Anatomical Limitations for Endoscopic Endonasal Skull Base Surgery in Pediatric Patients

Jason R. Tatreau, BS; Mihir R. Patel, MD; Rupali N. Shah, MD; Kibwei A. McKinney, MD; Adam M. Zanation, MD Department of OtolaryngologyHead and Neck Surgery, University of North Carolina Hospitals, Chapel Hill, North Carolina, U.S.A. INTRODUCTION
Expanded endonasal approaches (EEAs) to midline sellar or parasellar skull base lesions have reduced post-surgical morbidity and costs when compared with transcranial approaches.1 EEAs to these lesions are potentially limited by several boney sinonasal landmarks and critical neurovascular structures: 1. piriform aperture2 2. sphenoid sinus pneumatization3 3. intercarotid distances4 The majority of surgical complications in pediatric skull base approaches occurs in patients with sellar or suprasellar pathologies.5 Developmental immaturity of the skull base and appositional neurovasculature is likely to contribute to this morbidity. Age-related differences in midline skull base anatomy relevant to EEAs have not been characterized. Quantitative pediatric anatomical measurements relevant to skull base approaches are lacking. Our goal was to use radioanatomic analysis of computed tomography (CT) scans to determine anatomical limitations for trans-sphenoidal EEAs in pediatric skull base procedures.

RESULTS: PIRIFORM APERTURE WIDTH

Significantly different between patients under 2 years of age (17.2 0.5 mm) and adults (22.2 1.3 mm) (p<0.00003) Significantly narrower in patients up to 6-7 years of age compared to adults (p<0.002) No significant difference among patients 9-10 years of age and older

CONCLUSIONS
The major anatomical parameters governing midline skull base access do not pose limitations on the use of EEAs in pediatric patients with skull base lesions. Piriform aperture is likely a limit only in the youngest patients (under 2 years). While incomplete sphenoid sinus pneumatization necessitates more drilling, the early maturation of intercarotid distances as well as the availability of intra-operative imaging and neuronavigational systems indicate that this is not a contraindication for EEAs in pediatric patients. Drilling distances for trans-planar, trans-sellar, and trans-clival approaches are described Demarcation of the posterior sellar wall is not possible by trans-sphenoidal visualization in the majority of pediatric patients. Therefore, it is important to consider age-specific length of the pituitary fossa, which increases by more than 50% from age 2 to adulthood.

Figure 2. Maximum transverse distance of anterior nasal aperture, measured in coronal CT scans and reported as an average for each patient age group. Error bars represent 95% confidence intervals.

RESULTS: SPHENOID BONE PNEUMATIZATION

Anterior sphenoid bone/planum sphenoidale: anterior cranial fossa Pneumatization begins after age 2 at the antero-inferior wall of the sphenoid bone By 6-7 years of age, the sphenoid anterior wall was fully pneumatized in all patients By 6-7 years of age, 88 17% of the planum was pneumatized Sella turcica: middle cranial fossa On average, 6-7 year-old patients had 77% of the anterior sellar wall and 32% of the sellar floor pneumatized 84% (42/50) of patients under 16 years of age had no dorsum pneumatization Sellar floor length in patients under 2 years of age was only 66% of that in adults Superior clivus: posterior cranial fossa

LITERATURE CITED
Figure 3. Graphical representation of the age-related degree of pneumatization of the planum sphenoidale, anterior sellar wall, and sellar floor. The percent pneumatization was determined by measuring the length of each specific skull base dimension with <3 mm of bone thickness as a percent of the total length of that margin. Data are reported as the average for each age group. Error bars represent 95% CI.

