A Study of the Developing Paediatric Skullbase Anatomy and its Application to Endoscopic Endonasal Approaches in Children
Correspondence Address: Source of Support: None, Conflict of Interest: None DOI: 10.4103/0028-3886.294543
Source of Support: None, Conflict of Interest: None
Keywords: Endoscopic endonasal surgery, inter carotid distance, pediatric skullbase, skullbase pneumatisation, sphenoid sinus
The endoscope offers a wider visualization of the anatomic landmarks on the posterior wall of the sphenoid sinus. Furthermore, the close-up and multi-angled views provided by the endoscope allow the surgeon to maintain constant control of the neurovascular structures during dissection. Expanded endonasal approaches (EEA) for lesions of the anterior cranial base, suprasellar region, and the ventral posterior fossa have gained widespread acceptance due to improvements in the available technology like illumination, wide angle of view and high definition of images seen at surgery.,, EEA now is also being increasingly used in children for skull-base tumors like craniopharyngioma although the anatomical parameters of their sphenoid sinus vary significantly from adults. EEA uses the sphenoid sinus anatomy as a portal to access the anterior cranial base and ventral posterior fossa. Incomplete sphenoid sinus pneumatization and its septa may pose a challenge to the surgeon in safely identifying the location and orientation of the internal carotid arteries (ICA), the optic nerves and the sella. A thorough preoperative understanding of their anatomy is a sine qua non in planning an expanded endonasal approach.
The paediatric skull-base is constantly changing due to change in dimensions of the sinonasal skeleton and its progressive pneumatization.,,, The surgical approach to the skull-base involves passing through three cardinal corridors, the initial nasal phase from the nostril to the anterior face of the sphenoid, the sphenoid phase which involves bone removal within the sphenoid sinus and dural access through trans-planum, trans-sellar or trans-clival corridors. The initial approach to the anterior wall of the sella through the nostril involves passing the endoscope through the pyriform aperture, which has the potential to limit introduction of the endoscope into the nostril. The nasal cavity is typically narrow and is often limited by the middle turbinate. The extent of bone removal needed within the sphenoid sinus to facilitate instrumentation and the extent of bone removal for dural access is variable in children. The dimensions of the sphenoid as well as the pneumatization of the sphenoid determines the quantum of bone removal needed for dural access. The paediatric population also offers unique challenges because of the smaller working spaces and the smaller size of the skull base involved.
In this study, we have radiologically measured the dimensions of the corridors that are traversed during EEA. We have quantified the variations seen in these measurements in children of different age groups, this correlates with the extent of bone removal needed for endoscopic access to the paediatric skull base at various points during the phase of exposure. This data can be used to determine the extent of drilling needed for dural access through the sella, planum, and the clivus in children.
This is a retrospective review of computerized tomography (CT) scans done on patients of age less than 18 years for a variety of conditions, none of which involved the skull base [Table 3]. The study was performed after clearance from the institutional ethics committee. Patients with a history of head injury, skull-base trauma or a prior skull-base surgery and those with mid-face anomalies which would alter the measurements were excluded from the study. All the CT scans were reviewed by a neuroradiologist and a neurosurgeon simultaneously. The measurements were made at points described later. The information was then categorized according to age groups.
Radiological image analysis and measurements
We selected CT images of patients who were less than 18 years of age and had undergone contrast enhanced CT for this study. Patients who had high resolution thin section (0.9 mm) images were included in the study. CT scanning were performed on a Philips 256-section iCT scanner. The protocol used is characterized by 0.9 mm thickness, 0.45 mm increment, gantry rotation time 0.5 sec and pitch <1. All scans were analyzed in a work station with IMPAX PACS (™Agfa) which enables visualization of images in sagittal, axial, and coronal planes as well as manipulation of the images through reconstruction planes.
The measurements were made from the points described below.
