Liu 2017
Liu 2017
O p e n A p p ro a c h e s i n t h e
M a n a g e m e n t o f S i n o n a s a l an d
Ven t r a l Sk u l l B a s e M a l i g n a n c i e s
James K. Liu, MDa,b,*, Anni Wong, MS
c,d
,
Jean Anderson Eloy, MDe,f,g,h
KEYWORDS
Skull base malignancy Skull base defect Skull base surgery
Sinonasal malignancy Endoscopic endonasal surgery Craniotomy Transbasal
Nasoseptal flap
KEY POINTS
The use of combined transcranial and endoscopic endonasal approaches or so-called
cranionasal approaches to the anterior ventral skull base and paranasal sinuses remain
an important option in the surgical treatment of sinonasal and ventral skull base
malignancies.
The modified 1-piece extended transbasal approach provides wide panoramic exposure
to tumor that invades the frontal lobes, orbital roofs, and cribriform plate without using a
transfacial incision or orbital bar removal.
Continued
Continued
The endoscopic endonasal approach can be combined with the transbasal approach for
secondary inspection from below after tumor removal from the transcranial exposure,
further resection of tumor within the sinonasal cavity, and reconstruction with a vascular-
ized pedicled nasoseptal flap, if needed.
Skull base reconstruction can be performed using a simultaneous pericranial flap from
above and a nasoseptal flap from below (double flap), especially when postoperative
adjuvant radiation therapy is anticipated.
Abbreviations
CTA Computed tomography angiography
EEA Endoscopic endonasal approach
CSF Cerebrospinal fluid
INTRODUCTION
Since the conception of the bifrontal craniotomy by Frazier in 1913,1 Derome2 and
Tessier and colleagues3 popularized the transbasal approach to the anterior ventral
skull base. Numerous modifications of the transbasal approach have been developed,
each adding varying degrees of bone removal of the supraorbital bar, orbital roof and
wall, lateral orbital rims, nasal bones, and paranasal sinuses (frontal, ethmoid, and
sphenoid sinuses). In 1988, Raveh and Vuillemin,4,5 described the subcranial
approach for the removal of fronto-orbital and anteroposterior skull base tumors,
which entailed nasal and orbital osteotomies and minimal frontal lobe retraction. In
1991, Kawakami and colleagues,6 presented the extensive transbasal approach, per-
forming en bloc bilateral orbital roof and frontal sinus osteotomy. This allowed for ac-
cess to tumors extending laterally into the anterior cranial fossa. Sekhar and
colleagues7 discussed the extended frontal approach in 1992, which added an orbito-
frontal or orbitofrontoethmoidal osteotomy. These transbasal modifications have
allowed for increased posterior and inferior surgical view toward the clivus with less
frontal lobe retraction. These midline subfrontal approaches to the anterior ventral
skull base and paranasal sinuses remain critical in the treatment of anterior ventral
skull base and sinonasal malignancies.
In the past decade the role of the pure endoscopic endonasal approach (EEA) has
gained increasing popularity, driven by continuous advances in endoscopic instru-
mentation, intraoperative image guidance, and surgical technique. Resections with
negative margins via a purely EEA have been successfully performed for tumors
confined to the nasal cavity and paranasal sinuses with radiologic evidence of normal
cribriform plate and upper ethmoid sinuses.8
However, limitations of the pure EEA arise when there is significant intracranial
extension or considerable extension beyond the lamina papyracea.8,9 For instance,
when en bloc resection of the tumor including the cribriform plate is necessary, it
may be best accomplished with an anterior craniotomy.8,10 Thus, open approaches
remain an integral component in our surgical armamentarium. In the bifrontal trans-
basal approach, one can access the cribriform plate and perform a total ethmoidec-
tomy, sphenoidotomy, and midline clivectomy down to the craniovertebral junction.