METHODS
A retrospective radio-anatomic cross-sectional study Age-stratification of patients (n=60)
age n <2 8 3-4 8 6-7 9 9-10 8 12-13 8 15-16 9 adult 10

Not observed prior to age 10 Present in 89% of patients 15 years of age and older
Measurements of Sphenoid Bone Lengths and Thicknesses.* Measurement SKB-ASB SKB-PS SKB-PSTmin SKB-PSTmax SKB-ASW SKB-ASWTmin SKB-ASWTmax SKB-SF SKB-SFTmin SKB-SFTmax SKB-PSW SKB-SC SKB-SCTmin SKB-SCTmax SKB-ISB SKB-SOJ <24 mo (n=8) 3-4 y (n=8) 6-7 y (n=9) 9-10 y (n=8) 12-13 y (n=8) 15-16 y (n=9) Adults (n=10)

13.5 (12.3-14.7) 14.5 (13.0-15.9) 14.3 (13.3-15.2) 15.9 (14.4-17.4) 16.2 (14.9-17.4) 15.7 (14.8-16.5) 17.1 (14.4-19.8) 13.8 (12.4-15.2) 14.8 (13.0-16.6) 15.8 (14.6-16.9) 16.5 (15.0-18.0) 19.0 (16.8-21.3) 19.3 (17.3-21.4) 19.6 (17.9-21.3) 4.5 (3.9-5.1) 7.7 (6.7-8.8) 5.4 (4.5-6.2) 3.2 (2.4-4.0) 6.7 (5.6-7.8) 6.2 (5.6-6.7) 8.3 (6.0-10.6) 9.9 (7.6-12.2) 8.6 (7.7-9.4) 6.9 (6.2-7.7) 1.3 (0.7-1.8) 2.1 (0.9-3.3) 7.0 (6.2-7.7) 2.0 (0.8-3.1) 2.5 (0.9-4.2) 8.8 (7.9-9.8) 1.5 (0.7-2.3) 4.5 (3.6-5.4) 8.5 (8.0-9.1) <1.0 1.5 (0.5-2.4) 6.4 (5.5-7.2) 1.2 (0.8-1.6) 1.7 (0.4-3.0) <1.0 2.1 (0.8-3.5) 8.3 (7.5-9.2) 1.6 (1.0-2.2) 2.2 (0.9-3.4) <1.0 <1.0 7.4 (6.8-8.0) <1.0 <1.0 1.1 (0.9-1.4) 1.4 (0.8-2.1) 8.2 (7.0-9.3) <1.0 1.5 (0.8-2.1)

Exclusion criteria:
pre-existing conditions altering skull base anatomy (including trauma) previous sinus or skull base surgery congenital midface anomalies nasal polyposis premature birth

9.9 (9.1-10.7) 10.6 (10.1-11.1) 11.1 (10.5-11.7) 11.7 (11.2-12.3) <1.0 3.1 (2.5-3.8) 8.7 (7.6-9.8) 1.1 (0.9-1.3) 3.0 (1.6-4.3) 9.1 (8.7-9.6) <1.0 1.5 (1.0-2.0) 9.2 (8.3-10.1) <1.0 <1.0 8.8 (8.2-9.3)

Measurements:
Averaged within age groups, 95% CI Lengths: defined below Percent pneumatization: the ratio of pneumatized bone to the total length of that boney margin

9.0 (7.9-10.0) 12.3 (11.3-13.3) 12.5 (11.5-13.5) 13.4 (12.0-14.8) 15.5 (13.9-17.0) 17.5 (16.7-18.3) 18.9 (16.7-21.1) 18.4 (15.4-21.4) 11.3 (9.6-13.0) 8.1 (5.7-10.4) 7.8 (3.0-12.6) 9.4 (3.6-15.2) 2.9 (1.2-4.5) 4.0 (2.1-5.9) 3.0 (0.1-5.8) 4.7 (0.8-8.5)

21.2 (18.1-24.3) 13.8 (11.7-15.8) 10.6 (8.2-13.0)

19.1 (17.0-21.2) 20.8 (19.3-22.3) 22.3 (20.8-23.8) 23.2 (21.8-24.7) 24.4 (22.5-26.2) 26.3 (23.7-28.8) 26.7 (24.5-28.8) 10.2 (9.5-11.0) 12.5 (11.7-13.2) 14.6 (14.0-15.1) 14.9 (13.8-15.9) 16.1 (14.7-17.5) 16.0 (14.9-17.1) 15.0 (13.4-16.6)

Section: coronal

PA-W: piriform aperture width

SKB=skull base; ASB = anterior sphenoid bone; PS = planum sphenoidale; PST = planum sphenoidale thickness; ASW = anterior sellar wall; ASWT = anterior sellar wall thickness; SF = sellar floor; SFT = sellar floor thickness; PSW = posterior sellar wall; SC = superior clivus; SCT = superior clivus thickness; ISB = inferior sphenoid bone; SOJ = spheno-occipital junction. * Data reported as distance in mm (confidence interval). Distance is less than limit of measurability. Absence of pneumatization precludes measurement.

