontal bone flattening ipsilaterally to the affected suture (arrows, e) as well as elevation of the orbital roof (black arrow, f), contralateral deviation of the nasal pyramid (red arrow, f), moderate degree of vomer deviation, anterior displacement of the petrous bone (g), and symmetry of the craniovertebral junction (h). Group III (il); Note frontal bone flattening ipsilaterally to the affected suture (arrows, i) as well as elevation of the orbital roof (black arrow, j), contralateral nasal deviation (red arrow, j), ipsilateral deviation of the vomer, anterior displacement of the petrous bone (k), asymmetry of the craniovertebral junction (l)

CT scan

CT scans were performed using a GE Light Speed Pro 64 system (GE Medical System, Milwaukee, WI, USA) equipped with an automatic tube current modulation technique called the “AutomA” technique for low-dose scanning. The adaptive statistical iterative reconstruction technique (ASIR) had to be used in seven infants. Scans were obtained with a 1.25- or 0.6-mm axial slice thickness and data were processed using bone algorithms in addition to 2D-CT and 3D-CT reconstructions. Scanning was performed under spontaneous sleeping or sedation to avoid movements.

Analysis of the sutural pattern

Axial and coronal high-resolution slices implemented with 3D-CT reconstructions were used to determine the status of each suture in the length of the coronal ring and each splanchocranium suture; moreover, they were used to exclude the involvement of sutures of the other “sutural arches.” Each coronal suture was divided into three sections based on anatomical location (superior-central-inferior) and each section was scored as fused (f) or patent (p). Infants with a completely fused coronal suture were coded as “fff” (superior, central, and inferior sections fused); infants whose suture was patent in each section were coded as “ppp,” infants whose suture was partially fused were coded as “fpp,” “pfp,” “pff,” “ffp,” “ppf,” and “fpf,” according to the synostotic status of each section of the suture. Each other minor suture of the coronal ring and each splanchocranium suture was scored as fused (f), patent (p), or incompletely fused (fp) (Figs. 2 and 3).
Fig. 2

Coronal arch (a) begins at the bregma; composed of coronal sutures (white arrows, b), each of which is divided into an anterior branch, composed of the frontosphenoidal suture (white arrows, c) and ethmoido-sphenoidal synchondrosis (white arrow, d); and a posterior branch, composed of the spheno-parietal suture (white arrows, e), spheno-squamous suture (white arrows, f), and the spheno-petrosal synchondrosis (white arrows, g)

Fig. 3

Sutures of the splanchnocranium. 3D-CT (a) and 2D-CT (b–h). Sutures of the splanchnocranium visible in low-dose CT scans (a). Frontozygomatic sutures (white arrows: patent sutures, b); frontomaxillary sutures (white arrows: patent sutures, c); nasal suture (white arrowhead: patent suture, d); frontonasal sutures (white arrows: patent sutures, d); nasomaxillary sutures (white arrows: patent sutures, e); temporozygomatic sutures (white arrows: patent sutures, f); sphenozygomatic sutures (white arrows: patent sutures, g); zygomaticomaxillary sutures (white arrows: patent sutures, h); frontolachrymal sutures are not visible in low-dose CT scans

To characterize the side (i.e., half skull) of premature synostosis, we indicated as “affected” the side presenting premature fusion of the coronal suture associated or not to premature fusion of minor sutures synostosis of the coronal ring and “unaffected” the side displaying patent coronal and minor sutures of the coronal ring. The term “non affected” side only refers to the absence of premature fusion of the coronal suture on that side and does not imply that the skull shape of the non-affected side is normal.

Quantitative analysis of the skull base, orbital, and intracranial compartment

To avoid interobserver variability, the morphometric and volumetric measurements were performed twice by the same examiner (with 10-year experience in neuroradiology), in two different sittings. Linear measurements and volume outlines were subsequently verified by a second reader with the same experience to ensure consistency.