Traditionally, the transbasal approach was often combined with a transfacial approach
(combined craniofacial approaches) to treat a vast majority of sinonasal skull base ma-
lignancies. This combined approach allowed for access to tumors residing beneath
the orbit in the superolateral aspect of the maxillary sinus, where the bifrontal
Management of Ventral Skull Base Malignancies 333
approach alone was restricted from.11 Although the transfacial approach provides
ample exposure for complete tumor removal, it often involved rather invasive tech-
niques, including extensive facial incisions, facial disassembly, lateral rhinotomy, mid-
facial degloving, and/or facial osteotomies, leaving displeasing cosmetic results.11,12
Infectious complications or inadequate healing may lead to malunion of bones or loss
of grafts, resulting in unsightly scars and disfigurement.12 Additionally, compared with
craniofacial resection, transnasal endoscopic resection of anterior ventral skull base
tumors has been demonstrated to be associated with decreased hospital and inten-
sive care unit (ICU) stay, decreased estimated blood loss, and faster recovery.13–15
Subsequently, the EEA has become a more favorable adjunct (endoscopic-assisted
craniofacial approaches or cranionasal approaches) due to its superior panoramic
visualization, illumination, and avoidance of transfacial skin incisions.11 In this article,
we discuss the role of combined transcranial and EEA approaches (combined cranio-
nasal approach) in the surgical management of ventral skull base malignancies
(Figs. 1–3).
With the advent of skull base endoscopy, the EEA and its extended variations have
changed the paradigm by which ventral skull base lesions are treated. In recent years,
the surgical landscape of endoscopic skull base surgery has evolved as this anatomic
territory became better understood. By taking advantage of the natural anatomic cor-
ridors, such as the transnasal, transsphenoidal, transethmoidal, and transmaxillary
corridors, structures from the clivus to the Meckel cave to the pterygopalatine fossa
are now accessible without external incisions.11,16–18 The versatility of EEA has
increased minimally invasive surgical access to the ventral skull base dramatically.
In our practice, most sinonasal and anterior ventral skull base malignancies are treated
with a purely endoscopic endonasal transcribriform approach. However, if one is to
choose a transbasal approach from above, this can be used in conjunction with a
complementary EEA from below to treat large lesions involving multiple anatomic
compartments (see Figs. 1–3). The transbasal approach provides exposure from
the third ventricle to the base of the clivus with relatively limited frontal lobe retrac-
tion.19 In the past, such lesions were traditionally treated with extended transbasal ap-
proaches combined with open transfacial approaches involving facial skin incisions
and facial osteotomies. Because the extended EEAs provide wide panoramic access
and visualization to the ventral skull base in the sagittal and coronal planes, the tradi-
tional transfacial approaches have gradually fallen out of favor and use. From a trans-
cranial approach, the anterior nasal cavity and superolateral regions of the maxillary
sinus are difficult to visualize (blind spots). However, the EEA allows excellent visual-
ization and access to the entire paranasal sinuses, including these blind spots, partic-
ularly with angled endoscopy. Through this synergistic combined approach, the
surgeon can work from above to control and remove intracranial tumor, and also
from “below” to control tumor in the sinonasal cavity. A combined approach also
can be used from a reconstruction strategy because the EEA can provide an additional
vascularized pedicled nasoseptal flap, if needed. This may be useful in cases in which
the pericranial flap is compromised from prior craniotomies, or needs to be supple-
mented from below. Alternatively, the pericranial flap can serve as the primary source
of vascularized reconstruction if the nasoseptal flap is compromised or invaded by a
sinonasal malignancy.
carotid artery, and extensive dural and brain parenchymal involvement. In these in-
stances, the addition of a transfacial or transcranial approach is warranted for optimal
resection of the malignancy.18,21 Thus, it is important to maintain the open approaches
in the surgical repertoire for various indications.
