Surgical Anatomy and Technique
Corridor-Based Endonasal Endoscopic Surgery for Pediatric Skull Base Pathology With Detailed Radioanatomic Measurements
Banu, Matei A. MD*; Rathman, Allison DO*; Patel, Kunal S. BS*; Souweidane, Mark M. MD*,‡; Anand, Vijay K. MD§; Greenfield, Jeffrey P. MD, PhD*,‡; Schwartz, Theodore H. MD*,§,‖
*Department of Neurological Surgery, Weill Cornell Medical College, New York, New York;
‡Department of Pediatrics, Weill Cornell Medical College, New York, New York;
§Department of Otolaryngology, Head and Neck Surgery, Weill Cornell Medical College, New York, New York;
‖Department of Neurology and Neuroscience, Brain and Spine Center, Brain and Mind Research Institute, Weill Cornell Medical College, New York, New York
Correspondence: Jeffrey P. Greenfield, MD, PhD, 525 East 68th St, Box 99, New York, NY 10065. E-mail: email@example.com
Received June 12, 2013
Accepted November 11, 2013
BACKGROUND: Pediatric anatomy is more restricted, and the propagation of endonasal endoscopic approaches in the pediatric population has been limited.
OBJECTIVE: To demonstrate the feasibility of the endonasal endoscopic approach in a variety of age groups and to perform measurements of the corridors and spaces available for surgery as a guide for case selection.
METHODS: Only patients <18 years were included. The choice of operative corridor/approach is described in relation to pathological entity and location. Preoperative/postoperative visual fields and endocrine panels, extent of resection, as well as postoperative long-term complications are described. Prospective magnetic resonance image-based anatomic measurements of key distances were performed to determine age-dependent surgical indications and limitations.
RESULTS: Forty purely endoscopic procedures were performed in 33 pediatric patients (5-18 years of age) harboring a variety of skull base lesions, from benign tumors to congenital malformations. For the 20 patients in whom gross total resection was the intended goal of surgery, gross total resection was attained in 15 (75%). There were 2 infections (5%) and no cerebrospinal fluid leaks. Significant improvement was shown in 58.3% of patients with visual deficits. Hormone overproduction resolved in 75% of patients, while preoperative hormone insufficiency only improved in 29.2%. Wider intercarotid distance at the superior clivus (P = .01) and shorter nare-dens working distance (P = .001) predicted improved outcomes and fewer postoperative complications.
CONCLUSION: Endonasal endoscopic skull base approaches are viable in the pediatric population, they are not impeded by sphenoid sinus aeration, and they have minimal risk of cerebrospinal fluid leak and meningitis. Outcomes and complications can be predicted based on specific radio anatomical skull base measurements rather than age.
ABBREVIATIONS: ASB, anterior sphenoid bone
ASW, anterior sellar wall
DI, diabetes insipidus
EEA, endonasal endoscopic approach
FSE, fast spin echo
GH, growth hormone
GTR, gross total resection
ICD-CS, intercarotid distance at the level of the cavernous sinus
ICD-SC, intercarotid distance at the superior clivus
MaxWiT, maximum width between middle turbinates
NDD, nare-dens distance
NSD, nare-sellar distance
NVD, nare-vomer distance
SKB, skull base
STR, subtotal resection
TA, transsphenoidal angle
VCD, vomer-clival distance
Lesions of the cranial base in the pediatric population are a challenging entity to treat, being hampered by difficult access, local anatomic constraints of the developing skull, and complicated skull base reconstruction. Classical open approaches, either anterior craniotomies or combined craniofacial resections, are efficient, well-established methods in the adult population. However, the decreased incidence of such lesions in children has created a paucity of data regarding outcomes of open skull base procedures in pediatric patients. Using small case series, several groups have reported equal efficacy of these traditional techniques in children.1-4 Traditional approaches are sometimes avoided in the pediatric patient because they may transgress incompletely matured growth centers in the developing craniofacial skeleton with potential long-term sequelae.2,5 Craniofacial approaches require brain retraction and can lead to a cosmetically undesirable outcome with disruption of tooth buds despite intricate closure techniques used to reconstruct the nasomaxillary complex.5-10
Expanded endonasal endoscopic approaches (EEAs) offer a new surgical method to midline lesions of the pediatric skull base.11-17 Being minimally invasive approaches, EEAs not only minimize surgical trauma, but are also capable of navigating around bony growth centers. Improved visualization of the pathology through the intrinsic magnification of the lens and the wide panoramic view obtained through the use of angled endoscopes are the characteristics that make EEAs technically appealing.18 Specially adapted microinstruments now allow passage through the narrow sinonasal pathway to access the entire midline skull base in a rostrocaudal fashion, from the crista galli to the cervicomedullary junction.11,12,15,19-21
The use of EEA in the pediatric population has been limited.6,9,22-25 The narrower corridor afforded by the developing sinonasal tract renders these approaches more challenging.22,26-28 The pneumatization of the sphenoid sinus is a gradual process, starting at age 2 and completed by age 16, and impacts the entire anatomy of the developing skull base.27,29 Likewise, the nares themselves have a limited working area.26 Furthermore, little is known about the impact of skull base pathology on the developmental process and implicitly on the endoscopic corridors. In this article, we report our 8-year experience with a large series of pediatric patients undergoing EEA and use radioanatomic measurements of a variety of skull base parameters to assist in the selection of appropriate endoscopic corridors and of suitable candidates for surgery. Magnetic resonance imaging (MRI) measurements are used to assess age-dependent drilling distances, intracranial working space, and the main restriction areas. Furthermore, specific radioanatomic parameters can also be used as predictive markers for outcomes and to assess the risk for complications following EEA, regardless of age group. Unique surgical considerations and operative nuances in pediatric patients are also highlighted.
After obtaining institutional review board permission, we queried a prospectively compiled database of all purely endoscopic endonasal procedures performed at our institution by the senior authors (J.P.G., M.M.S., T.H.S., and V.K.A.) between January 2004 and August 2012 and identified patients younger than 18 years of age. Only pure endonasal endoscopic procedures for midline skull base lesions were selected for this study.