Skull base morphometry

On 3D-CT images using an endocranial view, we adopted definite landmarks to measure skull base asymmetry and hemi-fossae sizes [6]. The skull base was divided into two hemi-bases using an anatomic median line traced from the anterior edge of the crista galli for the anterior cranial fossa (C), to the center of the sella turcica for the middle cranial fossa (S) and to the opisthion for the posterior cranial fossa (O). The symmetry of each hemi-base was determined by the crista galli-sella turcica-opisthion angle (CSO^). The CSO angle was divided into three angles: the crista galli-sella turcica-xiphoid of the lesser wing of the sphenoid angle (CSX^) for the anterior cranial fossa, the xiphoid of the lesser wing of the sphenoid-sella turcica-internal acoustic meatus angle (XSM^) for the middle cranial fossa, and the internal acoustic meatus-opisthion angle (MSO^) for the posterior cranial fossa. The lengths CX, XM, and MO were measured on each side. The landmarks for lengths were the anterior edge of the crista galli (C), the xiphoid of the lesser wing of the sphenoid (X), the internal acoustic meatus (M), and the opisthion (O). Skull base asymmetry was assessed by comparing the angles of the two hemi-bases and angles/lengths of each hemicranial fossa of the affected side with the contralateral side and then by calculating the ratio between them (Fig. 4).
Fig. 4

Morphometric analysis of the skull base in subgroups IIa, IIb, and III of infants with anterior synostotic plagiocephaly. 3D-CT (a group IIA, b group IIB, c group III). Landmarks: C = anterior edge of the crista galli; S = center of the sella turcica; O = opisthion; X = xiphoid of the lesser wing; M = internal acoustic meatus. C, S, and O represent landmarks to divide the skull base into two hemi-bases. Lengths of ACF (CX), MCF (XM), and PCF (MO); angles of ACF (CSX^), MCF (XSM^), and PCF (MSO^). Asymmetry in CSX^ and MCF^, reduction in the length of the anterior (CX) and middle (XM) fossae on the synostotic side was found in IIA, IIB and III groups while asymmetry in MSO^ was found in groups IIB and III (angles and lengths altered are showed in red)

Volumetric analysis of intracranial compartment and orbits

Volumetric measurements were obtained with a semiautomatic segmentation open-source program called ITK-SNAP (version 2.4.0, Kitware, NY, USA), using the Cavalieri principle [2, 3, 17]. The ROI selected to represent the intracranial volume (ICV) included the entire intracranial cavity, after defining the start slice just above the foramen magnum and the end slice just beneath the vertex of the skull. The interface between the inner table of the skull and the surface of the brain was outlined in every slice. Cranial defects and foramina were manually closed. An analysis of each half skull was also performed calculating ICV on synostotic and non synostotic side (ICV affected side; ICV unaffected side). As bone signal of the midline, we considered, in supratentorial compartment, the sagittal suture while in the infratentorial compartment, the internal occipital crest.

The ROI representing the whole brain volume (WBV) included the cerebral hemispheres, midbrain, cerebellum, and brainstem to the level of the foramen magnum, excluding ventricles, venous sinuses, cranial nerves, and blood vessels.

Orbital volume (OV) was calculated outlining the interface between the bone walls and the soft tissue contents of the orbit in every slice of the CT images. Two areas of the orbit required particular attention: the posterior and the anterior boundaries. The posterior limit of the orbit was defined by a line connecting the medial and lateral walls of the optic foramen within the orbit, thus excluding the optic canal from volume estimations. The anterior boundary of the orbital cavity was defined by a line extending between the medial and lateral canthi in the appropriate slices, and between the corresponding most anterior bone edges of the medial and lateral orbital walls in the remaining slices. No attempt was made to include soft tissue orbital structures that lie outside the plane of the anterior boundaries of the orbits.