Nares to sphenoid distance (NSD) was measured from the anterior tip of nasal aperture to anterior wall of sphenoid sinus in the mid sagittal plane [Figure 5]. The distance from the anterior wall of sphenoid to floor of sella was measured in the mid sagittal plane [Figure 5]. In the axial plane, the lateral limits of the ICA were measured for the inter-sphenoidal angle [Figure 5]. The sphenoid sinus pneumatization was graded as 1: No pneumatization, 2: Pre-sellar pneumatization, 3: Sellar pneumatization, 4: Post-sellar pneumatization based on perpendicular line drawn through the tuberculum sellae in the sagittal plane [Figure 6]. The intercarotid distance was calculated as the distance measured between the ICA in the coronal plane at 1: At the level of proximal dural ring, 2: At the level of apex of the carotid siphon in the cavernous sinus, 3: At the level where the petrous ICA transitions into the paraclival ICA [Figure 7].
The drilling distances measured were Anterior sellar bone thickness (ASBT) which is the thickness of bone anterior to the sellar dura [Figure 8]. The Sellar Floor thickness (SFT) was the measured bone thickness between the anterior and posterior sellar wall in the sagittal plane. Anterior cranial base thickness (ACBT) was the thickness of bone measured from the anterior aspect of planum sphenoidal to anterior sella [Figure 8]. The posterior sellar bone thickness (PSBT) was measured from the anterior sphenooccipital junction (SOJ) to anteroinferior sphenoid bone in the sagittal plane [Figure 8]. The volumetry of the entire sphenoid sinus and its pneumatized part was done separately.
The data analysis was done using Intercooled Stata 14.1 (Stata corp, Texas, USA). Mean and Standard Deviation was used to describe the measurements and the mean values were compared between different age groups by one-way Anova with post hoc test (Bonferroni).
CT scan images of 110 patients (male-68, female-42) were included for the study. The number of patients in each age groups was as follows [0–6 years, 17; 7–9 years, 20; 10–12 years, 27; 13–15 years, 29; 16–18 years, 17].
The indications for CT cerebral angiogram in these children are given in [Table 3].
1) Nostril to sphenoid sinus: The distance between the nostril and the sphenoid sinus, is the initial corridor that the endoscope traverses. This distance was seen to increase significantly with age, while it was 62.6 ± 6.7 mm in children <6 years, it increased to 69.4 ± 5.2 mm in children aged 13-15 years (P = 0.003) and 72.3 ± 7.3 mm in children aged 16-18 years (P = 0.01). The increase signifies the growth of the sinonasal passage with age [Table 1] and [Figure 1], [Figure 5]a
2) Anterior wall of the sphenoid sinus to sella: The mean distance between the anterior wall of the sphenoid sinus and the sella in children below 6 years of age was 17.2 ± 2.9 mm. This distance was seen to increase significantly in children aged 13–15 years 20.7 ± 3.1 mm (P = 0.002) and 16–18 years 20.6 ± 3.3 mm (P = 0.011) [Table 1] and [Figure 5]b
3) Inter-sphenoid angle: The inter-sphenoid angle in children less that 6 years of age was 23.5 ± 2.6 degrees. This angle increased significantly in children between 13 and 15 years to 27.3 ± 5.4 degrees (P = 0.023) [Table 1] and [Figure 1], [Figure 5]c
4) Drilling distances: The anterior sellar bone thickness, which needs to be drilled to reach the dura of the sella was 6.7 ± 5.0 mm. The amount bone which needs to be drilled decreases with age, this difference is significant as the child grows, for children aged 13–15 years it was 2.0 ± 1.7 mm (P = 0.001) and for children aged 16–18 years it was 2.3 ± 3.2 mm (P = 0.001). This decrease in bone thickness is due to the progressive pneumatization of the sella as the child grows. It was noted that between the age groups 13-15 years and 16–18 years this distance was not statistically different, indicating that pneumatization is complete by the time the child is 13–15 years old [Table 1] and [Figure 8]
