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Recent progress in endoscopic skull base surgery: Functional preservation and multiportal approaches

Published:April 16, 2022DOI:https://doi.org/10.1016/j.anl.2022.04.001

      Abstract

      Over the past couple of decades, endoscopic skull base surgery (ESBS) has significantly evolved and is applied to a broad range of skull base pathologies, including sinonasal malignancies. Recent studies have demonstrated remarkable progress of ESBS in complete resection with low morbidity and extension of its application to larger and more complex lesions. In this review, we focus on the evolution of functional preservation and multiportal approaches. Progress in preoperative assessments and surgical techniques improved the preservation of olfactory function after ESBS. The technical feasibility of olfaction preservation even after resection of olfactory groove lesions has been reported. To overcome the limitations of extending use of the endoscopic endonasal approach in surgical fields, various types of multiportal approaches, including combinations of the endoscopic endonasal and transorbital, transmaxillary, or transoral approach, have been reported, as they are useful for complete resection of extensive pathologies while limiting morbidity. These innovative techniques are still in the process of maturation. Hence, an ongoing critical evaluation is essential to ensure efficacy.

      Keywords

      1. Introduction

      1.1 Brief history of endoscopic skull base surgery

      Endoscopic skull base surgery (ESBS) is a rapidly growing field of surgery that is applied to a broad range of skull base lesions, including sinonasal malignancies. The history of ESBS was initiated by the use of endoscopes that had been developed for endoscopic sinus surgery in trans-sphenoidal surgery for pituitary tumors in the late 1990s [
      • Jho H.D.
      • Carrau R.L.
      Endoscopic endonasal transsphenoidal surgery: experience with 50 patients.
      ,
      • Heilman C.B.
      • Shucart W.A.
      • Rebeiz E.E.
      Endoscopic sphenoidotomy approach to the sella.
      ,
      • Aust M.R.
      • McCaffrey T.V.
      • Atkinson J.
      Transnasal endoscopic approach to the sella turcica.
      ,
      • Cappabianca P.
      • Alfieri A.
      • de Divitiis E.
      Endoscopic endonasal transsphenoidal approach to the sella: towards functional endoscopic pituitary surgery (FEPS).
      ,
      • Sethi D.S.
      • Pillay P.K.
      Endoscopic management of lesions of the sella turcica.
      ,
      • Rodziewicz G.S.
      • Kelley R.T.
      • Kellman R.M.
      • Smith M.V.
      Transnasal endoscopic surgery of the pituitary gland: technical note.
      ,
      • Yaniv E.
      • Rappaport Z.H.
      Endoscopic transseptal transsphenoidal surgery for pituitary tumors.
      ]. After these early experiences, the endoscopic endonasal approach (EEA) has gained wide acceptance as a primary surgical approach to midline lesions of the skull base, followed by lateral, inferior, or anterior extension. The number of publications associated with ESBS has dramatically increased since 2010 (Fig. 1). The development of reconstruction procedures for EEA has also contributed to the extension of using EEA to treat skull base lesions [
      • Nakagawa T.
      • Asada M.
      • Takashima T.
      • Tomiyama K.
      Sellar reconstruction after endoscopic transnasal hypophysectomy.
      ,
      • Hadad G.
      • Bassagasteguy L.
      • Carrau R.L.
      • Mataza J.C.
      • Kassam A.
      • Snyderman C.H.
      • et al.
      A novel reconstructive technique after endoscopic expanded endonasal approaches: vascular pedicle nasoseptal flap.
      ,
      • Patel M.R.
      • Shah R.N.
      • Snyderman C.H.
      • Carrau R.L.
      • Germanwala A.V.
      • Kassam A.B.
      • et al.
      Pericranial flap for endoscopic anterior skull-base reconstruction: clinical outcomes and radioanatomic analysis of preoperative planning.
      ,
      • Hadad G.
      • Rivera-Serrano C.M.
      • Bassagaisteguy L.H.
      • Carrau R.L.
      • Fernandez-Miranda J.
      • Prevedello D.M.
      • et al.
      Anterior pedicle lateral nasal wall flap: a novel technique for the reconstruction of anterior skull base defects.
      ,
      • Rivera-Serrano C.M.
      • Bassagaisteguy L.H.
      • Hadad G.
      • Carrau R.L.
      • Kelly D.
      • Prevedello D.M.
      • et al.
      Posterior pedicle lateral nasal wall flap: new reconstructive technique for large defects of the skull base.
      ]. ESBS is often performed by a combination of otolaryngology-head and neck surgeons and neurosurgeons, which may be related to the rapid growth of ESBS use. The mixture of techniques and anatomical knowledge in different fields accelerated innovations in ESBS. An accumulation of publications associated with ESBS has provided evidence for its efficiency and indications [
      • Lund V.J.
      • Stammberger H.
      • Nicolai P.
      • Castelnuovo P.
      • Beal T.
      • Beham A.
      • et al.
      European position paper on endoscopic management of tumours of the nose, paranasal sinuses and skull base.
      ,
      • Wang E.W.
      • Zanation A.M.
      • Gardner P.A.
      • Schwartz T.H.
      • Eloy J.A.
      • Adappa N.D.
      • et al.
      ICAR: endoscopic skull-base surgery.
      ]. These international consensus or position papers, which were written by otolaryngology-head and neck surgeons and neurosurgeons, provide fundamental or established information on ESBS in various pathologies, including sinonasal malignancies. The European position paper for endoscopic management of tumors was published in 2010 [
      • Lund V.J.
      • Stammberger H.
      • Nicolai P.
      • Castelnuovo P.
      • Beal T.
      • Beham A.
      • et al.
      European position paper on endoscopic management of tumours of the nose, paranasal sinuses and skull base.
      ], and it provided fundamental knowledge of treatment modalities for sinonasal and skull base tumors. In this systematic review, most publications were published from selected high-volume centers. Ten years later, the international consensus statement on ESBS demonstrated remarkable progress in ESBS for that decade [
      • Wang E.W.
      • Zanation A.M.
      • Gardner P.A.
      • Schwartz T.H.
      • Eloy J.A.
      • Adappa N.D.
      • et al.
      ICAR: endoscopic skull-base surgery.
      ], supporting the validity of ESBS. Importantly, not only surgical outcomes but also nasal morbidity after ESBS were systematically reviewed.
      Fig 1
      Fig. 1Number of publications for the term “endoscopic skull base” in the PubMed search from 1990 to 2020. An increase in the number of publications since 2010 is noted.
      Reasons for rapid growth and worldwide expansion of ESBS use include its low invasiveness and excellent visualization of the surgical field. In general, endoscopic approaches require smaller incisions than traditional approaches. Recent studies have revealed a lower incidence of postoperative complications and shorter hospitalization in ESBS than in traditional surgeries [
      • Eloy J.A.
      • Vivero R.J.
      • Hoang K.
      • Civantos F.J.
      • Weed D.T.
      • Morcos J.J.
      • et al.
      Comparison of transnasal endoscopic and open craniofacial resection for malignant tumors of the anterior skull base.
      ]. Regarding visualization, endoscopic surgeries have several advantages, including an angled, panoramic view in comparison with surgeries using microscopic and conventional open approaches. It is also important that primary surgeons and assistants can share the same images during the operation, as this also contributes to education and may be associated with the development of multiportal approaches. In addition to these advantages, recent progress in technology provides high-definition images of endoscopes that are compatible with microscopic images. This has led to the development of trans-canal endoscopic ear surgery in the field of otology. Additionally, high-definition images can contribute to clear margin resection of tumors and/or preservation of nerves and vessels in ESBS.