Patients were divided into 4 categories based on pathology: (1) benign neoplastic lesions, (2) malignant neoplastic lesions, (3) congenital malformations, and (4) iatrogenic or posttraumatic cerebrospinal fluid leaks and meningoencephaloceles. Location and extension of the lesion were analyzed based on preoperative MRI studies and linked to the surgical corridor and skull base approach chosen for each case. The corridor approach-based paradigm for categorizing endonasal endoscopic skull base surgeries is derived from our previously published protocol.15 Postoperative outcomes, including the extent of resection, visual fields, endocrine studies, and complications are described.
In brief, the initial corridor comprises the nasal anatomic region transgressed to reach the skull base: (1) transsphenoidal, (2) transethmoidal, (3) transmaxillary, or (4) transnasal, ie, no sinus is breeched. Each of these corridors, in turn, exposes an anatomic region of the skull base. The transsphenoidal corridor is the most commonly used corridor in this case series and permits the exposure of the sella, suprasellar cistern, medial cavernous sinus, and superior clivus. The sellar and parasellar regions are the main focal points of pediatric pathology. The transethmoidal corridor exposes the orbital apex, the lateral cavernous sinus, and the anterior fossa through the fovea ethmoidalis. The transmaxillary corridor exposes the pterygopalatine fossa, the petrous apex, Meckel cave, and the infratemporal fossa. Finally, the transnasal corridor exposes the cribriform plate, the inferior two-thirds of the clivus, and the odontoid. Combinations of endoscopic corridors and approaches were used to access the skull base lesions based on the specifics of the pathology, and we attempted to assess the feasibility and level of risk for each, based on the pediatric age group and the MRI-based measurements of local anatomy (see below).
The details of endonasal endoscopic approaches have been described in detail in several previous articles.8,15,30-39 We will include only specific details that are unique to our center or to the pediatric population. Given the tight space provided by the pediatric skull, we frequently use a bimanual dissection procedure. Removal of the turbinates, inferior, middle, or superior, may be performed with increased frequency compared with adult cases to create more room for surgery. However, the initial approach involves lateralization of the turbinates with preservation of normal nasal anatomy as a primary goal. A generous posterior septectomy is also helpful. After intubation, the child is administered cefazolin (50 mg/kg) unless the tumor has an intra-arachnoidal component, in which case triple antibiotics are given. These generally consist of vancomycin (15 mg/kg), ceftazidime (50 mg/kg), and metronidazole (10 mg/kg). All patients receive intrathecal fluorescein (AK-Fluor, Akorn, Illinois) to better visualize dural defects intraoperatively and to assist in watertight closure.40 For patients in whom a large cerebrospinal fluid (CSF) leak is not anticipated, this is done through a lumbar puncture, withdrawing 10 mL of CSF mixed and reinjected with 0.25 mL of 10% fluorescein. For cases in which a large CSF leak is anticipated, a lumbar drain (LD) is placed. We premedicate with dexamethasone (10 mg) and diphenhydramine (50 mg) to reduce the incidence of an inflammatory reaction, although this has never been encountered. Intraoperative navigation is used in all cases. In the transsellar approach, we perform a posterior osteotomy after large sphenoidotomies to access the sellar floor more rostrally and dorsally and to protect the pituitary stalk. For craniopharyngioma dissection, we usually maintain an arachnoid plane between the tumor and the optic nerve to avoid iatrogenic damage to the optic apparatus. In tumors of the cavernous sinus, such as cavernous hemangiomas or chondrosarcomas, there is clear benefit from the Doppler probe, identifying the precise location of the internal carotid artery. In these cases, once the carotid is identified, the dura can be opened widely up to the carotid, and 45°-angled endoscopes are used to inspect the cavity. We frequently use computed tomography (CT) angiography-guided neuronavigation to identify the internal carotids during the intracavernous dissection. Access to the clival region is most often required for chordomas or brainstem and optic nerve decompression in tumors such as ependymomas and osteochondral dysplasia. Again, we liberally use a Doppler probe to identify basilar and vertebral arteries before debulking the tumor. Brainstem-evoked potentials also aid in guiding the extent of resection. Fibrous dysplasia and osteoblastomas are rare bone tumors extending to the cranial cavity through the ethmoid sinus and can be effectively accessed through the transethmoidal corridor. Nasopharyngeal angiofibromas extending into the middle cranial fossa and infiltrating osteosarcomas can be best accessed through a transmaxillary transpterygoid approach. We usually remove juvenile angiofibromas circumferentially with the use of a ball cautery, continuously preventing active bleeding and with preoperative embolization to decrease intraoperative hemorrhages. Using a purely endonasal endoscopic approach, we were also able to reach as far as the cervicomedullary junction. This approach is required for complex developmental anomalies such as Chiari malformations with retroinclination of the odontoid process. In basilar invagination, this approach can prove extremely useful for ventral decompression of the cervical spine and brainstem through anterior resection of the odontoid and clivus.
Although our closure technique has evolved over time, the following principles are currently used, with variations occurring in the earlier part of our series. Extradural tumors without a CSF leak are closed by using FloSeal (Baxter, Deerfield, Illinois) or Gelfoam for hemostasis. Small CSF leaks are closed with an autologous fat graft, covered with DuraSeal (Covidien, Mansfield, Massachusetts). For sellar tumors, the fat is held in place with a small piece of Medpor (Porex, Fairburn, Georgia) to reconstruct the floor of the sella. However, giant sellar tumors, where a large CSF leak is expected, are treated with lumbar drainage for 24 hours (5 mL/h) and a nasoseptal flap is harvested to cover the Medpor, which is held in place with DuraSeal. For encephaloceles, meningoencephaloceles, and posttraumatic CSF leaks, the defect in the skull base is usually very small, but patients often have elements of intracranial hypertension. For these cases we use an inlay of DuraGuard (DuraGuard Products Inc, Walden, New York) covered with an onlay of autologous fat, a nasoseptal flap, and DuraSeal. Lumbar drainage is used for 3 days (5 mL/h).33,41 Finally, for large intradural tumors, we use the “gasket-seal” closure in which a piece of autologous fascia lata is overlaid on the defect and held in place with a countersunk piece of Medpor.42,43 This construct is covered with a nasoseptal flap and DuraSeal. Lumbar drainage is used for 24 hours and is removed in the evening on postoperative day 1 so patients can be mobilized on postoperative day 2.