5) Sphenoid pneumatization: The pneumatization of the sphenoid sinus around the sella is not uniform. By measuring the height and thickness of the bone around the sella, we measured the change in bone thickness brought about by pneumatization. The pneumatization of the sphenoid sinus was noted to progress in an anterior to posterior direction. In all patients included in our study, early pneumatization was noted in the anterior aspect of the sphenoid sinus at the age of 7–8 years. The ACBT measuring the thickness of bone below the planum was 14.8 ± 4.8 mm in children <6 years of age, 9.3 ± 4.8 mm in children aged 13–15 years (P = 0.02). The SOJ was 10.2 ± 4.1 mm in children aged <6 years and 6.7 ± 3.3 mm in children between 13 and 15 years (P = 0.02). The thickness of the superior clivus in children <6 years was 10.2 ± 3.6 mm and 10.3 ± 4.5 mm in children between 13–15 years (P = 0.5) [Table 1] and [Figure 8]. These measurements indicate that the anterior part of the sphenoid below the planum achieves pneumatization in the most children by the age of 13 years, while the superior clivus and the dorsum are unlikely to pneumatize
6) Volume of pneumatization: We performed volumetric measurements of the total volume of the sphenoid sinus and the pneumatized volume of the sphenoid sinus. The volume of the sphenoid in children between 0 and 6 years was 4641.4 ± 1924.7 mm3. The pneumatized sphenoid volume in the same age group was 1655 ± 1631.1 mm3. In children between 7 and 9 years, the total volume of the sphenoid sinus was 8502.35 ± 2538.5 mm3, an increase of nearly 85% in volume. The pneumatized volume of the sphenoid was 4984.5 ± 2550.3 mm3. In older children between 13 and 15 years, the total volume of sphenoid sinus was 11732.8 ± 2614.4 mm3. The volume of pneumatization in the sphenoid sinus in this group was 6287.5 ± 2157.9 mm3. The total volume of the sphenoid sinus was seen to correlate with the age of the child. (Pearson coefficient (r) = 0.704, P < 0.001). The volume of pneumatization of the sphenoid sinus was also seen to have a positive correlation to the age of the child. (r = 0.62, P < 0.0001) [Table 1] and [Figure 2], [Figure 3], [Figure 6]
7) Intercarotid distance: The intercarotid distance (ICD) was measured at three different points along the course of the ICA in the skull base. The measurements in children <6 years of age were (1) proximal dural ring = 13.4 ± 2.0 mm, (2) cavernous = 15.9 ± 2.5 mm, (3) paraclival = 13.5 ± 1.8 mm. The narrowest measurement of ICD was seen at the level of the proximal dural ring. This distance was seen to change significantly with age, and in children between ages 10 and 12 years, this distance was measured to be 15.6 ± 2.2 mm (P = 0.036). In 110 observations made, the mean distances were (1) proximal dural ring = 14.6 ± 2.4 mm, (2) cavernous sinus = 16.73 ± 2.7 mm, (3) paraclival = 14.83364 ± 2.4 mm). Even in the youngest group of children (<6 years), the narrowest intercarotid distance at the level of the proximal dural ring was13.4 mm [Table 2] and [Figure 4], [Figure 7].
The paediatric sinonasal skeleton is work in progress. Proper knowledge about the sinonasal anatomy and sphenoid sinus development can be of help during pre-operative evaluation of children undergoing EEA. Many of the anatomical landmarks that we see in the adult sphenoid sinus are not seen in children. The gradual pneumatization of the sphenoid sinus is accompanied by increase in its vertical and horizontal dimensions, this also increases the volume of the sphenoid sinus., Age-related differences specific to EEA for the Indian children are not well described and there is paucity of literature on relevant quantitative paediatric anatomical measurements.
Banu et al. in a radio-anatomic study of 107 paediatric patients found that the volume of the sphenoid sinus increased with age. They noticed that the increase in volume most closely mirrored the progression of pneumatization within the sphenoid sinus. This is similar to our study where we have observed that the total volume of the sphenoid sinus as well as the volume of pneumatization within the sphenoid sinus increased as children grew older, the process of pneumatization results in the decrease of thickness of bone anterior and inferior to the sella. Tatreau et al. in a radio-anatomic cross-sectional survey of 50 paediatric and ten adult patients observed that pneumatization of the sphenoid sinus started at the anteroinferior wall and progressed in a posterior fashion, first reaching the floor of the sphenoid bone, followed by the planum sphenoidale and the anterior sellar wall. This anterior to posterior progression of pneumatization was also seen in our study. While comparing the thickness bone at various points in the skull base, we observed a far lesser decrease in the anterior sellar bone thickness (ASBT) when compared to the posterior sellar bone thickness (PSBT) in different age groups. This correlates well with our observation that more posteriorly located structures like the dorsum sellae and the posterior clinoids very rarely pneumatize.
