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Department of Otolaryngology, Head and Neck Surgery, Graduate School of Medicine, Kyoto University, 54 Kawaharacho, Shogoin, Sakyoku, Kyoto 606-8507, Japan
Department of Otolaryngology, Head and Neck Surgery, Graduate School of Medicine, Kyoto University, 54 Kawaharacho, Shogoin, Sakyoku, Kyoto 606-8507, Japan
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.
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 [
]. 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 [
]. 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 [
]. 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 [
], 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 [
], supporting the validity of ESBS. Importantly, not only surgical outcomes but also nasal morbidity after ESBS were systematically reviewed.
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 [
]. 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 [
]. 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 [
]. The proportion for olfactory dysfunction after microscopic pituitary surgery was 39.7%, while that after endoscopic surgery with flap elevation was 14.4% [
], 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 [
], 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 [
]. 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 [
]. 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 [
]. 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 [
]. 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 [
]. 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 [
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 [
], 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 [
]. 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 [
]. 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 [
]. 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.
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 [
]. 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. [
]. 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 [
]. 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 [
] lesions. Regarding the superior orbital fissure (SOF), TOEA is superior in accessing the lateral two-thirds of the SOF and the superolateral intraconal space [
]. 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 [
]. 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 [
]. 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 [
] and the requirement for angled endoscopes and instrumentation can be minimized, providing less disorientation, optimal visualization, illumination, and magnification [
]. 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 [
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.
Endoscopic endonasal transclival approach versus dual transorbital port technique for clip application to the posterior circulation: a cadaveric anatomical and cerebral circulation simulation study.
Dual endoscopic endonasal transsphenoidal and precaruncular transorbital approaches for clipping of the cavernous carotid artery: a cadaveric simulation.
Combined and simultaneous endoscopic endonasal and transorbital surgery for a Meckel's cave schwannoma: technical nuances of a mini-invasive, multiportal approach.
]. 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 [
]. 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 [
Combined and simultaneous endoscopic endonasal and transorbital surgery for a Meckel's cave schwannoma: technical nuances of a mini-invasive, multiportal approach.
]. 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 [
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) [
Management of parapharyngeal space tumors with transparotid-transcervical approach: analysis of prognostic factors related with disease-control and functional outcomes.
] and their combinations, have been traditionally performed. Recently, to provide minimally invasive approaches to PPS/ITF lesions, endoscopic-assisted transoral surgery [
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 [
]. 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 [
Endoscopic anterior transmaxillary "transalisphenoid" approach to Meckel's cave and the middle cranial fossa: an anatomical study and clinical application.
Combined biportal unilateral endoscopic endonasal and endoscopic anterior transmaxillary approach for resection of lesions involving the infratemporal fossa.
Endoscopic-assisted multi-portal compartmental resection of the masticatory space in oral cancer: anatomical study and preliminary clinical experience.
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 [
Combined biportal unilateral endoscopic endonasal and endoscopic anterior transmaxillary approach for resection of lesions involving the infratemporal fossa.
Endoscopic anterior transmaxillary "transalisphenoid" approach to Meckel's cave and the middle cranial fossa: an anatomical study and clinical application.
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 [
Endoscopic transvestibular paramandibular exploration of the infratemporal fossa and parapharyngeal space: a minimally invasive approach to the middle cranial base.
]. 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 [
] 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 [
], 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 [
Endoscopic-assisted multi-portal compartmental resection of the masticatory space in oral cancer: anatomical study and preliminary clinical experience.
]. 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 [
]. 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 [
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. 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.
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 [
]. 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 [
], 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 [
] (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 [
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.
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.
References
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Carrau R.L.
Endoscopic endonasal transsphenoidal surgery: experience with 50 patients.
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.
Endoscopic endonasal transclival approach versus dual transorbital port technique for clip application to the posterior circulation: a cadaveric anatomical and cerebral circulation simulation study.
Dual endoscopic endonasal transsphenoidal and precaruncular transorbital approaches for clipping of the cavernous carotid artery: a cadaveric simulation.
Combined and simultaneous endoscopic endonasal and transorbital surgery for a Meckel's cave schwannoma: technical nuances of a mini-invasive, multiportal approach.
Management of parapharyngeal space tumors with transparotid-transcervical approach: analysis of prognostic factors related with disease-control and functional outcomes.
Endoscopic transvestibular paramandibular exploration of the infratemporal fossa and parapharyngeal space: a minimally invasive approach to the middle cranial base.
Endoscopic anterior transmaxillary "transalisphenoid" approach to Meckel's cave and the middle cranial fossa: an anatomical study and clinical application.
Combined biportal unilateral endoscopic endonasal and endoscopic anterior transmaxillary approach for resection of lesions involving the infratemporal fossa.
Endoscopic-assisted multi-portal compartmental resection of the masticatory space in oral cancer: anatomical study and preliminary clinical experience.
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.
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