Age-Specific Anatomical Measurements
The pediatric population depicted here included all patients 18 years of age or younger. Because development of the pediatric skull base has been shown to be finalized by 18 years in healthy children, we only included patients with ages >18 in the radioanatomic analysis to assess potential delays in development.28 Patients were further stratified into 4 age groups, according to different stages of skull base development: <10 years, 10 to 14 years, 15 to 18 years, and 19 to 21 years. Classic radioanatomic measurements26,27 as well as our own parameters were used prospectively to better assess the pathology-disrupted anatomy of the developing pediatric skull and to preoperatively plan surgical trajectory. A brief definition of all radioanatomic measurements and the clinical relevance to the corridor and/or approach adopted are provided below. Although CT scans might be more sensitive to bone anatomy, measurements were made on preoperative MRI scans, because all patients had MRI scans and we try to avoid CT scans in the pediatric population unless absolutely necessary. Furthermore, MRI sequences allow for better discrimination of soft tissue and vascular structures. All measurements were independently confirmed by a neuroradiologist and an otolaryngologist on a Picture Archiving and Communication System (Agfa Healthcare). Special consideration was given to the sphenoid sinus region, with respect to bone limitations, length, and width on coronal sections as well as type of pneumatization to assess the working space provided for the endoscope and microinstruments. Additionally, we used a novel system of parameters and measurements to assess the impact of skull base development on EEA outcomes. Three types of MRI skull base parameters were used to assess anatomic limitations of sequential stages of EEAs: drilling parameters (length of planum sphenoidale, length of anterior and inferior sphenoid bone, length of the spheno-occipital junction, length of superior clivus, height of anterior and posterior sellar walls, length of the sellar floor); restriction parameters (intercarotid distance at the superior clivus and cavernous sinus, transsphenoidal angle, maximum width between middle and inferior turbinates); and working parameters (nare-sellar distance, nare-dens distance, nare-vomer distance, vomer-clivus distance). Different MRI sequences acquired at 5-mm thickness with no skip were used: sagittal T1 weighted fast spin echo (FSE), axial T1 and T2 weighted FSE, coronal T1 and T2 weighted FSE, axial diffusion-weighted imaging, and 2-plane T1-weighted FSE postgadolinium. Measurements were performed on patients undergoing EEA for a variety of skull base lesions. To assess the impact of skull base pathology on the developmental process, we then applied the novel set of skull base parameters to a cohort of 83 children with no skull base or maxillary-facial pathology, with ages ranging from 5 to 16 years. We performed measurements from age 5, the age of our youngest patient undergoing EEA, up to age 16, when the pneumatization of the sphenoid sinus and skull base development are considered finalized.26,27 A neuroradiologist and a neurosurgeon performed measurements independently. The extent of resection was determined based on a preoperative and postoperative volumetric analysis on spoiled grass sequences. Gross total resection was defined as the absence of residual tumor on postoperative imaging. We also used the set of radioanatomic parameters retrospectively to assess correlations with postoperative outcomes. Correlations between age, sex, pathology, surgical procedure, drilling, restriction and working measurements, and EEA outcome (extent of resection, endocrine outcome, visual outcome, overall outcome, and complications) were analyzed in SPSS (version 20.0, SPSS, Inc) using χ2, Fisher exact test, and analysis of variance as appropriate, with a P < .05 considered statistically significant.
Of a total of 534 endonasal skull base operations, 40 were performed on 33 patients in the pediatric population, indicating an incidence of 7.5% of all cases (Table 1). The range of pathology encountered is depicted in Table 2. The most common pathology consisted of pituitary tumors (9 patients), either secreting (prolactin, 4 patients [10%]; growth hormone, 2 patients [5%]) or nonsecreting (3 patients [7.5%]). Craniopharyngiomas (5 patients) and juvenile nasopharyngeal angiofibromas (5 patients) were the next most common lesions encountered. There were 3 malignant neoplastic lesions consisting of 2 germinomas and 1 juvenile pilocytic astrocytoma. Posttraumatic CSF leaks and meningoencephaloceles were encountered in 4 children (10%).
There were 6 repeat surgeries (3 surgeries in 1 patient), of which 4 were staged endoscopic approaches to achieve complete resection and 2 were procedures for postoperative complications. All cases requiring staged or additional EEAs are described in detail below. There were 18 males and 15 females with ages ranging from 5 to 18 years (13.5 ± 3.2 years). To assess if there was any correlation between the development of the skull base and the success of the endoscopic procedure or postoperative complication rates, we further divided patients into 3 different age groups, as follows: <10 years (n = 7); 11 to 14 (n = 13); and 15 to 18 (n = 20). In addition, radioanatomic measurements were also performed in a fourth group of patients harboring skull base lesions and undergoing EEA, with ages between 19 and 21 (n = 12), to further analyze potential delays in development. General characteristics of the patient cohort are summarized in Table 1, based on initial symptomatology. The most common symptoms were visual field defects (13 patients, 39.4%), headache (10 patients, 30.3%), and cranial nerve deficits (6 patients, 18.2%). The average follow-up was 24.7 months, ranging from 3 to 88 months, and was available for all 33 patients.
The scope of each of the corridors and approaches described in the Methods section is depicted in Table 2 according to pathological entity. Operative data are summarized in Table 3, while the overall frequency of the different types of corridors and approaches is shown in Table 4 and Figure 1. Corridors and approaches for common pediatric skull base lesions (craniopharyngiomas, CSF leaks/meningoencephaloceles, basilar invagination, and juvenile nasopharyngeal angiofibromas) are depicted in Figures 2, 3, 4, and 5, respectively. Gross total resection (GTR) was not always the goal of surgery, which was often skull base repair, debulking, and decompression of anatomic structures or biopsy. In the 20 cases in which GTR was the intended goal of the procedure, GTR was attained in 15 (75%, Figure 6 Left). Intraoperative CSF leaks were identified in 15 patients (37.5%) by using intrathecal fluorescein often accompanied by a Valsalva maneuver. The inferior turbinate was partially resected in 16 cases (40%), with the middle and superior turbinate resected in 5 (12.5%) and 3 (7.5%) cases, respectively.