      1.2 Objective

      In this review, from the viewpoint of otolaryngology-head and neck surgeons, we focused on two topics associated with the recent progress in ESBS. One is functional preservation, which is an important issue associated with low invasiveness. Previously, the equivalence or superiority of endoscopic approaches in surgical resection or oncological outcomes to traditional approaches has been the focal point. Recently, focal points have been moved to low morbidity and functional preservation, in addition to equivalent surgical outcomes. The other topic of this review is multiportal approaches for skull base lesions, which is one of the future directions of ESBS. Multiportal approaches may reduce the risk of injuries to vital organs, including the carotid artery, and contribute to clear margin resection.

      2. Functional preservation

      It is inevitable to change or sometimes destroy normal nasal constructions to approach or resect tumors, even if endoscopic procedures are further improved or sophisticated. An adequate reconstruction of the skull base, including elevation of nasoseptal flaps, also requires changes in normal and non-pathological nasal structures. As a result, negative effects on nasal function can be caused. The most common problems are nasal crusting, nasal discharge, nasal obstruction, and olfactory dysfunction [
      • Awad A.J.
      • Mohyeldin A.
      • El-Sayed I.H.
      • Aghi M.K.
      Sinonasal morbidity following endoscopic endonasal skull base surgery.
      ]. However, a paradigm shift in recent decades has made functional outcomes, including olfaction, more important than aesthetic outcomes. In the next decade, satisfactory surgical outcomes with minimum nasal morbidity will be required for ESBS. Herein, among nasal morbidities, we focused on olfaction preservation following ESBS.

      2.1 Olfactory preservation after pituitary surgery

      Olfaction is an important sensory input, and its dysfunction results in a significant decrease in quality of life. Endoscopic pituitary surgery is the most established procedure for ESBS. Therefore, there are a comparatively large number of publications describing olfactory outcomes following endoscopic pituitary surgery, most of which were published after 2010. The surgical corridor for endoscopic pituitary surgery includes the olfactory cleft and sphenoethmoidal recess, and elevation of the mucoperiosteal flaps, including a nasoseptal flap in the nasal septum and sphenoethmoidal recess, is frequently performed. These issues indicate the risk of injury to the olfactory system during surgical procedures. However, no direct injury to the olfactory epithelium occurs if surgeons pay attention to the location of the olfactory epithelium and avoid unnecessary resection of the superior and/or middle turbinate.
      A literature review of olfactory outcomes that were determined by objective measures following endoscopic pituitary surgery demonstrated favorable results in preservation of olfaction after surgery [
      • Majovsky M.
      • Astl J.
      • Kovar D.
      • Masopust V.
      • Benes V.
      • Netuka D.
      Olfactory function in patients after transsphenoidal surgery for pituitary adenomas-a short review.
      ]. The proportion for olfactory dysfunction after microscopic pituitary surgery was 39.7%, while that after endoscopic surgery with flap elevation was 14.4% [
      • Majovsky M.
      • Astl J.
      • Kovar D.
      • Masopust V.
      • Benes V.
      • Netuka D.
      Olfactory function in patients after transsphenoidal surgery for pituitary adenomas-a short review.
      ], suggesting that EEA is superior to the microscopic approach in the preservation of olfaction. This may be related to the use of speculums in microscopic approaches [
      • Kahilogullari G.
      • Beton S.
      • Al-Beyati E.S.
      • Kantarcioglu O.
      • Bozkurt M.
      • Kantarcioglu E.
      • et al.
      Olfactory functions after transsphenoidal pituitary surgery: endoscopic versus microscopic approach.
      ]. In contrast, the proportion of olfactory dysfunction following EEA without flap elevation was only 3% [
      • Kahilogullari G.
      • Beton S.
      • Al-Beyati E.S.
      • Kantarcioglu O.
      • Bozkurt M.
      • Kantarcioglu E.
      • et al.
      Olfactory functions after transsphenoidal pituitary surgery: endoscopic versus microscopic approach.
      ], which suggests that an elevation of flaps can have negative effects on olfaction preservation. Several studies have indicated that the use of electrocautery for flap incision can be associated with olfactory dysfunction [
      • Greig S.R.
      • Cooper T.J.
      • Sommer D.D.
      • Nair S.
      • Wright E.D.
      Objective sinonasal functional outcomes in endoscopic anterior skull-base surgery: an evidence-based review with recommendations.
      ,
      • Hong S.D.
      • Nam D.H.
      • Park J.
      • Kim H.Y.
      • Chung S.K.
      • Dhong H.J.
      Olfactory outcomes after endoscopic pituitary surgery with nasoseptal "rescue" flaps: electrocautery versus cold knife.
      ,
      • Kim S.W.
      • Park K.B.
      • Khalmuratova R.
      • Lee H.K.
      • Jeon S.Y.
      • Kim D.W.
      Clinical and histologic studies of olfactory outcomes after nasoseptal flap harvesting.
      ]. Conversely, Harvey et al. claimed that inappropriate incisions for nasoseptal flaps, not electrocautery, is a cause of olfactory dysfunction, based on their excellent outcomes following endoscopic pituitary surgery using electrocautery [
      • Harvey R.J.
      • Winder M.
      • Davidson A.
      • Steel T.
      • Nalavenkata S.
      • Mrad N.
      • et al.
      The olfactory strip and its preservation in endoscopic pituitary surgery maintains smell and sinonasal function.
      ]. Puccinelli et al. demonstrated no difference in olfactory outcomes between a cold knife and monopolar cautery [
      • Puccinelli C.L.
      • Yin L.X.
      • O'Brien E.K.
      • Van Gompel J.J.
      • Choby G.W.
      • Van Abel K.M.
      • et al.
      Long-term olfaction outcomes in transnasal endoscopic skull-base surgery: a prospective cohort study comparing electrocautery and cold knife upper septal limb incision techniques.
      ]. We also evaluated olfactory function assessed by a T & T olfactometer after endoscopic pituitary surgery using electrocautery, in which improvement of olfaction was found in 50% of patients, and 38% of patients exhibited the maintenance or preservation of olfaction [
      • Kuwata F.
      • Kikuchi M.
      • Ishikawa M.
      • Tanji M.
      • Sakamoto T.
      • Yamashita M.
      • et al.
      Long-term olfactory function outcomes after pituitary surgery by endoscopic endonasal transsphenoidal approach.
      ]. Similar to our results, several studies have shown improvement in olfaction after endoscopic pituitary surgery [
      • Hart C.K.
      • Theodosopoulos P.V.
      • Zimmer L.A.
      Olfactory changes after endoscopic pituitary tumor resection.
      ,
      • Upadhyay S.
      • Buohliqah L.
      • Dolci R.L.L.
      • Otto B.A.
      • Prevedello D.M.
      • Carrau R.L.
      Periodic olfactory assessment in patients undergoing skull base surgery with preservation of the olfactory strip.
      ]. The improvement of olfaction following endoscopic pituitary surgery may be associated with the improvement of odor access into the olfactory cleft due to enlargement of the surgical access to the sphenoethmoidal recess. Furthermore, resection of the inferior third of the superior turbinate had no negative effect on olfactory preservation in our study [
      • Kuwata F.
      • Kikuchi M.
      • Ishikawa M.
      • Tanji M.
      • Sakamoto T.
      • Yamashita M.
      • et al.
      Long-term olfactory function outcomes after pituitary surgery by endoscopic endonasal transsphenoidal approach.
      ]. Altogether, in endoscopic pituitary surgery, adequate designs of the mucosal incision in the nasal septum and appropriate turbinate preservation are key elements for olfactory preservation following endoscopic pituitary surgery.

