Adv Ther (2022) 39:2379–2397 https://doi.org/10.1007/s12325-022-02080-x REVIEW The Selective Role of Open and Endoscopic Approaches for Sinonasal Malignant Tumours Fernando López . Jatin P. Shah . Jonathan J. Beitler . Carl H. Snyderman . Valerie Lund . Cesare Piazza . Antti A. Mäkitie . Orlando Guntinas-Lichius . Juan P. Rodrigo . Luiz P. Kowalski . Miquel Quer . Ashok Shaha . Akihiro Homma . Alvaro Sanabria . Renata Ferrarotto . Anne W. M. Lee . Victor H. F. Lee . Alessandra Rinaldo . Alfio Ferlito Received: January 12, 2022 / Accepted: February 7, 2022 / Published online: March 30, 2022 Ó The Author(s) 2022 ABSTRACT debated. The present review aims to summarize the current state of knowledge on the utility of Endoscopic endonasal surgery has been demon- open approaches to resect sinonasal malignant strated to be effective in the treatment of selected tumours. Published comparative studies and cases of sinonasal cancers. However, in cases of meta-analyses suggest comparable oncological locally advanced neoplasms, as well as recur- results with lower morbidity for the endoscopic rences, the most appropriate approach is still approaches, but selection biases cannot be excluded. After a critical analysis of the available This article was written by members of the International literature, it can be concluded that endoscopic Head and Neck Scientific Group (www.IHNSG.com). surgery for selected lesions allows for F. López (&)  J. P. Rodrigo V. Lund Department of Otolaryngology, Hospital The Royal National Throat Nose and Ear Hospital, Universitario Central de Asturias, Oviedo, Spain UCLH Foundation Trust, London, UK e-mail: flopez_1981@yahoo.es C. Piazza F. López  J. P. Rodrigo Department of Otorhinolaryngology - Head and Instituto Universitario de Oncologı́a del Principado Neck Surgery, ASST Spedali Civili di Brescia, de Asturias, Instituto de Investigación Sanitaria del University of Brescia, Italy, Brescia, Italy Principado de Asturias and CIBERONC, ISCIII, University of Oviedo, Oviedo, Spain A. A. Mäkitie Department of Otorhinolaryngology, Head and J. P. Shah  A. Shaha Neck Surgery, University of Helsinki and Helsinki Head and Neck Service, Department of Surgery, University Hospital, Helsinki, Finland Memorial Sloan-Kettering Cancer Center, New York, NY, USA O. Guntinas-Lichius Department of Otorhinolaryngology, Institute of J. P. Shah Phoniatry/Pedaudiology, Jena University Hospital, Department of Oncology, Radiotherapy and Plastic Jena, Germany Surgery, Sechenov University, Moscow, Russia L. P. Kowalski J. J. Beitler Department of Otorhinolaryngology, Head and Departments of Radiation Oncology, Maine General Neck Surgery, A.C. Camargo Cancer Center, São Hospital, Augusta, Maine, USA Paulo, Brazil C. H. Snyderman L. P. Kowalski Department of Otolaryngology, University of Department of Head and Neck Surgery, University Pittsburgh School of Medicine, Pittsburgh, PA, USA of São Paulo Medical School, São Paulo, Brazil 2380 Adv Ther (2022) 39:2379–2397 oncologically safe resections with decreased There appears to be no difference in risk of morbidity. However, when endoscopic endonasal unfavourable outcomes with endoscopic surgery is contraindicated and definitive compared to open approaches in chemoradiotherapy is not appropriate, craniofa- appropriately selected patients. cial and transfacial approaches remain the best therapeutic option. When endoscopic endonasal surgery is contraindicated and conservative chemoradiotherapy is not appropriate, Keywords: Craniofacial Resection; Endoscopy; craniofacial and transfacial approaches Maxillectomy; Paranasal Sinus Cancer; still represent an option to consider, Sinonasal Malignant Tumours; Skull Base despite the non-negligible morbidity. Traditional open surgical approaches have become less destructive, with surgeons Key Summary Points disguising the incisions. Sinonasal malignancies, in general, are rare tumours with poor prognosis, despite advances in surgical techniques, radiotherapy and systemic therapy. INTRODUCTION The therapeutic modality used should be tailored individually according to tumour The sinonasal cavities represent an anatomical stage, histology, previous treatments and region affected by a variety of tumours with patient conditions as well as the clinical, aetiological, pathological, and genetic multidisciplinary team preferences. features distinct from tumours at other sites of Surgery is the mainstay of treatment both the upper aerodigestive tract [1]. Neither in management of the primary tumour smoking nor alcohol nor human papilloma and recurrences. Currently, whenever virus (HPV) is definitively associated with sino- possible, endoscopic approaches should nasal cancers [2]. As a result of their insidious be used in order to minimize the surgical symptoms in the early stages, patients are fre- morbidity for the patients. quently diagnosed