Measurements of corridors and angles of the developing skull base relevant to pediatric EEAs are summarized in Table 5 and Figure 7. The utility of each measurement in preoperative planning of specific corridors and approaches is also depicted. Patients not requiring an MRI study before surgery or patients with tumors obliterating the sinus did not have a measured set of skull base parameters, and thus were not included in the radiographic-anatomic portion of the study. Values of all parameters according to the 4 patient age groups are depicted in Table 6. Measurements were performed prospectively on 24 patients undergoing EEA and retrospectively on 83 healthy children. The most frequent pneumatization type was the postsellar type encountered in 13 patients with ages between 10 and 18 years; only 2 patients had a conchal pneumatization type, both in the <10 years age group, and 5 patients had a presellar pneumatization type, 4 of which were part of the 11 to 14 years age group, with 1 patient in the 15 to 18 years age group. One of the most important anatomic landmarks and the key limiting element for the transcavernous or transclival approach is the intercarotid distance at the level of the cavernous sinus (ICD-CS). No age-dependent growth trend could be observed in the 4 age groups. Although the ICD-CS value did not appear to increase with age, both the planum sphenoidale and the inferior sphenoid bone length seemed to increase in the 10 to 14 years and 15 to 18 year age groups. However, values for both SKB-planum sphenoidale and SKB-anterior sphenoid bone in the 19 to 21 year age group are inconsistent with this growth trend. The anterior sphenoid bone (SKB-ASB) length paradoxically decreased by more than 25% from 19.9 mm in the first age group to 15.5 mm in patients over 19 years. The length of the spheno-occipital junction had a clear and rather steep upward trend, increasing by 25% from 15.6 mm to 19.3 mm, while the anterior sellar wall (SKB-ASW) had a similar trend with an increase of approximately 40%. The sellar floor length did not have a discernible developmental trend in this patient cohort.
A second set of skull base measurements assesses working distances and anatomic restriction sites, guiding the intracranial dissection steps of EEA. These working measurements are depicted in Table 7. Table 8 offers an overview of the same set of measurements in a normal pediatric population consisting of 83 control pediatric patients without skull base pathology. Table 9 describes sphenoid pneumatization patterns in patients harboring skull base lesions. Effects of different pathological entities on the development of the cranial base can thus be analyzed. Despite the heterogeneity in skull base afflictions, the nare-sellar (NSD) and nare-dens (NDD) distances are uniformly reduced compared with the healthy population across all age groups, by as much as 12.5 mm and 23.1 mm, respectively. Furthermore, the vomer-clivus (VCD) distance and the transsphenoidal angle (TA) are 2 other measurements assessing the workspace for the EEA that are significantly reduced in patients with skull base pathology. On the other hand, the distance between the middle and inferior turbinates is increased across all age groups in comparison with the healthy pediatric population. This novel set of working measurements is also meant to aid the surgeon in choosing the best corridor and approach according to local anatomic constraints and local anatomic changes induced by the pathological process. The nare-vomer distance (NVD) and the TA have no clear growth trend across the age groups in the EEA patient series, being mainly dependent on the local pathology that distorts the normal anatomy of this region. Of note, the TA lacks a discernible developmental pattern in the healthy pediatric population as well. The NSD increases by only 7.4% from the youngest children measured to the 19 to 21 year age group in patients harboring skull base lesions, almost half of the 13% increase observed in the NSD of the healthy population.
Visual deficits improved in 58.3% of patients including 80% of patients with bitemporal hemianopsia (Table 10). Visual deficits caused by optic nerve or chiasmal compression or entrapment have an excellent response after endoscopic debulking of the mass and nerve decompression, with 7 of 12 patients showing vision improvement after the procedure. There was 1 case of transient worsening bitemporal hemianopsia following the endoscopic procedure. There were no new permanent visual deficits after surgery.
Hormone overproduction returned to normal in 9/12 patients (75%). However, preoperative hormone insufficiency only improved in 7/24 (29.2%). None of the 6 patients with primary hypothyroidism returned to their baseline. Growth hormone (GH) hypersecretion improved in 100% of cases, while GH deficiency improved in 50%. Similarly, hypocortisolemia improved in 33.3%. On the other hand, prolactin levels returned to baseline in 7/9 cases (77.8%). Panhypopituitarism was equally resilient, with none of the 2 cases having an improvement in function after surgery. One morbidly obese patient rapidly developed insulin resistance and diabetes mellitus after the excision of a nonsecreting pituitary adenoma and was placed on metformin. One 8-year-old girl with a recurrent germ cell tumor developed complete hypopituitarism after a repeat surgery. Several transient endocrine abnormalities developed after surgery: 1 GH overproduction, 1 GH deficiency, 1 hypothyroidism, and 1 luteinizing hormone/follicle-stimulating deficiency. There were 6 cases of transient diabetes insipidus (DI) and only 1 case of permanent DI. Postoperative radiotherapy was required in 1 patient with germinoma and 1 patient with prolactinoma, whereas chemotherapy was used in the ependymoma case.
In this series, there were only 2 cases of infection (5%) with no postoperative CSF leaks. Other complications, encountered in 5 patients, are provided in Table 11. Complications are depicted according to age group in Figure 6B. One patient, a 15-year-old girl, underwent endoscopic resection of a prolactinoma. She developed a postoperative intracavitary hematoma that required evacuation. She then acquired serratia marcescens meningitis and developed hydrocephalus requiring a shunt. She made a complete recovery. A second patient was a 5-year-old boy undergoing resection of a craniopharyngioma. Postoperatively he developed severe vasospasm and bilateral basal ganglia strokes from an infection around an intracerebral fat graft, which grew eikenella and prevotella. The graft was removed and the infection resolved, but he was left with a resolving hemiparesis. No surgical mortality burdened the series.
There were 2 staged and 2 recurrent surgeries. Two tumors recurred: a prolactinoma that required a second operation 3 years after the first procedure and a malignant ependymoma of the pons wrapped around the basilar artery, which recurred after initial debulking. The purposely staged surgeries were a juvenile nasopharyngeal angiofibroma that required 2 surgeries to access the intranasal and intracranial portion of the tumor owing to a large amount of blood loss in the first surgery and a Rathke cleft cyst that was inadequately fenestrated in the first surgery because of the presellar anatomic variant of the sphenoid sinus pneumatization that impeded access in the first procedure.