      2.2 Olfactory preservation after olfactory neuroblastoma surgery

      Olfactory preservation following anterior skull base surgery via EEA is more challenging than preservation following endoscopic pituitary surgery. Among sinonasal malignancies, olfactory neuroblastoma (ONB) or esthesioneuroblastoma is the forefront of ESBS [
      • Wang E.W.
      • Zanation A.M.
      • Gardner P.A.
      • Schwartz T.H.
      • Eloy J.A.
      • Adappa N.D.
      • et al.
      ICAR: endoscopic skull-base surgery.
      ,
      • Veyrat M.
      • Vérillaud B.
      • Fiaux-Camous D.
      • Froelich S.
      • Bresson D.
      • Nicolai P.
      • et al.
      Olfactory neuroblastoma.
      ]. ONB arises from the olfactory epithelium, and its stalk is usually located at the central skull base. Therefore, after removal of the bulk of the tumor, close endoscopic inspection is easy, which may contribute to complete margin-negative resection. ONB is suitable for ESBS because of its anatomical location, and this anatomical characteristic also means difficulty in olfactory preservation. Surgical resection of ONBs frequently results in loss of olfaction. However, recent studies have indicated the feasibility of olfactory preservation for early-stage ONBs while achieving margin-negative resection [
      • Wessell A.
      • Singh A.
      • Litvack Z.
      Preservation of olfaction after unilateral endoscopic approach for resection of esthesioneuroblastoma.
      ,
      • Tajudeen B.A.
      • Adappa N.D.
      • Kuan E.C.
      • Schwartz J.S.
      • Suh J.D.
      • Wang M.B.
      • et al.
      Smell preservation following endoscopic unilateral resection of esthesioneuroblastoma: a multi-institutional experience.
      ,
      • Gompel J.J.V.
      • Janus J.R.
      • Hughes J.D.
      • Stokken J.K.
      • Moore E.J.
      • Ryan T.
      • et al.
      Esthesioneuroblastoma and olfactory preservation: is it reasonable to attempt smell preservation?.
      ,
      • Nakagawa T.
      • Kodama S.
      • Kobayashi M.
      • Sanuki T.
      • Tanaka S.
      • Hanai N.
      • et al.
      Endoscopic endonasal management of esthesioneuroblastoma: a retrospective multicenter study.
      ,
      • Matsunaga M.
      • Kikuchi M.
      • Kuwata F.
      • Kitada Y.
      • Omori K.
      • Nakagawa T.
      Psychophysical assessments of olfaction after endoscopic unilateral resection with post-operative radiotherapy in olfactory neuroblastomas.
      ].
      In selected early-stage ONBs, close endoscopic inspection of the tumor stalk enables preservation of the contralateral olfactory system with complete margin-negative resection of a diseased side, namely “complete” unilateral resection, in which the benefit from the progress of imaging technology may play a critical role. In previous case reports [
      • Wessell A.
      • Singh A.
      • Litvack Z.
      Preservation of olfaction after unilateral endoscopic approach for resection of esthesioneuroblastoma.
      ,
      • Tajudeen B.A.
      • Adappa N.D.
      • Kuan E.C.
      • Schwartz J.S.
      • Suh J.D.
      • Wang M.B.
      • et al.
      Smell preservation following endoscopic unilateral resection of esthesioneuroblastoma: a multi-institutional experience.
      ,
      • Gompel J.J.V.
      • Janus J.R.
      • Hughes J.D.
      • Stokken J.K.
      • Moore E.J.
      • Ryan T.
      • et al.
      Esthesioneuroblastoma and olfactory preservation: is it reasonable to attempt smell preservation?.
      ,
      • Matsunaga M.
      • Kikuchi M.
      • Kuwata F.
      • Kitada Y.
      • Omori K.
      • Nakagawa T.
      Psychophysical assessments of olfaction after endoscopic unilateral resection with post-operative radiotherapy in olfactory neuroblastomas.
      ], olfaction was still retained in 57% of patients after unilateral resection, and 24% of patients had preserved olfactory function at the normal or preoperative level including no patients with anosmia preoperatively (Table 1), suggesting the difficulty of complete preservation of the contralateral olfactory system following unilateral resection. In our case series, one possible explanation for the failure of olfactory preservation was mechanical force at the contralateral olfactory bulb during additional resection of the dura matter according to the results of intraoperative frozen biopsy [
      • Matsunaga M.
      • Kikuchi M.
      • Kuwata F.
      • Kitada Y.
      • Omori K.
      • Nakagawa T.
      Psychophysical assessments of olfaction after endoscopic unilateral resection with post-operative radiotherapy in olfactory neuroblastomas.
      ]. To attempt unilateral resection of ONBs, preoperative imaging analyses are critical. Van Gompel et al. examined whether surgeons can predict the pathology and tumor involvement in the olfactory bulb and tract by reviewing preoperative magnetic resonance imaging (MRI) scans [
      • Gompel J.J.V.
      • Janus J.R.
      • Hughes J.D.
      • Stokken J.K.
      • Moore E.J.
      • Ryan T.
      • et al.
      Esthesioneuroblastoma and olfactory preservation: is it reasonable to attempt smell preservation?.
      ]. The accuracy for the prediction of pathology was 96%, suggesting the feasibility of olfactory preservation in selected early-stage ONBs. They recommended high-quality computed tomography, coronal T2-weighted MRI, and coronal T1-weighted MRI with enhancement by gadolinium [
      • Gompel J.J.V.
      • Janus J.R.
      • Hughes J.D.
      • Stokken J.K.
      • Moore E.J.
      • Ryan T.
      • et al.
      Esthesioneuroblastoma and olfactory preservation: is it reasonable to attempt smell preservation?.
      ]. Altogether, olfactory preservation should be considered for patients with early-stage ONB, and precise preoperative imaging examinations will be necessary to determine the indication for unilateral resection. Further improvement of surgical techniques can contribute to better olfactory preservation following unilateral resection of ONBs.
      Table 1Olfactory preservation following unilateral resection of olfactory neuroblastomas.
      AuthorNo. of PtNo. of Pt with postop RTOlfactory outcome
      Normal or equal to preop (no. of Pt)Microsmia (no. of Pt)Anosmia (no. of Pt)Olfaction retainment (%)
      Wessell et al. [
      • Wessell A.
      • Singh A.
      • Litvack Z.
      Preservation of olfaction after unilateral endoscopic approach for resection of esthesioneuroblastoma.
      ]
      10010
      Tajudeen et al. [
      • Tajudeen B.A.
      • Adappa N.D.
      • Kuan E.C.
      • Schwartz J.S.
      • Suh J.D.
      • Wang M.B.
      • et al.
      Smell preservation following endoscopic unilateral resection of esthesioneuroblastoma: a multi-institutional experience.
      ]
      1414248
      Von Gompel et al. [
      • Gompel J.J.V.
      • Janus J.R.
      • Hughes J.D.
      • Stokken J.K.
      • Moore E.J.
      • Ryan T.
      • et al.
      Esthesioneuroblastoma and olfactory preservation: is it reasonable to attempt smell preservation?.
      ]
      10010
      Maggiore et al. [
      • Matsunaga M.
      • Kikuchi M.
      • Kuwata F.
      • Kitada Y.
      • Omori K.
      • Nakagawa T.
      Psychophysical assessments of olfaction after endoscopic unilateral resection with post-operative radiotherapy in olfactory neuroblastomas.
      ]
      10100
      Matsunaga et al. [
      • Almeida J.P.
      • de Andrade E.
      • Reghin-Neto M.
      • Radovanovic I.
      • Recinos P.F.
      • Kshettry V.R.
      From above and below: the microsurgical anatomy of endoscopic endonasal and transcranial microsurgical approaches to the parasellar region.
      ]
      44211
      All studies211857957%
      Equal to preop includes no patients showing anosmia preoperatively. No., number; Pt, patients; postop, postoperative; RT, radiotherapy; preop, preoperative levels.