PREOPERATIVE CONSIDERATIONS
Preoperative MRI is essential to assess the tumor and to check for intracranial exten-
sion. Computed tomography angiography (CTA) is useful to assess the anatomy of the
anterior and posterior arterial circulation relative to the tumor, to rule out any vascular
encasement, and to study the neighboring venous anatomy, including the cavernous
sinus, petrosal sinuses, and any large draining veins. CTA is preferred over magnetic
resonance angiography, as it also shows the bony anatomy of the skull base in high
resolution. Digital subtraction angiography is reserved for complicated vascular anat-
omy not adequately assessed on CTA or for balloon test occlusion in cases of signif-
icant arterial encasement. In patients with sellar and suprasellar tumor involvement,
baseline pituitary function should be assessed with appropriate endocrine testing. It
is important to obtain formal baseline neuro-ophthalmological testing for patients
who present with visual disturbances due to optic nerve and/or orbital involvement.
SURGICAL TECHNIQUE
Patient Positioning
After general endotracheal anesthesia and appropriate arterial and venous access is
obtained, the patient is positioned supine and the head placed in 3-pin fixation
(Fig. 4). The bed is flexed 10 to 15 to facilitate venous drainage. The neck is slightly
extended to promote frontal lobe relaxation away from the anterior ventral skull base
and to reduce the need for brain retraction.
Neuronavigation can be useful and can be used to plan the craniotomy and verify
anatomic landmarks. Neurophysiologic monitoring of somatosensory and motor
evoked potentials are performed. Additional neurophysiologic monitoring modalities
can be used as needed depending on the location of the tumor. Antibiotics, mannitol,
decadron, and antiepileptics are administered before skin incision.
Skin Incision
A preauricular bicoronal skin incision is planned behind the patient’s hairline that ex-
tends from one zygoma to the other, no more than 1 cm anterior to the tragus
(see Fig. 4). The nose and nares are also prepped, in case endoscopic endonasal
Fig. 4. (A, B) For a combined cranionasal approach, the patient is positioned supine with the
head in 3-pin fixation. A standard bicoronal incision is used.
Management of Ventral Skull Base Malignancies 337
corridor. Care is taken to avoid compromise of any bridging veins so as to avoid a venous
infarct. The intradural portion of the tumor is removed with care to create a plane to sepa-
rate the frontal lobes from the tumor capsule (Fig. 6A–C). Solid and firm tumors can be
debulked with an ultrasonic aspirator, whereas hemorrhagic and friable tumor may need
to be removed in a piecemeal fashion suctions and bipolar cautery. After tumor removal,
the frontal lobes are inspected and frozen sections are sent for margins.
Before entering the sinonasal cavity via the cribriform plate, the dura can be closed
in a watertight fashion with a dural patch graft (Fig. 6D). The remainder of the extra-
dural tumor can be removed and access to the clivus can be achieved through the
transcribriform corridor microsurgically (Fig. 6E, F). The cribriform plate and crista galli
are drilled off to expose the anterior and posterior ethmoid sinuses and lamina papy-
racea. The anterior and posterior ethmoidal arteries and coagulated and divided
sharply. Care is taken to avoid retraction of an incompletely coagulated ethmoidal ar-
tery back into the globe to avoid an orbital hematoma. Removal of the planum sphe-
noidale posteriorly provides exposure of the sphenoid sinus. Both optic canals are
identified posterolaterally within the sphenoid sinus. Bilateral bony prominences
formed by the cavernous segment of the internal carotid arteries are identified on
either side of the sella. The sphenoid sinus can be widened, and the sellar floor can
be removed if access to the clivus is needed. Exposure of both maxillary sinuses
can also be achieved. However, visualization to the anterior nasal cavity and supero-
lateral aspect of the maxillary sinus is limited from above (blind spots).11 Thus, further
inspection for remaining tumor from below via an EEA is performed. Endoscopic
debulking of the intranasal portion of the lesion also can be performed if necessary.21
It is important to preserve the nasal septum and mucosa during the tumor removal, in
case a nasoseptal flap is needed for reconstruction (see later in this article).