Figure 4. Graphical representation of the temporal pattern of sphenoid sinus pneumatization. Top: Representative midsagittal CT images of age-specific sphenoid sinus pneumatization patterns. Bottom: A qualitative depiction of age-specific pneumatization patterns. The percent pneumatization was determined by measuring the length of each specific skull base dimension (defined in Table I) with <3 mm of bone thickness as a percent of the total length of that margin. Data are reported as the average for each age cohort. Lines were smoothed and error bars omitted to qualitatively describe pneumatization patterns.

Section: midsagittal

SKB-PS: skull base, planum sphenoidale length SKB-ASB: skull base, anterior sphenoid bone height SKB-ISB: skull base, inferior sphenoid bone length SKB-SOJ: skull base, spheno-occipital junction length SKB-SC: skull base, superior clivus length SKB-ASW: skull base, anterior sellar wall height SKB-SF: skull base, sellar floor length SKB-PSW: skull base, posterior sellar wall height

1. Ceylan S, Koc K, Anik I. Endoscopic endonasal trans-sphenoidal approach for pituitary adenomas invading the cavernous sinus. J Neurosurg 2009; May 29. [Epub ahead of print]. 2. Gruber DP, Brockmeyer. Pediatric skull base surgery, 1. Embryology and developmental anatomy. Pediatr Neurosurg 2003; 38:2-8. 3. Kassam A, Thomas AJ, Snyderman C, et al. Fully endoscopic expanded endonasal approach treating skull base lesions in pediatric patients. J Neurosurg (2 Suppl Pediatrics) 2007; 106:75-86. 4. Yilmazlar S, Kocaeli H, Eyigor O, Hakyemez B, Korfali E. Clinical importance of the basal cavernous sinuses and cavernous carotid arteries relative to the pituitary gland and macroadenomas: quantitative analysis of the complete anatomy. Surg Neurol 2008; 70:165175. 5. Brockmeyer D, Gruber DP, Haller J, Shelton C, Walker ML. Pediatric skull base surgery, 2. Experience and outcomes in 55 patients. Pediatr Neurosurg 2003; 38:9-15.

RESULTS: INTERCAROTID DISTANCES

At the level of the cavernous sinus: Significantly narrower in patients up to 6-7 years-old (10.21.0mm) compared with adults (12.60.9) (p<0.003) No significant difference among patients 9-10 years of age and older (p>0.36) At the level of the superior clivus:

Section: midsagittal

ACKNOWLEDGEMENTS
This work was funded by a T35 training grant from the National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK) (T35-DK007386-29)
Figure 5: Graphical representation of minimum intercarotid distances. At the level of the superior clivus, measured as the minimum distance between the medial margins of the posterior vertical segment of the carotid canal inferior to the sellar floor. At the level of the cavernous sinus measured as the minimum distance between the medial aspects of the intracavernous carotid sulcus, inferior to the optic canals. Distances were measured in axial CT scans and reported as an average for each patient age group. Error bars represent a 95% confidence interval

Section: axial

ICD-CS: minimum intercarotid distance at the cavernous sinus, between the medial aspects of the carotid prominence at the anterior vertical loop of the ICA

Section: axial

ICD-SC: minimum intercarotid distance at the superior clivus, immediately caudal to the sellar floor
Figure 1. Representative radiographic measurements in adult patients. Measurement parameters were identical in pediatric patients.

Not statistically different between adults and any of the pediatric cohorts (p>0.18)

None of the authors have any conflicts of interest, financial or otherwise.

Data analysis:
unpaired, 2-tailed t-tests with unequal variance