      3. Multiportal combined approach in endoscopic skull base surgery

      EEA to the midline skull base has evolved over the last few decades and is now being widely used for “non-midline” skull base regions. However, for lesions with far lateral or inferior extension, EEA has access limitations because of the presence of important neurovascular structures, including the optic nerve and internal carotid artery (ICA) in the surgical pathway.
      Adding an adequate non-nasal corridor with EEA provides a larger surgical field and extensive visualization and allows surgeons to easily access these tumors. Surgery with this multiportal combined approach has the potential to perform complete tumor resection with reduced operative time and blood loss, fewer postoperative complications, and excellent cosmetic results compared to traditional open surgeries.

      3.1 Transorbital approach combined with the endoscopic endonasal approach

      EEA to the medial middle cranial fossa, such as the parasellar region and medial aspect of the cavernous sinus, has been reported as an effective approach [
      • Almeida J.P.
      • de Andrade E.
      • Reghin-Neto M.
      • Radovanovic I.
      • Recinos P.F.
      • Kshettry V.R.
      From above and below: the microsurgical anatomy of endoscopic endonasal and transcranial microsurgical approaches to the parasellar region.
      ]. However, for lesions with far lateral extension to the anterior or lateral middle cranial fossa, EEA has access limitations because of surgical obstacles such as orbital contents and optic nerve in the surgical pathway.
      To overcome the limitations of EEA, the transorbital endoscopic approach (TOEA) was developed by Moe et al. [
      • Moe K.S.
      • Bergeron C.M.
      • Ellenbogen R.G.
      Transorbital neuroendoscopic surgery.
      ]. This transorbital surgical trajectory is based on an orbital quadrant system consisting of four approaches: superior lid crease, precaruncular, lateral retrocanthal, and inferior transconjunctival approaches [
      • Moe K.S.
      • Bergeron C.M.
      • Ellenbogen R.G.
      Transorbital neuroendoscopic surgery.
      ]. The type of approach is selected based on the site of the targeted lesion and the surgeon's confidence and competency with the incision. Through one or two adjacent approaches of the four with drilling of the required orbital walls, TOEA can be used to approach various orbital [
      • Azad A.D.
      • Sears C.M.
      • Hwang P.H.
      • Mohyeldin A.
      • Fernandez-Miranda J.
      • Kossler A.L.
      Multi-compartment skull base orbital cavernous venous malformation: a rare presentation of a common orbital mass.
      ], infratemporal fossa (ITF) [
      • Mahmoud M.S.
      • Diab A.G.
      • Ngombu S.
      • Prevedello D.M.
      • Carrau R.L.
      Endoscopic transorbital ligation of the maxillary artery through the inferior orbital fissure.
      ], petrous apex [
      • Lee W.J.
      • Hong S.D.
      • Woo K.I.
      • Seol H.J.
      • Choi J.W.
      • Lee J.I.
      • et al.
      Endoscopic endonasal and transorbital approaches to petrous apex lesions.
      ], anterior cranial fossa [
      • Vedhapoodi A.G.
      • Periyasamy A.
      • Senthilkumar D.
      A novel combined transorbital transnasal endoscopic approach for reconstruction of posttraumatic complex anterior cranial fossa defect.
      ,
      • Raza S.M.
      • Quinones-Hinojosa A.
      • Lim M.
      • Boahene K.D.
      The transconjunctival transorbital approach: a keyhole approach to the midline anterior skull base.
      ] and middle cranial fossa [
      • Lee M.H.
      • Hong S.D.
      • Woo K.I.
      • Kim Y.D.
      • Choi J.W.
      • Seol H.J.
      • et al.
      Endoscopic endonasal versus transorbital surgery for middle cranial fossa tumors: comparison of clinical outcomes based on surgical corridors.
      ,
      • Dallan I.
      • Sellari-Franceschini S.
      • Turri-Zanoni M.
      • de Notaris M.
      • Fiacchini G.
      • Fiorini F.R.
      • et al.
      Endoscopic transorbital superior eyelid approach for the management of selected spheno-orbital meningiomas: preliminary experience.
      ] lesions. Regarding the superior orbital fissure (SOF), TOEA is superior in accessing the lateral two-thirds of the SOF and the superolateral intraconal space [
      • Li L.
      • London N.R.
      • Chen X.
      • Prevedello D.M.
      • Carrau R.L.
      Expanded exposure and detailed anatomic analysis of the superior orbital fissure: implications for endonasal and transorbital approaches.
      ]. Among the pathologies and clinical conditions for which surgeries with TOEA were applied in the literature, meningioma was the most common, followed by cerebral spinal fluid leak, inflammation/infection/abscess, and schwannoma [
      • Vural A.
      • Carobbio A.L.C.
      • Ferrari M.
      • Rampinelli V.
      • Schreiber A.
      • Mattavelli D.
      • et al.
      Transorbital endoscopic approaches to the skull base: a systematic literature review and anatomical description.
      ,
      • Houlihan L.M.
      • Staudinger Knoll A.J.
      • Kakodkar P.
      • Zhao X.
      • O'Sullivan M.G.J.
      • Lawton M.T.
      • et al.
      Transorbital neuroendoscopic surgery as a mainstream neurosurgical corridor: a systematic review.
      ]. The key step in using TOEA includes the identification of superior and inferior orbital fissures and then drilling the ocular surface of the greater sphenoid wing to expose the middle cranial fossa [
      • Lee W.J.
      • Hong S.D.
      • Woo K.I.
      • Seol H.J.
      • Choi J.W.
      • Lee J.I.
      • et al.
      Endoscopic endonasal and transorbital approaches to petrous apex lesions.
      ]. TOEA is usually co-planar with the anterior cranial fossa, middle cranial fossa, optic nerve, chiasm, and petrous apex; therefore, it provides a direct corridor to the targeted lesion involving those areas [
      • Moe K.S.
      • Bergeron C.M.
      • Ellenbogen R.G.
      Transorbital neuroendoscopic surgery.
      ,
      • Lee W.J.
      • Hong S.D.
      • Woo K.I.
      • Seol H.J.
      • Choi J.W.
      • Lee J.I.
      • et al.
      Endoscopic endonasal and transorbital approaches to petrous apex lesions.
      ] and the requirement for angled endoscopes and instrumentation can be minimized, providing less disorientation, optimal visualization, illumination, and magnification [
      • Moe K.S.
      • Bergeron C.M.
      • Ellenbogen R.G.
      Transorbital neuroendoscopic surgery.
      ]. Compared with open craniotomy, the advantages of TOEA are minimal retraction of the temporal lobe and limited disruption of adjacent tissues [
      • Lee W.J.
      • Hong S.D.
      • Woo K.I.
      • Seol H.J.
      • Choi J.W.
      • Lee J.I.
      • et al.
      Endoscopic endonasal and transorbital approaches to petrous apex lesions.
      ]. However, it should be noted that there are several drawbacks and possible postoperative complications associated with TOEA. First, the working space is narrow, which may restrict instrument maneuverability [
      • Li L.
      • London N.R.
      • Chen X.
      • Prevedello D.M.
      • Carrau R.L.