Reconstruction
The large skull base defects and communication with the nasal sinuses present a
unique challenge in reconstruction. Although endonasal repair of smaller skull base
defects with fascial or mucosal grafts in conjunction with tissue sealants have been
successful in preventing cerebrospinal fluid (CSF) leaks, its adequacy for endonasal
reconstruction of major skull base and dural defects is of debate.13,20,26 Vascularized
tissue is optimal for reconstruction with goals of separation of the intracranial
compartment from the sinonasal cavity and prevention of postoperative CSF leakage.
Additionally, vascularized flaps promote rapid and complete healing.26–28 Pericranium
is a commonly used vascularized tissue flap that is readily available with a bicoronal
incision. Undermining beneath the incision posteriorly provides several additional cen-
timeters of pericranium for increased surface area of coverage. It is important to
attempt watertight closure of durotomies and dural defects, if possible, before place-
ment of the pericranial flap. We typically suture a dural patch using acellular dermal
allograft at the cribriform dural defect of the anterior ventral skull base. Endoscopic
endonasal inspection of the skull base reconstruction from below can be very useful
in ensuring an adequate pericranial flap reconstruction to prevent CSF leakage. This
strategy can allow an endoscopic-assisted repair with direct visualization of the ante-
rior ventral skull base repair and optimal positioning of the pericranial flap.
If postoperative radiation therapy is anticipated, particularly for sinonasal skull base
malignancies, one can consider using a “double-flap” technique in which a pericranial
flap is simultaneously used with a nasoseptal flap (Figs. 7 and 8).29 The 2 flaps can
complement each other at their respective areas of weakness. The pericranial flap
is strongest anteriorly at the region of the frontal sinus and cribriform plate, whereas
the nasoseptal flap is strongest at the area of the clivus defect. When used together,
these 2 vascularized tissue flaps can provide optimal skull base reconstruction in
select cases that are at high risk of postoperative CSF leakage.
In some instances, a vascularized pedicled nasoseptal flap may be used as a
salvage strategy if the pericranial flap is unavailable due to prior usage in revision cra-
niotomies.27 This durable yet pliable flap is robustly vascularized by the posterior
nasoseptal arteries arising from the sphenopalatine artery. Its large surface area
and superior rotational arc allow for flexibility in flap design, contributing to its high
POSTOPERATIVE MANAGEMENT
DISCUSSION
Traditionally, extensive malignant tumors of the paranasal sinuses and ventral skull
base have been surgically managed via a transcranial-transfacial (combined craniofa-
cial) approach and postoperative radiotherapy with satisfactory success. However,
craniofacial resection is associated with significant perioperative morbidity, mortality,
and complications.8,13,34 These limitations prompted the search for safer and
improved methods for the surgical management of extensive paranasal sinus and
anterior ventral skull base malignancies, which would improve the patient’s function-
ality and quality of life with satisfactory cosmetic results while preserving oncological
principles. Advancing developments in endoscopic surgical technology, refinements
in endoscopic techniques, and increased familiarity of the endoscopic endonasal
anatomy have allowed the EEA to transcend its expected uses, where its applicability
has expanded from its initial use for the treatment of inflammatory paranasal sinus dis-
ease to resection of benign sinonasal neoplasms,9,35,36 and ultimately to resection of
malignant neoplasms, including those of the ventral skull base.21,37,38 In tumors with
significant intracranial extension that is not amenable to a pure EEA, a combined
transcranial/EEA (combined cranionasal approach) can be performed.8,10,12,37,39
Management of Ventral Skull Base Malignancies 343
In 1997, Yuen and colleagues39 first described the combined transcranial and endo-
scopic transnasal approach for the resection of an esthesioneuroblastoma that infil-
trated the ethmoidal cribriform plate and their subsequent experience with the
implementation of the approach in a series of esthesioneuroblastomas that do not
require free-flap reconstruction, demonstrating complete tumor removal with no local
recurrences.40 Carrau and colleagues,12 demonstrated that endoscopic-assisted sur-
gery in the treatment of juvenile angiofibromas, was a suitable complement to the
traditional approaches, thus avoiding additional transfacial incisions. In the pediatric
population, this was of particular importance, as it avoided additional interference
with developing facial growth centers and minimized functional and cosmetic deficits.