To quantify the brain growth respect to the bone cavity, the ICV/WBV ratio was calculated. To quantify the skull alterations in terms of side-to-side asymmetry, the ratio of one half-skull with respect to the contralateral one was calculated (ICVaffected side/ICVunaffected side). To evaluate the orbital side-to-side asymmetry the ratio between the orbital cavity volume on the affected and not affected side was calculated (OVaffected side/OVunaffected side) (Fig. 5).
Fig. 5

Volumetric analysis of intracranial compartment and orbits. Intracranial volume (ICV) is showed in red shaded areas (a and b); it includes the entire intracranial cavity from the foramen magnum to the vertex of the skull. The interface between the inner table of the skull and the surface of the brain are outlined. Half ICV is represented in bright and dark red shared areas (c and d); the sagittal suture (arrows, d) and the internal occipital crest (arrow, c) are the midline points dividing one half ICV from the contralateral one. Whole brain volume (WBV) is represented in green shared areas (e and f); it includes the cerebral hemispheres, midbrain, cerebellum , and brainstem to the level of the foramen magnum, excluding ventricles, and liquoral pericephalic spaces. Orbital volume is represented in blue shared areas (g and h): The posterior limit of the orbit was defined by a line connecting the medial and lateral walls of the optic foramen (OF) within the orbit (dot line, g), the anterior boundary of the orbital cavity was defined by a line extending between the medial (MC) and lateral canthi (LC) in the appropriate slices, and between the corresponding most anterior bone edges of the medial (MABE) and lateral orbital walls (LABE) in the remaining slices (dot lines, g and h)

Statistical analysis

Statistical analysis was performed on both skull base morphometric and cranio-orbital volumetric data. Descriptive statistics were expressed as the means ± SD for continuous variables. All statistical analyses were performed with Stat View version 5.0 (SAS Institute Inc.). Because of the skewed data distribution, a Kruskal-Wallis test followed by post hoc Mann-Whitney U test was performed to compare data from different groups. Statistical significance was set at p < 0.05. All statistical comparisons were corrected for multiple comparisons.

Results

Examination of all sutures along the coronal ring showed synostosis of one side coronal suture in 24 infants (complete synostosis in 14 children, partial synostosis in 10) and synostosis of one side frontosphenoidal (fs) suture in only 2 children (incompletely synostosis). The splanchnocranium sutures and sutures of the other sutural arches resulted patent in all patients (Table 1).
Table 1

Distribution of synostoses of the “coronal arch” and splanchnocranium sutures in children with anterior synostotic plagiocephaly. Classification based on the cranial base and facial 3D-CT scan

Anterior synostotic plagiocephaly

Age (days)

Coronal arch

Splanchnocranium sutures

Classification

Major sutures

Minor sutures

  

AB

PB

1

150

Crpfp

IIA

2

150

Clpff

IIA

3

170

Crppf

IIA

4

130

Crpfp

IIA

5

242

Crfff

IIA

6

163

Crfff

 

IIA

7

164

Crfff

IIA

8

120

Crffp

IIB

9

183

Crpff

IIB

10

153

Crfff

IIB

11

138

Crfff

IIB

12

140

Crpfp

IIB

13

256

Crfff

IIB

14

134

Crpfp

IIB

15

139

Clfff

IIB

16

180

Clfff

IIB

17

242

Clfff

IIB

18

160

Crpfp

III

19

164

Crfff

III

20

174

Clfff

III

21

105

Crpfp

III

22

221

Crfff

III

23

100

Crfff

_

_

_

III

24

156

Crfff

III

25

195

fsl fp

26

90

fsl fp

According to the status of each section of the suture, coronal suture (C) was scored as: “fff” = completely fused suture; “fpp”, “pfp”, “pff”, “ffp” = incompletely fused suture; frontosphenoidal suture (fs) was scored as: “ff” = completely fused suture, “fp” = incompletely fused suture

AB anterior branch, PB posterior branch

Following the Di Rocco classification, no child was included in group I, seven children were included in group IIA, ten children were included in group IIB, and seven were included in group III. Children with early fs synostosis were not included in this classification due to the absence of a corresponding clinical and radiological phenotype and were not quantitative evaluated (Table 1). No relationship between the extension of unilateral coronal synostosis and phenotype severity was found.