Prognostic Markers in Pediatric EEAs
Skull base measurements were used preoperatively to plan surgical corridors. To assess the utility of different parameters in patient selection, we then analyzed correlations of age, sex, pathology, surgical approach, and radioanatomic measurements, with the following clinical end points: extent of resection, visual outcome, endocrine outcome, overall outcome, and complication rates of EEAs (Table 12). For this purpose, we analyzed overall outcome, visual outcome, and endocrine outcome, and we separated patients into 2 subgroups: good and poor outcome. A good overall outcome was considered both an improved endocrine panel and improved visual function or complete resolution of presenting symptomatology. As we have shown, certain endocrine abnormalities are more resilient than others. However, we grouped all endocrine abnormalities for this portion of the analysis to verify if specific factors can predict endocrine outcome irrespective of pathology. When analyzing the extent of resection, only the 20 cases in which GTR was the goal of the surgery were included. For statistical power, we also grouped pathologies as either tumors or congenital malformations, including CSF leaks/meningoencephaloceles. We also combined corridors and approaches in 2 subgroups: single-corridor surgeries (transsphenoidal transsellar and transethmoidal transcribriform) and expanded and/or combined procedures. Although only certain correlations were statistically significant, measurement trends according to outcome were observed for several parameters (Table 12). Lack of statistical significance may be due to the low numbers in this cohort.
Based on these numbers, pathology did not significantly correlate with any of the analyzed end points. Single-corridor procedures correlated with better visual outcomes (P = .048, Fisher exact test). Furthermore, although it did not reach statistical significance, 80% of complications occurred in the expanded approaches. Given that, in the EEA cohort, skull base measurements were significantly different from those in the healthy population, irrespective of age group, we hypothesized that specific radioanatomic measurements rather than age would more accurately predict outcomes. As expected, in this cohort, age did not significantly correlate with overall outcome, endocrine outcome, visual outcome, or complication rate (P = .68, P = .81, P = .64, and P = .063, respectively). The shorter working distances, such as NSD and NDD, in the single-digit-age patients would imply better access to intracranial pathology in younger age groups. However, in our cohort, GTR was achieved irrespective of age group (Figure 6A; P = .97). Furthermore, based on the numbers in this cohort, GTR did not significantly correlate with improved overall outcome, endocrine outcome, or visual outcome (Fisher exact test, P = .127, P = .580, and P = .486, respectively).
Three different skull base parameters predicted the overall outcome (Table 12): SKB-posterior sellar wall (P = .013), intercarotid distance at the superior clivus (ICD-SC) (P = .003), and NDD (P = .018). Mean NDD in patients with good outcome was 7.1 mm shorter than NDD in patients with poor outcome (75.7 ± 6.1 vs 82.8 ± 5.9). Mean ICD-SC in patients with poor overall outcome was narrower by 3 mm than in patients with good outcome (17.7 mm ± 2.4 vs 20.75 ± 1.8). Furthermore, wider ICD-SC also correlated with better endocrine outcome (P = .015, Δ = 2.9 mm between the 2 outcome groups). Interestingly, sex almost approached statistical significance in predicting endocrine outcome (P = .07). In the healthy population, restriction parameters, specifically ICD-CS and TA, are significantly smaller in the youngest age groups (ICD-CS: 11 mm at 5 years compared with 14 mm at 10 years; TA: 17.7° at 5 years compared with 19.2° at 10 years; P < .001). In our patients undergoing EEA, TA at 10 years was 17.4°. Skull base pathology can disrupt sphenoid pneumatization and delay ICD and TA expansion, thus potentially hindering access in older age groups as well (Figure 7). This would imply a high risk of iatrogenic neurovascular injuries in the pediatric patients harboring aggressive skull base lesions irrespective of age. As we have shown in this clinical series, with the use of neuronavigation, Doppler, and continuous intraoperative monitoring, there is no significant difference in complication rates based on age group (Figure 6B, P = .063). We also found that, paradoxically, a wider maximum width between inferior turbinates (MaxWiT) significantly correlates with higher risk of postoperative complications (P = .025).
A major confounder in this analysis is the type of pathology. Certain tumors, known to encroach on neurovascular structures and thus impede resection, have specific age distributions. A potential bias also to be taken into account when analyzing differences in skull base measurements between the healthy cohort and patients undergoing EEA is the fact that these preoperative measurements had been part of the therapeutic decision. Measurements were performed preoperatively to assess available space, and choices of corridors were made according to these parameters. This leads to an inevitable selection bias, and the effect of skull base pathology on development should be addressed in a more rigorous prospective randomized study. Importantly, we have not had cases in which endoscopy was considered untenable owing to restricted corridors as assessed by our measurements.
To assess the role of skull base measurements in predicting the prognosis of children undergoing EEA, we used overall outcome and complications in a combined analysis. Drilling parameters SKB-ASW and SKB-posterior sellar wall (P = .022 and P = .007), restriction parameters ICD-SC and MaxWiT (P = .01 and P = .041), and working parameter NDD (P = .001) predicted a better prognosis, with better outcomes and a reduced risk of postoperative complications. Last, we analyzed the effects of cutoff values for the different measurements based on the values observed in the normal population or based on the observed growth trends, using binary logistic regression in a series of univariate analyses. ICD-SC > 19 mm correlates with better outcomes and lower complication risk (P = .019, odds ratio [OR] = 11.6, 95% confidence interval [CI] = 1.48-91.543). An NDD < 77 mm also predicts better outcomes with fewer complications because of easier access to posterior skull base structures (P = .028, OR = 0.071, 95% CI = 0.007-0.752). The limited number of patients and the fact that most skull base measurements are collinear parameters precluded a multivariate analysis of outcome predictors.