      Expanded exposure and detailed anatomic analysis of the superior orbital fissure: implications for endonasal and transorbital approaches.
      ,
      • Houlihan L.M.
      • Staudinger Knoll A.J.
      • Kakodkar P.
      • Zhao X.
      • O'Sullivan M.G.J.
      • Lawton M.T.
      • et al.
      Transorbital neuroendoscopic surgery as a mainstream neurosurgical corridor: a systematic review.
      ]. Second, orbital complications such as diplopia, ptosis, and V2 numbness may occur because of the proximity to the orbital contents [
      • Houlihan L.M.
      • Staudinger Knoll A.J.
      • Kakodkar P.
      • Zhao X.
      • O'Sullivan M.G.J.
      • Lawton M.T.
      • et al.
      Transorbital neuroendoscopic surgery as a mainstream neurosurgical corridor: a systematic review.
      ]. Third, skin/conjunctiva incision and lateral canthotomy may affect facial aesthetics [
      • Li L.
      • London N.R.
      • Chen X.
      • Prevedello D.M.
      • Carrau R.L.
      Expanded exposure and detailed anatomic analysis of the superior orbital fissure: implications for endonasal and transorbital approaches.
      ]. Finally, retraction of the globe may cause visual impairment [
      • Li L.
      • London N.R.
      • Chen X.
      • Prevedello D.M.
      • Carrau R.L.
      Expanded exposure and detailed anatomic analysis of the superior orbital fissure: implications for endonasal and transorbital approaches.
      ].
      TOEA can be used alone as a monoportal technique or used in combination with EEA as a multiportal technique [
      • Vedhapoodi A.G.
      • Periyasamy A.
      • Senthilkumar D.
      A novel combined transorbital transnasal endoscopic approach for reconstruction of posttraumatic complex anterior cranial fossa defect.
      ,
      • Raza S.M.
      • Quinones-Hinojosa A.
      • Lim M.
      • Boahene K.D.
      The transconjunctival transorbital approach: a keyhole approach to the midline anterior skull base.
      ,
      • Lee M.H.
      • Hong S.D.
      • Woo K.I.
      • Kim Y.D.
      • Choi J.W.
      • Seol H.J.
      • et al.
      Endoscopic endonasal versus transorbital surgery for middle cranial fossa tumors: comparison of clinical outcomes based on surgical corridors.
      ,
      • Dallan I.
      • Sellari-Franceschini S.
      • Turri-Zanoni M.
      • de Notaris M.
      • Fiacchini G.
      • Fiorini F.R.
      • et al.
      Endoscopic transorbital superior eyelid approach for the management of selected spheno-orbital meningiomas: preliminary experience.
      ,
      • Lubbe D.E.
      • Douglas-Jones P.
      • Wasl H.
      • Mustak H.
      • Semple P.L.
      Contralateral precaruncular approach to the lateral sphenoid sinus-a case report detailing a new, multiportal approach to lesions, and defects in the lateral aspect of well-pneumatized sphenoid sinuses.
      ,
      • Lubbe D.
      • Mustak H.
      • Taylor A.
      • Fagan J.
      Minimally invasive endo-orbital approach to sphenoid wing meningiomas improves visual outcomes - our experience with the first seven cases.
      ,
      • Ciporen J.N.
      • Lucke-Wold B.
      • Dogan A.
      • Cetas J.
      • Cameron W.
      Endoscopic endonasal transclival approach versus dual transorbital port technique for clip application to the posterior circulation: a cadaveric anatomical and cerebral circulation simulation study.
      ,
      • Ciporen J.
      • Lucke-Wold B.
      • Dogan A.
      • Cetas J.S.
      • Cameron W.E.
      Dual endoscopic endonasal transsphenoidal and precaruncular transorbital approaches for clipping of the cavernous carotid artery: a cadaveric simulation.
      ,
      • Alqahtani A.
      • Padoan G.
      • Segnini G.
      • Lepera D.
      • Fortunato S.
      • Dallan I.
      • et al.
      Transorbital transnasal endoscopic combined approach to the anterior and middle skull base: a laboratory investigation.
      ,
      • Di Somma A.
      • Langdon C.
      • de Notaris M.
      • Reyes L.
      • Ortiz-Perez S.
      • Alobid I.
      • et al.
      Combined and simultaneous endoscopic endonasal and transorbital surgery for a Meckel's cave schwannoma: technical nuances of a mini-invasive, multiportal approach.
      ,
      • Tham T.
      • Costantino P.
      • Bruni M.
      • Langer D.
      • Boockvar J.
      • Singh P.
      Multiportal combined transorbital and transnasal endoscopic resection of fibrous dysplasia.
      ]. Multiportal surgery can be performed by taking advantage of eight orbital portals on both sides in TOEA and two nasal corridors in various combinations to treat various skull base pathologies [
      • Vedhapoodi A.G.
      • Periyasamy A.
      • Senthilkumar D.
      A novel combined transorbital transnasal endoscopic approach for reconstruction of posttraumatic complex anterior cranial fossa defect.
      ]. The multiportal transorbital approach combined with EEA provides a wider surgical field and allows better visualization than the monoportal approach and may expand the clinical applications of the monoportal approach for various skull base lesions [
      • Alqahtani A.
      • Padoan G.
      • Segnini G.
      • Lepera D.
      • Fortunato S.
      • Dallan I.
      • et al.
      Transorbital transnasal endoscopic combined approach to the anterior and middle skull base: a laboratory investigation.
      ,
      • Di Somma A.
      • Langdon C.
      • de Notaris M.
      • Reyes L.
      • Ortiz-Perez S.
      • Alobid I.
      • et al.
      Combined and simultaneous endoscopic endonasal and transorbital surgery for a Meckel's cave schwannoma: technical nuances of a mini-invasive, multiportal approach.
      ,
      • Tham T.
      • Costantino P.
      • Bruni M.
      • Langer D.
      • Boockvar J.
      • Singh P.
      Multiportal combined transorbital and transnasal endoscopic resection of fibrous dysplasia.
      ,
      • Dallan I.
      • Castelnuovo P.
      • Locatelli D.
      • Turri-Zanoni M.
      • AlQahtani A.
      • Battaglia P.
      • et al.
      Multiportal combined transorbital transnasal endoscopic approach for the management of selected skull base lesions: preliminary experience.
      ,
      • A D.I.S.
      • Guizzardi G.
      • Valls Cusiné C.
      • Hoyos J.
      • Ferres A.
      • Topczewski T.E.
      • et al.
      Combined endoscopic endonasal and transorbital approach to skull base tumors: a systematic literature review.
      ]. Faulkner et al. recently reported that the combined robotic transorbital and transnasal approach to the nasopharynx and anterior cranial fossa is feasible because combined ports overcome funnel effects, allowing current robotic instruments to operate within the space and limit the risk of collisions [
      • Faulkner J.
      • Naidoo R.
      • Arora A.
      • Jeannon J.P.
      • Hopkins C.
      • Surda P.
      Combined robotic transorbital and transnasal approach to the nasopharynx and anterior skull base: feasibility study.
      ]. Additionally, the multiportal combined approach is less likely to result in diplopia, ptosis, and V2 numbness [
      • Houlihan L.M.
      • Staudinger Knoll A.J.
      • Kakodkar P.
      • Zhao X.
      • O'Sullivan M.G.J.
      • Lawton M.T.
      • et al.
      Transorbital neuroendoscopic surgery as a mainstream neurosurgical corridor: a systematic review.
      ].