In all groups, the synostotic involvement of the unilateral coronal suture showed a marked anterior and middle skull asymmetry revealed by altered CSX^ and XSM^ ratios, a reduced growth of the anterior and middle fossae on the synostotic side with expansion of the opposite anterior cranial fossa. Although the size of the posterior cranial fossae was not altered, an asymmetry of the posterior cranial fossa (MSO^ ratio) was found in groups IIB and III (Table 2).
Table 2

Evaluation of hemi-base asymmetries, cranial fossae angles and lengths in the subgroup IIA and IIB and group III of children with anterior synostotic plagiocephaly compared with a healthy group control

 

Group IIA (n.7)

average

Group IIB (n.10)

average

Group III (n.7)

average

Control (n.24)

average

Group IIA

p value

Group IIB

p value

Group III

p value

Age (days)

167

168.5

154.28

161.33

0.5

0.8

0.9

CSO^(affected side)

170.57

167.5

164.42

179.87

< 0.0001

< 0.0001

< 0.0001

CSO^(unaffected side)

189.28

192.5

195.42

180.12

< 0.0001

< 0.0001

< 0.0001

Ratio

0.90

0.87

0.84

0.99

< 0.0001

< 0.0001

< 0.0001

CSX^(affected side)

50.5

50.99

46.24

54.35

0.04

0.02

0.0006

CSX^(unaffected side)

63.71

68.01

68.48

54.82

0.001

< 0.0001

0.0002

Ratio

0.79

0.75

0.67

0.99

0.0001

< 0.0001

< 0.0001

CX(affected side)

3.21

3.27

2.95

3.64

0.0005

0.0007

0.001

CX(unaffected side)

3.97

4.06

3.92

3.65

0.01

0.0011

0.02

Ratio

0.81

0.80

0.75

0.99

< 0.0001

< 0.0001

< 0.0001

XSM^(affected side)

75.01

70.95

73.3

82.00

0.0009

< 0.0001

0.01

XSM^(unaffected side)

81.25

80.69

81.65

82.00

0.9

0.7

0.8

Ratio

0.92

0.88

0.89

1

< 0.0001

< 0.0001

0.004

XM(affected side)

3.35

3.17

3.08

3.81

0.005

< 0.0001

0.0008

XM(unaffected side)

3.84

3.77

3.51

3.79

0.6

0.98

0.08

Ratio

0.87

0.84

0.87

1.006

< 0.0001

< 0.0001

< 0.0001

MSO^(affected side)

44.55

44.6

45.98

43.40

0.4

0.07

0.4

MSO^(unaffected side)

44.4

43.72

44.42

43.50

0.3

0.3

0.9

Ratio

1.003

1.02

1.03

0.99

0.8

0.003

0.01

MO(affected side)

3.62

3.61

3.55

3.67

0.4

0.3

0.1

MO(unaffected side)

3.64

3.6

3.55

3.66

0.5

0.6

0.2

Ratio

0.99

1.003

1.00

1.002

0.6

0.5

0.9

CSO^ crista galli-sella turcica-opisthion angle, CSX^ crista galli-sella turcica-xiphoid of the lesser wing of the sphenoid angle, XSM^ xiphoid of the lesser wing of the sphenoid-sella turcica-internal acoustic meatus angle, MSO^ internal acoustic meatus-opisthion angle, CX crista galli-xiphoid of the lesser wing of the sphenoid length, XM xiphoid of the lesser wing of the sphenoid-internal acoustic meatus length, MO internal acoustic meatus-opisthion length

In all groups: ICV, WBV, and ICV/WBV were not significantly different while ICVaffected/ICVunaffected and OVaffected/OVunaffected resulted significant difference (p < 0.05). ICV on the synostotic side resulted reduced only in group III. OV on the synostotic side was not significantly reduced although from group IIa to group III, a trend in progressively reducing volumes was noted (Table 3).
Table 3

Quantitative skull and orbital analysis in subgroups IIA and IIB and group III of children with anterior synostotic plagiocephaly compared with healthy subjects

 

Group IIA (n.7)

Average

Group IIB (n.10)

Average

Group III (n.7)

Average

Control (n.24)