Corridors and Approaches in Pediatric vs Adult EEAs
Endoscopic approaches to the sella, parasellar area, and midline skull base are well-described and now commonly performed in the adult population.8,12,15,21,30,33,35 The nasal cavity of the adult is generally sufficiently wide to permit the passage of a standard 4-mm endoscope as well as 2 or 3 instruments. The key steps to create adequate room are a wide sphenoidotomy, posterior septectomy, and, in some circumstances, resection of the middle turbinate. In the pediatric population, however, the anatomy is more constricting and limiting and the sphenoid sinus is not always completely aerated, rendering the endonasal approaches more challenging.22,28 Thus, adoption of endoscopic skull base techniques has occurred more slowly in the pediatric population and only a few centers have published their experience.10,22,24,25 The purpose of this article was to demonstrate our results with a large series of pediatric patients in whom the EEA was utilized to manage a variety of skull base pathologies and to characterize measurements of the skull base anatomy in different age groups. We analyzed the correlation of different MRI skull base parameters with outcome and postoperative complications to more clearly define indications and limitations of EEAs in the pediatric population.
Skull base pathology and goals of surgery differ significantly between adults and children.44,45 Avoiding cosmetic deformity in the developing skull base has a higher priority in children. Therefore, decompression, debulking, and reconstructive procedures are very common in pediatric patients. Clear visualization of anatomic structures is quintessential. To this end, a binasal approach, which may require more aggressive resection of turbinates, is even more important in pediatric patients. In the pediatric population, special measures are required to ensure the safety of the procedure. Furthermore, several areas of the developing pediatric skull severely limit EEA compared with the adult patient.26,46,47 When choosing the best EEA corridor to reach lesions along the rostrocaudal midline, 2 elements have to be considered: neurovascular structures impeding access and short anatomic routes, passing through the most pneumatized areas, with minimal transgression of active growth centers. In the developing child, the optic apparatus and the pituitary stalk are structures that are extremely sensitive to thermal, electrical, and mechanical injury. Caution must be displayed when manipulating these structures during the intracranial dissection steps of EEAs.
A potential restrictive site is the nasal aperture, which may be insufficiently wide to accommodate the necessary endoscopic instrumentation. Before the age of 5, adjuvant methods are required to adequately open the corridor, such as the sublabial approach with facial degloving. However, these invasive surgical endeavors can lead to cosmetic disfigurement or facial and gum numbness. We have thus not performed endoscopic procedures in patients below the age of 5. No growth complications of the nasomaxillary complex have been observed thus far, granted that our mean follow-up time was only 26.24 months. Recent studies report similar results.22,24 Our skull base measurements suggest that skull base pathology can significantly alter and delay the developmental process. This underscores the importance of early surgical intervention using methods capable of navigating around growth centers, such as EEA. Whether resection of the pathological process is sufficient to restart and normalize the developmental process remains to be determined in prospective trials.
Outcomes and Complications
Extent of Resection
In assessing the extent of resection in our pediatric series, it is critical to understand our surgical philosophy, which varies depending on pathology. For craniopharyngiomas, avoiding damage to the hypothalamus is a priority; hence, the goal of surgery is decompression of the optic apparatus in preparation for adjuvant radiotherapy.48 Complete resection is only attempted if the hypothalamus is not involved. Similarly, goals of surgery for germinoma are biopsy and decompression only, and for fibrous dysplasia, decompression of the optic apparatus. Chondrosarcomas invading the cavernous sinus respond well to radiation and the morbidity of complete resection is quite high in this area. Juvenile angiofibromas are hormone sensitive49 and can resolve after puberty50; hence, radical yet safe near-total resection is often the goal. For pituitary tumors, on the other hand, a GTR is generally the goal of surgery, assuming that the lateral cavernous sinus is not invaded. Hence, GTR is not always the goal of surgery, and our rate of GTR should be analyzed in this light.
Endocrine and Vision Outcomes
In our pediatric series, neither GTR nor age significantly correlates with an improved endocrine or vision outcome. We attribute this finding to our conservative goals, which emphasize decompression for symptom resolution depending on the pathology. In this cohort, 77.7% of hyperprolactinemias and 100% of GH overproduction cases had return to baseline following EEA. Hypothyroidism and panhypopituitarism were particularly recalcitrant to tumor decompression. On the other hand, the optical apparatus has a much higher plasticity, with decompression resulting in impressive vision improvement and, frequently, complete recovery of the entire visual field. Our results support similar outcomes reported by other groups.24,25,51
DI, hypopituitarism, and other endocrine abnormalities, such as increased weight gain, are common complications following pediatric endoscopic skull base procedures.52 In our series, most patients experienced only transient postoperative DI (83.4%, 5 of 6 cases), compared with the significantly higher rates of persistent DI encountered in the literature.24 Chivukula et al24 reported a 68.8% rate of permanent DI in craniopharyngioma surgeries and 8.3% in patients with Rathke cleft cyst, with an overall rate of 60% (12 of 20 cases). Furthermore, only 1 patient in our series, with an aggressive germinoma infiltrating the pituitary stalk, developed panhypopituitarism.
We did not encounter any CSF leaks in our pediatric series. In a 27-patient series, Locatelli et al reported 3 cases of CSF leaks (11.1%) that required LD placement or second-look endoscopic surgeries for complete closure.51 Chivukula et al24 reported a 10.5% incidence of CSF leaks in their 133-patient series. Other pediatric endoscopic skull base series reported leak rates of 8 to 13%.6,27 We use several techniques that are unique to our center. The first is the liberal use of intrathecal fluorescein. Since successful closure of CSF leaks starts with their identification, this adjunct may be helpful in lowering postoperative leak rates. Second, when a large intraoperative CSF leak is anticipated, such as with intradural tumors, we place a lumbar drain and use postoperative drainage for at least 1 day. Finally, we have developed a technique called the “gasket-seal” that we use to close intraoperative CSF leaks in patients with intradural tumors.42,43
The rate of infection in most large series of adult EEA is extremely low, in general, <1%.53,54 However, in our pediatric series, we have noticed a slightly higher rate of infection (2 patients, 5%). This infection rate is similar to that reported in another recent pediatric series.24 The 2 patients were 5 and 15 years old, respectively, and both underwent extended transsphenoidal transplanum approaches, one for a craniopharyngioma and the other for a pituitary adenoma. Hence, neither age nor pathology was a significant risk factor for infection. Both patients had intraoperative visible CSF leaks. Interestingly, both skull base defects were closed with an intracavitary fat graft, known to be a nidus for infection.17 Pediatric nasal bacteria may be different and adjustment of the preoperative antibiotic regimen might be required for pediatric patients.55 Likewise, passing a large fat graft through narrow nasal passages may drag bacteria into the intracranial space. As a result of these cases, we now use a nasal speculum when introducing fat grafts through the nares and also avoid fat altogether in all intra-arachnoidal surgeries. Further studies are needed, however, to clearly establish the risk factors for post-EEA infectious complications in children.