      3.2 Transmaxillary/transoral approach combined with the endoscopic endonasal approach

      3.2.1 Infratemporal fossa and parapharyngeal space

      The ITF is a deeply seated retromaxillary space, which is bounded laterally by the mandibular ramus, medially by the lateral pterygoid plate, superiorly by the greater wing of the sphenoid, and opens inferiorly into the parapharyngeal space (PPS) [
      • Abdomen G.J.
      Grant's atlas of anatomy.
      ]. The PPS is described as an inverted pyramid with the base formed by the skull base and the apex pointing to the greater cornu of the hyoid bone [
      • Liu Q.
      • Wang H.
      • Zhao W.
      • Song X.
      • Sun X.
      • Yu H.
      • et al.
      Endoscopic transnasal transmaxillary approach to the upper parapharyngeal space and the skull base.
      ]. These areas are difficult to reach, so open surgery through various lateral approaches [
      • Prasad S.C.
      • Piccirillo E.
      • Chovanec M.
      • La Melia C.
      • De Donato G.
      • Sanna M.
      Lateral skull base approaches in the management of benign parapharyngeal space tumors.
      ], including transcervical [
      • Basaran B.
      • Polat B.
      • Unsaler S.
      • Ulusan M.
      • Aslan I.
      • Hafiz G.
      Parapharyngeal space tumours: the efficiency of a transcervical approach without mandibulotomy through review of 44 cases.
      ], transparotid [
      • Fermi M.
      • Serafini E.
      • Ferri G.
      • Alicandri-Ciufelli M.
      • Presutti L.
      • Mattioli F.
      Management of parapharyngeal space tumors with transparotid-transcervical approach: analysis of prognostic factors related with disease-control and functional outcomes.
      ], and subtemporal preauricular ITF approaches [
      • Fisch U.
      • Fagan P.
      • Valavanis A.
      The infratemporal fossa approach for the lateral skull base.
      ] and their combinations, have been traditionally performed. Recently, to provide minimally invasive approaches to PPS/ITF lesions, endoscopic-assisted transoral surgery [
      • Dallan I.
      • Seccia V.
      • Muscatello L.
      • Lenzi R.
      • Castelnuovo P.
      • Bignami M.
      • et al.
      Transoral endoscopic anatomy of the parapharyngeal space: a step-by-step logical approach with surgical considerations.
      ,
      • Patwa H.S.
      • Yanez-Siller J.C.
      • Gomez Galarce M.
      • Otto B.A.
      • Prevedello D.M.
      • Carrau R.L.
      Analysis of the far-medial transoral endoscopic approach to the infratemporal fossa.
      ,
      • Cai W.W.
      • Zou Y.
      • Kang Z.
      • Liang J.G.
      • He H.Y.
      • Yang Q.T.
      Endoscopic anatomical study of the trans-lateral molar approach to the infratemporal fossa.
      ,
      • Torres-Gaya J.
      • Puche-Torres M.
      • Marqués-Mateo M.
      • García Callejo F.J.
      Transoral (transvestibular-paramandibular) endoscopic approach for benign tumours in the infratemporal fossa.
      ,
      • Chan J.Y.
      • Li R.J.
      • Lim M.
      • Hinojosa A.Q.
      • Boahene K.D.
      Endoscopic transvestibular paramandibular exploration of the infratemporal fossa and parapharyngeal space: a minimally invasive approach to the middle cranial base.
      ] has been reported. Moreover, recent literature has presented a purely transnasal transpterygoid approach for managing lesions located in the PPS/ITF, reducing the functional and cosmetic morbidity related to open surgery [
      • Wasano K.
      • Yamamoto S.
      • Tomisato S.
      • Kawasaki T.
      • Ogawa K.
      Modified endoscopic transnasal-transmaxillary-transpterygoid approach to parapharyngeal space tumor resection.
      ,
      • Karkas A.
      • Zimmer L.A.
      • Theodosopoulos P.V.
      • Keller J.T.
      • Prades J.M.
      Endonasal endoscopic approach to the pterygopalatine and infratemporal fossae.
      ,
      • Theodosopoulos P.V.
      • Guthikonda B.
      • Brescia A.
      • Keller J.T.
      • Zimmer L.A.
      Endoscopic approach to the infratemporal fossa: anatomic study.
      ,
      • Herzallah I.R.
      • Germani R.
      • Casiano R.R.
      Endoscopic transnasal study of the infratemporal fossa: a new orientation.
      ]. EEA provides improved access to the anterior and medial portions of the superior PPS and medial portion of the superior ITF; however, in cases of lesions with lateral extension toward the ITF and inferior extension toward the PPS, EEA alone seems inadequate to permit optimal control of the lesions [
      • Theodosopoulos P.V.
      • Guthikonda B.
      • Brescia A.
      • Keller J.T.
      • Zimmer L.A.
      Endoscopic approach to the infratemporal fossa: anatomic study.
      ,
      • Van Rompaey J.
      • Suruliraj A.
      • Carrau R.
      • Panizza B.
      • Solares C.A.
      Access to the parapharyngeal space: an anatomical study comparing the endoscopic and open approaches.
      ]. To overcome this limitation, a multiportal transmaxillary approach combined with EEA [
      • Liu Q.
      • Wang H.
      • Zhao W.
      • Song X.
      • Sun X.
      • Yu H.
      • et al.
      Endoscopic transnasal transmaxillary approach to the upper parapharyngeal space and the skull base.
      ,
      • Truong H.Q.
      • Sun X.
      • Celtikci E.
      • Borghei-Razavi H.
      • Wang E.W.
      • Snyderman C.H.
      • et al.
      Endoscopic anterior transmaxillary "transalisphenoid" approach to Meckel's cave and the middle cranial fossa: an anatomical study and clinical application.
      ,
      • Martinez-Perez R.
      • Aref M.
      • Ramakhrisnan V.
      • Youssef A.S.
      Combined biportal unilateral endoscopic endonasal and endoscopic anterior transmaxillary approach for resection of lesions involving the infratemporal fossa.
      ] or multiportal transoral approach combined with EEA [
      • Turri-Zanoni M.
      • Battaglia P.
      • Dallan I.
      • Locatelli D.
      • Castelnuovo P.
      Multiportal combined transnasal transoral transpharyngeal endoscopic approach for selected skull base cancers.
      ,
      • Sreenath S.B.
      • Rawal R.B.
      • Zanation A.M.
      The combined endonasal and transoral approach for the management of skull base and nasopharyngeal pathology: a case series.
      ,
      • Carrau R.L.
      • Prevedello D.M.
      • de Lara D.
      • Durmus K.
      • Ozer E.
      Combined transoral robotic surgery and endoscopic endonasal approach for the resection of extensive malignancies of the skull base.
      ,
      • Deganello A.
      • Ferrari M.
      • Paderno A.
      • Turri-Zanoni M.
      • Schreiber A.
      • Mattavelli D.
      • et al.
      Endoscopic-assisted maxillectomy: operative technique and control of surgical margins.
      ,
      • Schreiber A.
      • Mattavelli D.
      • Accorona R.
      • Rampinelli V.
      • Ferrari M.
      • Grammatica A.
      • et al.
      Endoscopic-assisted multi-portal compartmental resection of the masticatory space in oral cancer: anatomical study and preliminary clinical experience.
      ] has been developed (Fig. 2).
      Fig 2
      Fig. 2A 13-year-old male patient with recurrent juvenile angiofibroma treated with “a multiportal transcranial / transoral approach combined with endoscopic endonasal approach”., (a) T1 contrast-enhanced magnetic resonance imaging showing the recurrent tumor. The lesion was totally removed by a multiport approach using an orbit-zygomatic approach (b) for a cavernous sinus lesion (1), transvestibular approach through a gingival incision (c) for an inferior temporal fossa lesion (2), and transnasal approach for a nasal and pterygopalatine fossa lesion (3)., For the transoral approach, (c) transvestibular approach via the retro-posterior wall of the maxillary sinus are used. Asterisk indicates the posterolateral wall of the maxillary sinus on the right side., (d) The three approaches show that it is possible to manipulate the lesion from various angles., Two bipolar electrocoagulation forceps (one by orbitozygomatic approach (#1) and the other by transvestibular approach (#2)) and two suction tubes (one by orbitozygomatic approach (#1) and the other by transnasal approach (#3)) are used to stop bleeding from the pterygoid venous plexus. The endoscope is inserted transorally.