Average

Group IIA

p value

Group IIB

p value

Group III

p value

ICV

790,800

776,799

748,515.28

807,804.16

0.4

0.4

0.1

WBV

676,437.85

669,333.8

641,896.28

696,098.54

0.4

0.1

0.1

Ratio

1.17

1.16

1.16

1.16

0.8

0.7

0.8

ICV(affected side)

385,242.85

377,520

357,271.42

405,244.16

0.2

0.1

0.03

ICV(unaffected side)

405,557.14

399,279

388,457.14

402,572.5

0.9

0.9

0.3

Ratio

0.95

0.94

0.92

1.005

0.0002

< 0.0001

< 0.0001

OV(affected side)

11,561.85

11,259

10,513.57

11,600.29

0.9

0.4

0.07

OV(unaffected side)

12,471.14

12,127

11,462.85

11,578.54

0.2

0.4

0.7

Ratio

0.92

0.92

0.91

1.001

0.0005

< 0.0001

< 0.0001

ICV entire intracranial cavity volume, WBV whole brain volume, ICVaffected side half skull intracranial volume on the synostotic side, ICVunaffected side half skull intracranial volume on the non synostotic side, OV orbital volume

Discussion

The prematurely fused unilateral coronal suture, in many cases associated with involvement of the frontosphenoidal suture, causes skull and orbital alterations in terms of side-to-side asymmetry [10, 15, 23]. Several authors published measurements of skull volume in infant with ASP but no univocal data was found [15, 25, 27, 31]; moreover, little attention has been given so far to the orbital volume and its changes during the first years of life as an indicator of orbital growth [2]. The previous studies were barely comparable due to scan protocols and the techniques to calculate volumetry on CT; furthermore, they did not report the skull and orbit volumetric changes related to severity of skull base phenotype.

The first step of the present study was to analyze the early synostotic involvement along the coronal ring and to subdivide our children in subgroups according to the severity of skull base phenotype according to Di Rocco and Velardi classification. The second step was to perform a morphometric analysis of the skull base and a volumetric analysis on the orbits and the skull in order to investigate the relationship between the skull base changes and the cranial-orbital growth. In agreement with previous studies, we found that the severity of skull base deformity did not depend on premature fusion of minor sutures in the length of the coronal ring nor on the degree of extension of the coronal suture synostosis [5]. In all groups, we found asymmetry of the anterior and middle fossae along with reduction in the length of the anterior and middle fossae on the synostotic side and increasing in the length of the opposite anterior cranial fossa; on the other hand, asymmetry of the posterior cranial fossa was found only in groups IIB and III.

These data suggest that the early unilateral coronal suture synostosis causes a localized growth defect of the anterior and middle cranial fossa of the affected side with consequent expansion of the opposite anterior cranial fossa. The asymmetry of the posterior cranial fossa found in groups IIB and III may depend on the anterior displacement of the petrous bone; this finding is in agreement with previous studies reporting the skull base results in an integral rigid biomechanical structure, deviated in one piece toward the synostotic side [6].

In all analyzed subgroups, ICV, WBV, and ratio ICV/WBV did not result significant difference from the control group. These findings demonstrated that the well-known changes in brain and skull shape due to coronal suture fusion and secondary compensatory growth pattern did not reflect in an altered overall brain and skull volume. On the other hand, the skull side-to-side asymmetry, demonstrated by a reduced hemi skull volume on the affected side respect to a compensatory volumetric increase on the non-affected side, support the redirected growth of the skull in infant with anterior synostotic plagiocephaly [15, 17]. Moreover, in the subgroup III, the significant reduction of the half skull on the synostotic side suggests that the severity of skull base dysmorphology, probably linked on the earlier timing of unicoronal suture synostosis, may reflect in early volumetric skull changes on the synostotic side.

The analysis of the orbital region showed a side to side asymmetry in all subgroups, but orbital volumes were not significantly different from normal subjects although in synostotic side a trend in progressively reducing volumes was noted according to the severity of the group. These data could be explained by the early age of our infants as facial growth and maturation follows the skull growth [9].

The relationship between the severity of skull base dysmorphology and cranial-orbital volumetric changes found in our infants with ASP suggests that skull base changes drive orbital and intracranial growth. Group III infants are those where the effects of the premature synostosis on the cranio-facial compartments appear earlier respect the groups IIa and IIb.