Previously defined MRI measurements26 have been used to assess pneumatization patterns and local anatomy of the sphenoid sinus.56 We have also developed a new system of MRI skull base parameters to plan safe surgical trajectories by assessing working space, anatomic restriction sites, as well as distances to specific skull base targets. The literature suggests an intercarotid distance less than 10 mm to be an absolute contraindication to EEA.57,58 In our measurements, ICD was beyond this limiting threshold in all age groups, > 5 years of age. Drilling MRI parameters also show that the sellar region is far more expanded in children harboring skull base lesions than in the healthy pediatric population (Table 6, Figure 7). Pituitary pathology, suprasellar masses, or even parasellar lesions significantly distort local anatomy, enlarging the sellar floor and thereby actually facilitating extended endoscopic approaches.
Expanding and eroding lesions affect local anatomy and impede or delay the normal development of the growing skull base. The maximal width between the inferior turbinates is increased in the pediatric population bearing skull base lesions, providing easier access. Interestingly, a wider MaxWiT also correlates with increased risk of postoperative complications, potentially due to altered local anatomy. In accordance with our measurements, the flexible cartilage of the nasal aperture as well as the middle and inferior turbinates did not pose significant problems. We rarely completely resected the middle turbinate (5 cases), with simple lateralization offering sufficient space. Importantly, skull base lesions delaying the developmental process significantly attenuated age-dependent differences (Table 7 vs Table 8) and cancelled the pneumatization-dependent growth trends of the sellar region (Table 6). In the axial plane, the skull base pathology can directly impact the working space regardless of age group. The TA establishes the lateral limits of the transsphenoidal approach accessing parasellar lesions. The NVD and VCD distances guide trajectories accessing pathological entities in the anterior or posterior extremities of the cranial base. However, these axial measurements cannot be predicted based on age. This underscores the importance of radioanatomic measurements in planning surgical trajectory before surgery by assessing local anatomy potentially distorted by the neoplastic process.
A variety of approaches hinged on the transsphenoidal corridor allowed us to safely and effectively access different types of tumors and lesions in this case series. The transsphenoidal route offers a versatile and safe corridor, allowing access to the sellar and parasellar regions that can be further extended along the midline or laterally, as needed. Pneumatization of the sphenoid sinus is a gradual, asymmetric process. It starts late, at about 2 years, and progresses slowly. It has been suggested that the conchal or presellar pneumatization types preclude the use of the transsphenoidal transplanum approach, particularly for craniopharyngiomas.19 In such cases, we found that drilling is feasible and is mostly done into immature, heavy vascularized bone. Careful hemostasis during the drilling step using Gelfoam or bone wax can mitigate this obstacle. We do not consider pneumatization types to be absolute contraindications for EEA in children, irrespective of corridor. Pneumatization largely progresses in a lateral direction, thus not significantly modifying the effective drilling distance. As pneumatization progresses, the width of the sellar floor also increases, opening up new endoscopic corridors for parasellar lesions. Indeed, the majority of our expanded EEAs were performed in older children (Table 2).
On the other hand, several groups59 have emphasized the role of sphenoid sinus pneumatization in shaping the spatial anatomic relationships along the skull base, thereby changing restriction parameters. With incomplete pneumatization, the neurosurgeon cannot rely on the usual anatomic landmarks used for skull base EEA in adults. Using thorough preoperative MRI measurements of the skull base anatomy as well as intraoperative neuronavigation, we were able to safely circumvent this limitation. Moreover, TA seems to be directly affected by skull base pathology, a narrower working space being observed in patients undergoing EEA. Despite these findings, we did not encounter any difficulties in accessing intracavernous or clival lesions irrespective of age or pathology, nor did we have any major vascular complications related to internal carotid artery injury. ICD was not significantly different in patients with postoperative complications. Intraoperative Doppler can help overcome the tighter intercarotid corridor. Furthermore, the pneumatization process drives the entire developmental process and can directly impact working parameters.56 Most patients with postoperative complications had longer working distances; mean NDD was 4.8 mm longer and NVD was 7.2 mm longer in patients with postoperative complications. Longer working parameters in conjunction with the restricted pediatric anatomy lead to tedious and long dissection steps, increasing the risk of postoperative complications. Overall, development of the pediatric skull base directly impacts EEA outcomes and prognosis in children with skull base lesions. Furthermore, when analyzing the risk of postoperative complications, age should also be taken into account despite the even distribution across age groups in our cohort. We have encountered a wide variety of anatomic variants of the posterior-superior skull base. Therefore, thorough preoperative MRI measurements of this restriction area can readily aid the neurosurgeon in choosing the best approach and should be considered in pediatric EEAs.
Our skull base measurements were primarily used preoperatively to plan surgical trajectory. We also retrospectively analyzed the prognostic role of different skull base measurements and found that certain parameters can also predict outcome of EEAs. Closer intracranial targets with shorter working distances along with wider intercarotid corridors and restriction parameters predict better postoperative outcomes. A wide ICD-SC allows for better visualization, dissection, and decompression, thus correlating with improved endocrine outcomes irrespective of hormone imbalance or pathology. On the other hand, the need for expanded approaches indicates a risk of poor visual outcome, potentially due to the extensive manipulation of the sensitive optic apparatus. Overall, EEA in the pediatric population can be a useful tool in accessing a variety of skull base lesions as long as the advantages and risks are well balanced. To this end, MRI-based skull base measurements can be an important adjunct in perioperative decision making, not only guiding surgical trajectory, but also predicting prognosis.