      In the former approach, the ipsilateral sublabial antrostomy (Caldwell-Luc procedure) is used, which is helpful for exposing a large surgical field in the upper and lateral portions of the PPS/ITF [
      • Liu Q.
      • Wang H.
      • Zhao W.
      • Song X.
      • Sun X.
      • Yu H.
      • et al.
      Endoscopic transnasal transmaxillary approach to the upper parapharyngeal space and the skull base.
      ,
      • Martinez-Perez R.
      • Aref M.
      • Ramakhrisnan V.
      • Youssef A.S.
      Combined biportal unilateral endoscopic endonasal and endoscopic anterior transmaxillary approach for resection of lesions involving the infratemporal fossa.
      ], and even to the Meckel cave [
      • Truong H.Q.
      • Sun X.
      • Celtikci E.
      • Borghei-Razavi H.
      • Wang E.W.
      • Snyderman C.H.
      • et al.
      Endoscopic anterior transmaxillary "transalisphenoid" approach to Meckel's cave and the middle cranial fossa: an anatomical study and clinical application.
      ]. With this approach, surgeons can access the lesions without the need to transect the Vidian nerve or perform a posterior nasal septectomy [
      • Martinez-Perez R.
      • Aref M.
      • Ramakhrisnan V.
      • Youssef A.S.
      Combined biportal unilateral endoscopic endonasal and endoscopic anterior transmaxillary approach for resection of lesions involving the infratemporal fossa.
      ].
      For larger benign lesions, malignant lesions that require a greater safety margin, or those with inferior extension, the latter approach is preferred. This transoral approach has several names, including the transvestibular approach [
      • Chan J.Y.
      • Li R.J.
      • Lim M.
      • Hinojosa A.Q.
      • Boahene K.D.
      Endoscopic transvestibular paramandibular exploration of the infratemporal fossa and parapharyngeal space: a minimally invasive approach to the middle cranial base.
      ], far-medial transoral approach [
      • Patwa H.S.
      • Yanez-Siller J.C.
      • Gomez Galarce M.
      • Otto B.A.
      • Prevedello D.M.
      • Carrau R.L.
      Analysis of the far-medial transoral endoscopic approach to the infratemporal fossa.
      ], trans-lateral molar approach [
      • Cai W.W.
      • Zou Y.
      • Kang Z.
      • Liang J.G.
      • He H.Y.
      • Yang Q.T.
      Endoscopic anatomical study of the trans-lateral molar approach to the infratemporal fossa.
      ], and transvestibular-paramandibular approach [
      • Torres-Gaya J.
      • Puche-Torres M.
      • Marqués-Mateo M.
      • García Callejo F.J.
      Transoral (transvestibular-paramandibular) endoscopic approach for benign tumours in the infratemporal fossa.
      ]. In each approach, there are slight differences in oral incisions, but the surgical corridor is made between the lateral maxilla and medial mandible without cutting any bones. The multiportal approach obtained by combining EEA with endoscopic transoral surgery [
      • Turri-Zanoni M.
      • Battaglia P.
      • Dallan I.
      • Locatelli D.
      • Castelnuovo P.
      Multiportal combined transnasal transoral transpharyngeal endoscopic approach for selected skull base cancers.
      ] or transoral robotic surgery [
      • Sreenath S.B.
      • Rawal R.B.
      • Zanation A.M.
      The combined endonasal and transoral approach for the management of skull base and nasopharyngeal pathology: a case series.
      ,
      • Carrau R.L.
      • Prevedello D.M.
      • de Lara D.
      • Durmus K.
      • Ozer E.
      Combined transoral robotic surgery and endoscopic endonasal approach for the resection of extensive malignancies of the skull base.
      ] has been demonstrated to provide excellent exposure for selected malignancies that occur in the PPS/ITF. By means of endoscopic assistance through both coridors, surgical landmarks such as the Eustachian tube, mandibular nerve (V3), temporal muscle, medial pterygoid muscle [
      • Dallan I.
      • Seccia V.
      • Muscatello L.
      • Lenzi R.
      • Castelnuovo P.
      • Bignami M.
      • et al.
      Transoral endoscopic anatomy of the parapharyngeal space: a step-by-step logical approach with surgical considerations.
      ], styloglossus muscle [
      • Dallan I.
      • Seccia V.
      • Muscatello L.
      • Lenzi R.
      • Castelnuovo P.
      • Bignami M.
      • et al.
      Transoral endoscopic anatomy of the parapharyngeal space: a step-by-step logical approach with surgical considerations.
      ], stylopharyngeal muscle [
      • Dallan I.
      • Seccia V.
      • Muscatello L.
      • Lenzi R.
      • Castelnuovo P.
      • Bignami M.
      • et al.
      Transoral endoscopic anatomy of the parapharyngeal space: a step-by-step logical approach with surgical considerations.
      ], and most importantly, the course of the ICA from the parapharyngeal portion to the lateral genu, petrous portion, and foramen lacerum are identified, and their combined use can minimize the morbidity of surgery and provide a safe and effective alternative to traditional open surgeries or endoscopic-assisted transoral surgery.
      The multiportal transoral approach combined with EEA has also been used in the treatment of head and neck cancers, such as nasopharyngeal [
      • Sreenath S.B.
      • Rawal R.B.
      • Zanation A.M.
      The combined endonasal and transoral approach for the management of skull base and nasopharyngeal pathology: a case series.
      ], oral [
      • Schreiber A.
      • Mattavelli D.
      • Accorona R.
      • Rampinelli V.
      • Ferrari M.
      • Grammatica A.
      • et al.
      Endoscopic-assisted multi-portal compartmental resection of the masticatory space in oral cancer: anatomical study and preliminary clinical experience.
      ] and maxillary sinus cancers [
      • Deganello A.
      • Ferrari M.
      • Paderno A.
      • Turri-Zanoni M.
      • Schreiber A.
      • Mattavelli D.
      • et al.
      Endoscopic-assisted maxillectomy: operative technique and control of surgical margins.
      ]. In such treatment, endoscopes are often used as an adjunct; however, cutting of the pterygoid plates with diamond burs via the transnasal approach seems to be a very useful technique under endoscopic guidance [
      • Hanazawa T.
      • Yamasaki K.
      • Chazono H.
      • Okamoto Y.
      Endoscopic contralateral transmaxillary approach for pterygoid process osteotomy in total maxillectomy: a technical case report.
      ]. In other words, there is no need to insist on purely endoscopic surgery, but it may be useful to use it effectively in areas that require magnification to remove deep lesions.
      Furthermore, there is no need to be concerned about using the transnasal approach, and a multiportal endoscopic approach without a transnasal approach, in which a facial incision is combined with a transvestibular approach, is also useful [
      • Youssef A.S.
      • Arnone G.D.
      • Farell N.F.
      • Thompson J.A.
      • Ramakrishnan V.R.
      • Gubbels S.
      • et al.
      The combined endoscopic endonasal far medial and open postauricular transtemporal approaches as a lesser invasive approach to the jugular foramen: anatomic morphometric study with case illustration.
      ] (Fig. 3).
      Fig 3
      Fig. 3A 67-year-old female patient with a schwannoma extending form the temporal fossa to the infratemporal fossa on the right side treated with “a multiportal endoscopic approach without a transnasal approach”., (a) T1 contrast-enhanced magnetic resonance imaging showing that the tumor (*) extends from the temporal fossa to the inferior temporal fossa on the right side. The lesion is completely removed by a multiportal approach with transfacial approach and transvestibular approach (yellow arrows)., (b) Surgical view of a multi-port approach using a transfacial approach with a small incision on the face (c) and a transvestibular approach (d), (d) The arrow indicates the tail of the tumor. #: Posterolateral wall of the maxillary sinus on the right side.