Conclusion

CT-based quantitative evaluation of the skull and orbital compartments in infants with ASP can increase the understanding of the secondary effects of premature unicoronal synostosis. Our findings indicate that skull base alterations drive the skull and orbital growth changes; the effects of the premature unicoronal synostosis are more evident among the infants with the higher severity of skull deformity suggesting an earlier timing of premature unicoronal synostosis in group III respect groups IIa and IIb.

In particular, the degree of the skull base asymmetry is a direct parameter of the severity of skull base deformity and it causes intracranial and orbital volumes changes on the synostotic side. Consequently, the assessment of skull base asymmetry may be a useful parameter to predict the intracranial and orbital growth changes and it may be helpful to select those infants needing an earlier surgical intervention. Further studies involving a larger sample are required to validate these results.

Notes

Compliance with ethical standards

Conflict of interest

Rosalinda Calandrelli declares that she has no conflict of interest. Fabio Pilato declares that he has no conflict of interest. Luca Massimi declares that he has no conflict of interest. Marco Panfili declares that he has no conflict of interest. Di Rocco Concezio declares that he has no conflict of interest. Cesare Colosimo declares that he is scientific consultant for Bracco Diagnostics Inc. and Bayer HealthCare.

Research involving human participants

Ethical approval

We declare that all procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. For this type of study formal consent is not required.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. 1.
    Aldridge K, Kane AA, Marsh JL, Panchal J, Boyadjiev SA, Yan P, Govier D, Ahmad W, Richtsmeier JT (2005) Brain morphology in nonsyndromic unicoronal craniosynostosis. Anat Rec A Discov Mol Cell Evol Biol 285:690–698.  https://doi.org/10.1002/ar.a.20201 CrossRefPubMedGoogle Scholar
  2. 2.
    Bentley RP, Sgouros S, Natarajan K, Dover MS, Hockley AD (2002) Changes in orbital volume during childhood in cases of craniosynostosis. J Neurosurg 96:747–754.  https://doi.org/10.3171/jns.2002.96.4.0747 CrossRefPubMedGoogle Scholar
  3. 3.
    Bentley RP, Sgouros S, Natarajan K, Dover MS, Hockley AD (2002) Normal changes in orbital volume during childhood. J Neurosurg 96:742–746.  https://doi.org/10.3171/jns.2002.96.4.0742 CrossRefPubMedGoogle Scholar
  4. 4.
    Bertelsen TI (1958) The premature synostosis of the cranial sutures. Acta Ophthalmol Suppl 36:1–176PubMedGoogle Scholar
  5. 5.
    Calandrelli R, D'Apolito G, Massimi L, Gaudino S, Visconti E, Pelo S, Di Rocco C, Colosimo C (2016) Quantitative analysis of craniofacial dysmorphology in infants with anterior synostotic plagiocephaly. Childs Nerv Syst 32:2339–2349.  https://doi.org/10.1007/s00381-016-3218-8 CrossRefPubMedGoogle Scholar
  6. 6.
    Captier G, Leboucq N, Bigorre M, Canovas F, Bonnel F, Bonnafe A, Montoya P (2003) Plagiocephaly: morphometry of skull base asymmetry. Surg Radiol Anat 25:226–233.  https://doi.org/10.1007/s00276-003-0118-x CrossRefPubMedGoogle Scholar
  7. 7.
    Cooper GM, Singhal VK, Barbano T, Wigginton W, Rabold T, Losken HW, Siegel MI, Mooney MP (2006) Intracranial volume changes in craniosynostotic rabbits: effects of age and surgical correction. Plast Reconstr Surg 117:1886–1890.  https://doi.org/10.1097/01.prs.0000218845.70591.7e CrossRefPubMedGoogle Scholar