Castelnuovo and colleagues41 also described the combined cranionasal approach for
en bloc resection of malignant neoplasms with minimal disturbance to the facial skel-
eton. These advantages were similarly echoed by Galassi and colleagues,42 in their
report of the combined cranionasal approach for the resection of infantile myofibroma-
tosis of the ethmoid and anterior ventral skull base. Although most studies have
focused mainly on specific neoplasms, Hanna and colleagues20 reported the use of
the combined cranionasal approach to a wide range of malignant tumors of the sino-
nasal tract. Their study demonstrated that there was no significant difference in
disease-specific or overall survival rate between groups of patients surgically treated
exclusively via EEA and those treated via combined cranionasal approach. This is
probably due to appropriate patient selection for each approach strategy. For
example, smaller, less extensive tumors were selected for EEA, and larger tumors
with significant intracranial extension were selected for a cranionasal approach.
It is important to emphasize that the combined cranionasal approach should be per-
formed only in specialized centers with an experienced skull base team consisting of
an endoscopic/skull base–trained otolaryngologist and neurosurgeon to ensure
optimal success of the operation. When managing malignancies, definitive resection
should, whenever possible, result in complete oncologic removal with tumor-free sur-
gical margins regardless of the approach, as principles of surgical oncology should be
upheld. Although surgery is the mainstay of treatment of most sinonasal and ventral
skull base malignancies, the use of adjuvant or neoadjuvant therapy when appropriate
is critical to achieving optimal oncologic outcomes.20 Advancements in microsurgical
and endoscopic skull base techniques have further added to the armamentarium of
surgical management of sinonasal and ventral skull base malignancies in both the
resection and reconstruction process. The EEA has made great strides in the manage-
ment of anterior ventral skull base malignancies and has consistently yielded good
oncologic outcomes in well-selected patients. When used in conjunction with the
transcranial approach, the combined cranionasal approach is a suitable option in
those with significant intracranial disease, to improve tumor resection and skull
base repair.20 The surgical treatment of sinonasal and ventral skull base malignancies
has evolved to be one of integrated collaboration between the otolaryngologist and
neurosurgeon, necessitating their combined advanced technical expertise and
knowledge.
SUMMARY
Combined transcranial and EEA approaches remain useful in the treatment of sino-
nasal and ventral skull base malignancies. The modified 1-piece extended transbasal
approach provides wide access to the anterior ventral skull base and paranasal
sinuses. The endoscopic endonasal approach has largely replaced transfacial ap-
proaches for combined craniofacial approaches and also can provide additional
344 Liu et al
vascularized tissue for skull base reconstruction, if needed, via the nasoseptal flap.
Double-flap reconstruction with simultaneous vascularized pericranial and nasoseptal
flaps is a useful strategy for malignant tumors that require postoperative adjuvant ra-
diation therapy.
REFERENCES
1. Frazier CH. I. An approach to the hypophysis through the anterior cranial fossa.
Ann Surg 1913;57:145–50.
2. Derome P. Spheno-ethmoidal tumors. Possibilities for exeresis and surgical
repair. Neurochirurgie 1972;18(Suppl 1):1–164 [in French].
3. Tessier P, Guiot G, Rougerie J, et al. Cranio-naso-orbito-facial osteotomies.
Hypertelorism. Ann Chir Plast 1967;12:103–18 [in French].
4. Raveh J, Vuillemin T. Advantages of an additional subcranial approach in the
correction of craniofacial deformities. J Craniomaxillofac Surg 1988;16:350–8.
5. Raveh J, Vuillemin T. Subcranial-supraorbital and temporal approach for tumor
resection. J Craniofac Surg 1990;1:53–9.