Interestingly our measurements reveal that the sinonasal dimensions even in younger children are by no means prohibitive for safe endoscopic instrumentation. From the endonasal perspective, due to the short nares-sphenoid distance, in younger children, the final field is likely to be less deep with a shorter working distance as compared to older children and adults. We used the inter-sphenoid angle as a surrogate for the width of the sphenoid as it more closely replicates the corridor utilized while manipulating two long shafted instruments introduced through both the nares. The width of the sphenoid determines the degree of freedom available a side-to-side fashion for positioning multiple instruments in the nasal corridor, this dimension increases progressively and a statistically significant change is noted in the dimensions as the child grows older. The shorter distance of approach in younger children probably compensates for the smaller width of the corridor.
We also observed that the volume of the sphenoid in children between 0 and 6 years was 4641.4 ± 1924.7 mm3, whereas the pneumatized volume was 1655 ± 1631.1 mm3. In children between 7 and 9 years, the total volume of the sphenoid sinus was 8502.35 ± 2538.5 mm3, an increase of nearly 85% in volume. This increase in the working space available for instrumentation within the sinus facilitates surgery. In fact, nearly its entire volume can be drilled to create space for the manipulation of instruments. Drilling the bone in these regions is not difficult as it is typically soft developing bone. However, lack of pneumatization conceals impressions and recesses like the OCR and the clival recess that are familiar landmarks seen during surgery on adults. Drilling in the midline to access the sellar dura before drilling laterally can be a useful method of determining the depth of drilling needed to reach the dura. Drilling down the bone till it is thin enough to be lifted off by the foot plate of a Kerrison ronguer, can also avoid vascular injuries that may occur during bone removal. The mean distance between the anterior wall of the sphenoid sinus and the sella in children below six years of age was 17.2 ± 2.9 mm. This dimension directly correlates with the increasing pneumatization of the sphenoid sinus, thereby adding depth to the operating field. Progressive pneumatization also increases the ease of instrument manipulation within the sphenoid.
A narrow ICD has been long held as a limiting factor in children. Various authors have speculated that an ICD less than 10 mm would preclude the use of this corridor.,, Banu et al. found that the ICD varied in children with age and degree of pneumatization of the sphenoid sinus. However, in their study, even in the youngest age group of 2–4 years, the narrowest ICD measured was 11.3 mm. In our study, we found that the intercarotid distance was more than 10 mm at all measured levels along the course of the ICA. We did not find any child with an ICD less than 10 mm. Even in the youngest age group of 0–6 years, the narrowest distance at the level of the proximal dural ring was 13.4 mm. While an intercarotid distance of 10 mm has been considered the minimum distance which precludes endonasal access especially in children, it is clear from these measurements that this long held contention is unfounded.
These dimensions are also important in considering the design of instruments for EEA. Currently available adult sinus endoscopes are 4 mm in diameter, while pediatric sinus scopes are 2.8 mm in diameter. The length of instruments used for EEA is 15–18 cm. These are designed with the adult sinonasal anatomy in mind. Our measurements show that a statistically significant difference exists in nasal distances of children who are less than six years old and those who are older than 13 years of age, whose nasal measurements are similar to that seen in adults. Instruments which are shorter with narrower profile will probably decrease the restrictions in instrument mobility within smaller nasal cavities, thereby decreasing the instances of “sword-fighting” between the endoscope and the instruments and as a result, facilitate microsurgical handicraft.
The sinonasal anatomy shows maximal development between the age of 6 to15 years after which it plateaus. During this period the sphenoid sinus pneumatization proceeds from its anterior to posterior aspect. Neurovascular structures are affected by the asymmetrical development of skull base. Developmental process like pneumatization brings about changes in the thickness of the skull base and affects the drilling distances. The intercarotid distance was not seen to be a hindrance for endoscopic endonasal surgery. The pneumatization in young children may be incomplete and this necessitates drilling within the sphenoid sinus, however, this is unlikely to be a contraindication for EEA in children. None of the sinonasal parameters measured in this study appear to restrict EEA in children. However, a meticulous preoperative assessment of the CT scan may be needed for optimal surgical outcome. [16,17]
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Conflicts of interest
There are no conflicts of interest.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8]
[Table 1], [Table 2], [Table 3]