  8. 8.
    Currarino G (1985) Premature closure of the frontozygomatic suture: unusual frontoorbital dysplasia mimicking unilateral coronal synostosis. AJNR Am J Neuroradiol 6:643–646PubMedGoogle Scholar
  9. 9.
    Derderian C, Seaward J (2012) Syndromic craniosynostosis. Semin Plast Surg 26:64–75.  https://doi.org/10.1055/s-0032-1320064 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Derderian CA, Wink JD, Cucchiara A, Taylor JA, Bartlett SP (2014) The temporal region in unilateral coronal craniosynostosis: a volumetric study of short- and long-term changes after fronto-orbital advancement. Plast Reconstr Surg 134:83–91.  https://doi.org/10.1097/PRS.0000000000000284 CrossRefPubMedGoogle Scholar
  11. 11.
    Di Rocco C, Velardi F (1988) Nosographic identification and classification of plagiocephaly. Childs Nerv Syst 4:9–15CrossRefPubMedGoogle Scholar
  12. 12.
    Di Rocco C, Paternoster G, Caldarelli M, Massimi L, Tamburrini G (2012) Anterior plagiocephaly: epidemiology, clinical findings, diagnosis, and classification. A review. Childs Nerv Syst 28:1413–1422.  https://doi.org/10.1007/s00381-012-1845-2 CrossRefPubMedGoogle Scholar
  13. 13.
    Esparza J, Munoz MJ, Hinojosa J, Romance A, Munoz A, Mendez MD (1998) Operative treatment of the anterior synostotic plagiocephaly: analysis of 45 cases. Childs Nerv Syst 14:448–454.  https://doi.org/10.1007/s003810050258 CrossRefPubMedGoogle Scholar
  14. 14.
    Francel PC, Park TS, Marsh JL, Kaufman BA (1995) Frontal plagiocephaly secondary to synostosis of the frontosphenoidal suture. Case report. J Neurosurg 83:733–736.  https://doi.org/10.3171/jns.1995.83.4.0733 CrossRefPubMedGoogle Scholar
  15. 15.
    Gault DT, Renier D, Marchac D, Ackland FM, Jones BM (1990) Intracranial volume in children with craniosynostosis. J Craniofac Surg 1:1–3CrossRefPubMedGoogle Scholar
  16. 16.
    Heuze Y, Martinez-Abadias N, Stella JM, Senders CW, Boyadjiev SA, Lo LJ, Richtsmeier JT (2012) Unilateral and bilateral expression of a quantitative trait: asymmetry and symmetry in coronal craniosynostosis. J Exp Zool B Mol Dev Evol 318:109–122.  https://doi.org/10.1002/jezb.21449 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Hill CA, Vaddi S, Moffitt A, Kane AA, Marsh JL, Panchal J, Richtsmeier JT, Aldridge K (2012) Intracranial volume and whole brain volume in infants with unicoronal craniosynostosis. Cleft Palate Craniofac J 48:394–398.  https://doi.org/10.1597/10-051 CrossRefGoogle Scholar
  18. 18.
    Khorasani M, Barzi MH, Derakhshan B (2013) Correction of maxillofacial deformities in a patient with unilateral coronal craniosynostosis (plagiocephaly): a case report and a review of literatures. J Dent (Tehran) 10:478–486Google Scholar
  19. 19.
    Kolar JC (2011) An epidemiological study of nonsyndromal craniosynostoses. J Craniofac Surg 22:47–49.  https://doi.org/10.1097/SCS.0b013e3181f6c2fb CrossRefPubMedGoogle Scholar
  20. 20.
    Lajeunie E, Le Merrer M, Bonaiti-Pellie C, Marchac D, Renier D (1995) Genetic study of nonsyndromic coronal craniosynostosis. Am J Med Genet 55:500–504.  https://doi.org/10.1002/ajmg.1320550422 CrossRefPubMedGoogle Scholar
  21. 21.
    Littlefield TR, Cherney JC, Luisi JN, Beals SP, Kelly KM, Pomatto JK (2005) Comparison of plaster casting with three-dimensional cranial imaging. Cleft Palate Craniofac J 42:157–164.  https://doi.org/10.1597/03-145.1 CrossRefPubMedGoogle Scholar