6. Kawakami K, Yamanouchi Y, Kubota C, et al. An extensive transbasal approach
to frontal skull-base tumors. Technical note. J Neurosurg 1991;74:1011–3.
7. Sekhar LN, Nanda A, Sen CN, et al. The extended frontal approach to tumors of
the anterior, middle, and posterior skull base. J Neurosurg 1992;76:198–206.
8. Komotar RJ, Starke RM, Raper DM, et al. Endoscopic endonasal compared with
anterior craniofacial and combined cranionasal resection of esthesioneuroblasto-
mas. World Neurosurg 2013;80:148–59.
9. Liu JK, Husain Q, Kanumuri V, et al. Endoscopic graduated multiangle, multicor-
ridor resection of juvenile nasopharyngeal angiofibroma: an individualized,
tailored, multicorridor skull base approach. J Neurosurg 2016;124:1328–38.
10. Devaiah AK, Larsen C, Tawfik O, et al. Esthesioneuroblastoma: endoscopic nasal
and anterior craniotomy resection. Laryngoscope 2003;113:2086–90.
11. Liu JK, Decker D, Schaefer SD, et al. Zones of approach for craniofacial resec-
tion: minimizing facial incisions for resection of anterior cranial base and para-
nasal sinus tumors. Neurosurgery 2003;53:1126–35 [discussion: 1135–7].
12. Carrau RL, Snyderman CH, Kassam AB, et al. Endoscopic and endoscopic-
assisted surgery for juvenile angiofibroma. Laryngoscope 2001;111:483–7.
13. Eloy JA, Vivero RJ, Hoang K, et al. Comparison of transnasal endoscopic and
open craniofacial resection for malignant tumors of the anterior skull base. Laryn-
goscope 2009;119:834–40.
14. Belli E, Rendine G, Mazzone N. Malignant ethmoidal neoplasms: a cranionasal
endoscopy approach. J Craniofac Surg 2009;20:1240–4.
15. Wood JW, Eloy JA, Vivero RJ, et al. Efficacy of transnasal endoscopic resection
for malignant anterior skull-base tumors. Int Forum Allergy Rhinol 2012;2:487–95.
16. Hosemann W, Schroeder HW. Comprehensive review on rhino-neurosurgery.
GMS Curr Top Otorhinolaryngol head Neck Surg 2015;14:Doc01.
17. Zacharia BE, Romero FR, Rapoport SK, et al. Endoscopic endonasal manage-
ment of metastatic lesions of the anterior skull base: case series and literature re-
view. World Neurosurg 2015;84:1267–77.
18. Su SY, Kupferman ME, DeMonte F, et al. Endoscopic resection of sinonasal can-
cers. Curr Oncol Rep 2014;16:369.
19. Terasaka S, Day JD, Fukushima T. Extended transbasal approach: anatomy, tech-
nique, and indications. Skull Base Surg 1999;9:177–84.
Management of Ventral Skull Base Malignancies 345
38. Casiano RR, Numa WA, Falquez AM. Endoscopic resection of esthesioneuroblas-
toma. Am J Rhinol 2001;15:271–9.
39. Yuen AP, Fung CF, Hung KN. Endoscopic cranionasal resection of anterior skull
base tumor. Am J Otolaryngol 1997;18:431–3.
40. Yuen AP, Fan YW, Fung CF, et al. Endoscopic-assisted cranionasal resection of
olfactory neuroblastoma. Head Neck 2005;27:488–93.
41. Castelnuovo P, Battaglia P, Locatelli D, et al. Endonasal micro-endoscopic treat-
ment of malignant tumors of the paranasal sinuses and anterior skull base. Oper
Tech Otolayngol Head Neck Surg 2006;17:152–67.
42. Galassi E, Pasquini E, Frank G, et al. Combined endoscopy-assisted cranionasal
approach for resection of infantile myofibromatosis of the ethmoid and anterior
skull base. Case report. J Neurosurg Pediatr 2008;2:58–62.