      3.2.2 Petrous apex

      The petrous apex is the pyramid-shaped anteromedial part of the petrous part of the temporal bone, which articulates with the posterior aspect of the greater wing of the sphenoid and occipital bones. Rarely, lesions such as cholesterin granuloma, chordoma, and chondrosarcoma develop or extend to the petrous apex. Surgical management of petrous apex lesions is challenging because of the presence of critical neurovascular structures, including the petrous part of the ICA [
      • Kassam A.B.
      • Vescan A.D.
      • Carrau R.L.
      • Prevedello D.M.
      • Gardner P.
      • Mintz A.H.
      • et al.
      Expanded endonasal approach: vidian canal as a landmark to the petrous internal carotid artery.
      ]. Transcranial approaches are traditional, but EEA is replacing open surgery as a less invasive alternative. However, EEA is also challenging to perform because it is necessary to mobilize the paraclival ICA laterally with complete bony decompression and transection of the fibrocartilage of the foramen lacerum to reach the lesion and gain working space [
      • Taniguchi M.
      • Akutsu N.
      • Mizukawa K.
      • Kohta M.
      • Kimura H.
      • Kohmura E.
      Endoscopic endonasal translacerum approach to the inferior petrous apex.
      ,
      • Patel C.R.
      • Wang E.W.
      • Fernandez-Miranda J.C.
      • Gardner P.A.
      • Snyderman C.H.
      Contralateral transmaxillary corridor: an augmented endoscopic approach to the petrous apex.
      ], which introduces considerable risk of ICA injury.
      Adding a corridor made by a “contralateral” sublabial transmaxillary approach (the Caldwell Luc approach) with EEA can provide a straight access to a lesion located posterior to the petrous ICA and/or lateral to the paraclival ICA [
      • Patel C.R.
      • Wang E.W.
      • Fernandez-Miranda J.C.
      • Gardner P.A.
      • Snyderman C.H.
      Contralateral transmaxillary corridor: an augmented endoscopic approach to the petrous apex.
      ,
      • Lawrence J.D.
      • Marsh R.
      • Turner M.T.
      Contralateral transmaxillary approach for resection of chondrosarcoma of the petrous apex: a case report.
      ,
      • Wang W.H.
      • Lan M.Y.
      • Snyderman C.H.
      • Gardner P.A.
      Combined endoscopic endonasal and contralateral transmaxillary approach for petrous cholesteatoma: 2-dimensional operative video.
      ] (Fig. 4). Compared to purely EEA as an ipsilateral transmaxillary transpterygoid approach, the multiportal contralateral transmaxillary approach combined with EEA provides direct visualization and enables surgeons to use straight instruments and increases accessibility to the lesion without the need for manipulation of the paraclival ICA, resulting in easier and safer instrumentation and a decrease in the potential risk of ICA injury [
      • Patel C.R.
      • Wang E.W.
      • Fernandez-Miranda J.C.
      • Gardner P.A.
      • Snyderman C.H.
      Contralateral transmaxillary corridor: an augmented endoscopic approach to the petrous apex.
      ,
      • Lawrence J.D.
      • Marsh R.
      • Turner M.T.
      Contralateral transmaxillary approach for resection of chondrosarcoma of the petrous apex: a case report.
      ,
      • Wang W.H.
      • Lan M.Y.
      • Snyderman C.H.
      • Gardner P.A.
      Combined endoscopic endonasal and contralateral transmaxillary approach for petrous cholesteatoma: 2-dimensional operative video.
      ].
      Fig 4
      Fig. 4A 52-year-old male patient with a chondrosarcoma extending form the petrous apex to the clivus on the left side treated with "a multiportal contralateral transmaxillary approach combined with endoscopic endonasal approach”., (a) Schematic view of multiportal contralateral transmaxillary approach combined with endoscopic endonasal approach, which can provide a straight instrument access to the lesion located posterior to the petrous ICA (dotted red line), (b) Anterior wall of maxillary sinus on the right side (contralateral side) is removed by Caldwell-Luc antrostomy. Surgical instruments such as curette and suction are inserted through this contralateral corridor., (c) 45° endoscopic view from the left side (ipsilateral side). Suction tube (#) is inserted from the contralateral transmaxillary corridor to the petrous apex behind the paraclival ICA (*). The red filled circle in the left figure (a) shows the position of the tip of the suction tube. Note that the entire suction tube entering the petrous apex posterior to the paraclival ICA (*) and foramen lacerum (**) can be seen with the endoscope.

      4. Future directions

      ESBS has gained consensus as a primary choice for surgical approaches to the ventral skull base and continues to evolve. For this decade, the concern regarding the outcomes of ESBS in benign lesions or early-stage malignancies has become complete resection with minimal invasiveness. The preservation of nasal function, including olfaction, will be included as an essential issue in the next decade. The combination of multi-corridor approaches has the potential for complete resection with low morbidity and extensive pathologies. The multiportal approach requires multiple surgeons, which indicates that the ergonomics of surgeons’ positions will become a matter for ESBS in the next decade. Along this trend, robotic-assisted approaches will be developed in this field. To ensure the efficacy of these novel techniques and approaches, an ongoing critical evaluation is crucial.

      Ethics statement

      This study was approved by the Ethics Committee of Kyoto University Hospital (number: R-2805).

      Declaration of Competing Interest

      The authors report no conflicts of interest related to this research.

      Acknowledgments

      We thank Dr. Masahiro Tanji at Kyoto University for clinical recording and valuable discussions on surgical procedures.

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