An important limiting factor of our study is selection bias. Only certain cases considered amenable to endoscopic resection were selected and are thus included in this analysis. Although strict selection criteria definitely lead to improved outcomes, certain complex cases with invasive lesions or facial deformities were not included because alternative treatment options such as open craniotomy were necessary. Adequate radioanatomic measurements and proper preoperative planning based on pathology type and location can help the neurosurgeon select only those candidates that will benefit from the surgery with minimal risks and complications. Furthermore, adjuvant operative methods such as neuronavigation, Doppler, and fluorescein staining of CSF add to the level of safety by guiding the drilling trajectory. The low numbers of specific pathologies, such as malignant neoplastic lesions, also represent an important limitation of our study. Pediatric skull base pathology, whether benign or malignant, is rare. These low numbers cannot generate the necessary statistical power and thus significantly affect the statistical analysis of outcomes based on pathology type and skull base measurements. The heterogeneity of skull base pathology further hinders statistical analysis of outcomes in this patient cohort, making extrapolations difficult. The retrospective nature of the study leads to inevitable biases that should be considered when analyzing the outcomes and conclusions of this report.
In this article, we show the utility of endonasal endoscopic skull base approaches in the pediatric population. These approaches have proliferated more quickly in the adult population likely because of the assumption of limited access provided by the smaller nasal sinuses. Through collaboration between our pediatric neurosurgery service and adult endonasal endoscopic skull base service, we have shown the applicability of these approaches in the pediatric patient. MRI-based radioanatomic measurements can be used to guide the trajectory according to the skull base developmental stage for a safe navigation around growth centers and can potentially predict outcomes, being a useful preoperative study. Appropriate selection of patients and surgical trajectory based on the pathology-location-corridor paradigm can lead to successful endoscopic procedures for a wide variety of skull base lesions, irrespective of location or age group, in children older than 5 years of age.
The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.
We would like to thank Thomas Graves for excellent assistance with the schematic drawings of the endoscopic corridors and approaches.
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This paper describes outcomes in 33 pediatric patients (< 18 years old) who underwent 40 endonasal, endoscopic approaches (EEA) for a variety of skull base pathologies. They also describe a battery of MRI-based anatomical measurements that can be used to help improve outcomes from EEA in this patient population. The authors clearly outline the specific challenges of EEA in the pediatric age group and explain why this has limited the application of these approaches in children. They also provide a number of helpful suggestions on how these specific challenges can be handled to achieve excellent results with low complication rates.
The most novel contribution, and the main focus of the article, involves a battery of MRI-based anatomical measurements that can be performed pre-op and used to help in surgical planning. They are arranged in 3 groups: working distances, restriction areas, and drilling parameters. They found that 5 parameters predicted better prognosis (ie, better overall outcome and reduced complication): the length of the anterior and posterior sellar walls, the minimum intercarotid distance at the cavernous sinus, the maximum width between the inferior turbinates, and the nare dens distance. Given that the number of comparisons was larger and the number of patients was relatively small, we probably shouldn't read too much into the statistical significance of the data as it relates to each of the measurements. But they do provide evidence that these spatial relationships can have a concrete impact the outcome of surgery. Perhaps more importantly, they can alert the surgeons to potential pitfalls in a particular case that can then receive increased attention at the time of surgery (eg, increased use of Doppler in patients with small intercarotid distances). Whether one ultimately decides to use all of these measurements in every case, the overall gestalt of the information seems to be quite useful. It is interesting to note that the authors did not exclude any patient from EEA based on the measurements themselves. Therefore, there were no specific measurements that were “deal-breakers” for EEA. However, the authors report that a number of patients with skull base pathology underwent open skull base approaches over the duration of the study. One wonders if any of those were excluded based on spatial anatomical limitations that were just so obvious that no measurements were needed. The authors also provide some intriguing data comparing anatomical measurements in 83 controls to the patients in this study. They suggest that the presence of skull base pathologies may affect development of the skull base with disrupted pneumatization of the sphenoid sinus and delayed expansion of the intercarotid distance and the transphenoidal angle. Although potentially impaired by selection bias (again, we don't know the measurements in patients with skull base lesions who underwent open surgery), these findings definitely identify a need for future studies to address this possibility.
The results for outcome and complication data are fairly strait-forward and standard. However, they are still important given the paucity of data on EEA in the pediatric population. In addition, there are a number of “pearls” interspersed throughout the report on specific techniques that the authors have developed over the years to maximize resection and minimize complications that are quite helpful.
In conclusion, this paper provides important information on the challenges of EEA in children and shows how they can be successfully addressed to ensure excellent outcomes and low complication rates. They also identify specific spatial relationships that can impact prognosis from this type of surgery. And they provide helpful information on the types skull base of pathologies that occur in children and intriguing data on how those pathologies may affect development of the skull. This paper will be of great interest to anyone who treats skull base lesions in children and may help foster the increased use of powerful endoscopic techniques in this age group.
Steven N. Roper
The authors have analyzed standard and novel anatomic parameters in pediatric patients undergoing endonasal endoscopic surgery for a variety of skull base pathology. Half of the 40 patients were younger than 14 at the time of surgery and 7 were younger than 10 years of age. 40% of patients underwent partial inferior turbinate resection and 12.5% required partial middle turbinectomy. The authors reported good outcomes with low morbidity. In spite of the pediatric population, only 2 of the 7 patients under the age of 10 had a conchal-type sphenoid sinus. Anatomical measurements that correlate with a shorter and wider working distance were associated with improved outcomes. This manuscript emphasizes the importance of adequate exposure in producing good outcomes. These data support the use of endoscopy in the pediatric population and further delineates those who will benefit most from these techniques.
John A. Jane, Jr
In this report the authors describe their experience with use of the endonasal endoscopic approach in 33 pediatric patients aged 5 to 18 years with a wide range of skull base pathology, including 9 with pituitary adenomas. While their report suggests that patient size per se is not a limitation to this approach, a wider intra-carotid distance and shorter nare-dens distance did predict better outcomes and fewer complications. This report adds to a growing body of literature confirming the safety and efficacy of the endoscopic technique for parasellar and other skull base lesions even in younger patients, provided it is performed by an experienced multidisciplinary team using essential instrumentation and neuro-navigation techniques.
Santa Monica, California
Anatomical measurements; Complications: endonasal endoscopic surgery; Pediatric neurosurgery; Pediatric skull base pathology; Visual and endocrine outcome
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