  22. 22.
    Mathijssen IM, van der Meulen JJ, van Adrichem LN, Vaandrager JM, van der Hulst RR, Lequin MH, Vermeij-Keers C (2008) The frontosphenoidal suture: fetal development and phenotype of its synostosis. Pediatr Radiol 38:431–437.  https://doi.org/10.1007/s00247-008-0750-z CrossRefPubMedGoogle Scholar
  23. 23.
    Matushita H, Alonso N, Cardeal DD, de Andrade F (2012) Frontal-orbital advancement for the management of anterior plagiocephaly. Childs Nerv Syst 28:1423–1427.  https://doi.org/10.1007/s00381-012-1765-1 CrossRefPubMedGoogle Scholar
  24. 24.
    Mooney MP, Burrows AM, Wigginton W, Singhal VK, Losken HW, Smith TD, Dechant J, Towbin A, Cooper GM, Towbin R, Siegel MI (1998) Intracranial volume in craniosynostotic rabbits. J Craniofac Surg 9:234–239CrossRefPubMedGoogle Scholar
  25. 25.
    Netherway DJ, Abbott AH, Anderson PJ, David DJ (2005) Intracranial volume in patients with nonsyndromal craniosynostosis. J Neurosurg 103:137–141.  https://doi.org/10.3171/ped.2005.103.2.0137 PubMedGoogle Scholar
  26. 26.
    Pelo S, Tamburrini G, Marianetti TM, Saponaro G, Moro A, Gasparini G, Di Rocco C (2011) Correlations between the abnormal development of the skull base and facial skeleton growth in anterior synostotic plagiocephaly: the predictive value of a classification based on CT scan examination. Childs Nerv Syst 27:1431–1443.  https://doi.org/10.1007/s00381-011-1514-x CrossRefPubMedGoogle Scholar
  27. 27.
    Polley JW, Charbel FT, Kim D, MaFee MF (1998) Nonsyndromal craniosynostosis: longitudinal outcome following cranio-orbital reconstruction in infancy. Plast Reconstr Surg 102:619–628 discussion 629-632CrossRefPubMedGoogle Scholar
  28. 28.
    Rogers GF, Mulliken JB (2005) Involvement of the basilar coronal ring in unilateral coronal synostosis. Plast Reconstr Surg 115:1887–1893 doi: 00006534-200506000-00011CrossRefPubMedGoogle Scholar
  29. 29.
    Seeger JF, Gabrielsen TO (1971) Premature closure of the frontosphenoidal suture in synostosis of the coronal suture. Radiology 101:631–635.  https://doi.org/10.1148/101.3.631 CrossRefPubMedGoogle Scholar
  30. 30.
    Selber J, Reid RR, Chike-Obi CJ, Sutton LN, Zackai EH, McDonald-McGinn D, Sonnad SS, Whitaker LA, Bartlett SP (2008) The changing epidemiologic spectrum of single-suture synostoses. Plast Reconstr Surg 122:527–533.  https://doi.org/10.1097/PRS.0b013e31817d548c00006534-200808000-00026 CrossRefPubMedGoogle Scholar
  31. 31.
    Sgouros S, Hockley AD, Goldin JH, Wake MJ, Natarajan K (1999) Intracranial volume change in craniosynostosis. J Neurosurg 91:617–625.  https://doi.org/10.3171/jns.1999.91.4.0617 CrossRefPubMedGoogle Scholar
  32. 32.
    Singhal VK, Mooney MP, Burrows AM, Wigginton W, Losken HW, Smith TD, Towbin R, Siegel MI (1997) Age related changes in intracranial volume in rabbits with craniosynostosis. Plast Reconstr Surg 100(1121–1128):1129–1130Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Polo scienze delle immagini, di laboratorio ed infettivologiche Area diagnostica per immagini Università Cattolica del Sacro CuoreFondazione Policlinico Universitario Agostino GemelliRomeItaly
  2. 2.Polo scienze dell’invecchiamento, neurologiche, ortopediche e della testa-collo, Area neuroscienze Università Cattolica del Sacro CuoreFondazione Policlinico Universitario Agostino GemelliRomeItaly

Personalised recommendations