with locally advanced disease. M. Quer A. W. M. Lee  V. H. F. Lee Department of Otolaryngology, Hospital Santa Creu Department of Clinical Oncology, Li Ka Shing i Sant Pau, Barcelona, Spain Faculty of Medicine, The University of Hong Kong, Pok Fu Lam, Hong Kong A. Homma Department of Otolaryngology, Head and Neck A. W. M. Lee  V. H. F. Lee Surgery, Faculty of Medicine and Graduate School of Clinical Oncology Center, The University of Hong Medicine, Hokkaido University, Sapporo, Hokkaido, Kong-Shenzhen Hospital, Shenzhen, People’s Japan Republic of China A. Sanabria A. Rinaldo Department of Surgery, School of Medicine, University of Udine School of Medicine, Udine, Italy Universidad de Antioquia/Hospital Universitario San Vicente Fundación, Medellı́n, Colombia A. Ferlito Coordinator of the International Head and Neck A. Sanabria Scientific Group, Padua, Italy CEXCA Centro de Excelencia en Enfermedades de Cabeza y Cuello, Medellı́n, Colombia R. Ferrarotto Department of Thoracic/Head and Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA Adv Ther (2022) 39:2379–2397 2381 Based on evidence from a number of retro- particularly in the case of poorly differentiated spective studies, it is commonly accepted that a neoplasms [9]. On the other hand, the growing complete surgical resection, when feasible, experience acquired in endonasal endoscopic often combined with adjuvant therapies [ra- surgery has led to its widespread use in the diotherapy (RT) with or without chemotherapy surgical treatment of selected SNMT and the (ChT)], is the mainstay of treatment of sinona- concept of tumour ‘‘oriented disassembling’’ has sal malignant tumours (SNMT). The therapeutic definitively demonstrated its validity in terms modality should be tailored according to of oncological safety with results comparable to tumour stage, histology, previous treatments, those of en bloc resection [10–14]. However, in patient comorbidities as well as the multidisci- interpreting published reports, one needs to be plinary team preferences [3, 4]. Numerous cognizant of the fact that there is significant improvements in modern imaging have made selection bias in selecting a particular surgical diagnosis and surgical planning more accurate approach. Thus, comparison of various surgical but imaging can also be misleading. Also, con- approaches with outcomes would be inappro- temporary technical advances in surgical tools, priate. Further, traditional open surgical including high-resolution endoscopes, powered approaches, such as maxillectomy, with the instrumentation and neuronavigation, facilitate standard Weber Fergusson incision, have more extensive and safer tumour resections become less deforming, with surgeons modify- with reduced risk of neurovascular injuries [5]. ing the standard incision respecting the nasal However, as a result of close proximity to criti- subunits or avoiding the incisions altogether by cal neurovascular structures, variable sinonasal using facial-degloving approaches, when feasi- anatomy, challenging reconstruction of the ble for selected patients and minimizing mor- skull base and cosmesis surgical challenges still bidity with regional or free flap reconstruction abound [1, 6]. [15, 16]. Once multidisciplinary teams have decided There is no high-level clinical evidence to on surgical resection, the choice of open versus guide decision-making and only a few studies endoscopic procedure should be based on the have compared open versus endoscopic resec- extent of the tumour as well as the patient’s tions using historical records. Published studies general condition. Consensus on contraindica- have mostly been single-institution, retrospec- tions to an exclusive endoscopic approach tive studies hampered by limited sample sizes includes extensive brain or orbital invasion, [17–20]. Indirect comparisons lead to the pos- infiltration of the superficial tissues (skin, nasal sibility of selection bias in establishing the bones, and subcutaneous tissue), hard or soft indication for the type of approach. Tumours of palate invasion, extensive involvement of the small volume which are accessible without frontal sinus, extensive erosion of the anterior, involving critical structures are usually selected inferior, or lateral bony walls of the maxillary for endonasal endoscopic surgery. It is plausible sinus, extensive involvement of the lacrimal that the improved outcomes seen with endo- duct, and significant extension to the scopic surgery are a result of this selection bias. infratemporal fossa, masticatory, and parapha- The study by Fu et al. [21] illustrates the con- ryngeal spaces [7]. It should be noted that a sequences of heterogeneity in the management hybrid, combined cranioendoscopic approach of SNMT. As a result of imbalance in the num- may be beneficial in improving surgical resec- bers of various groups, their cohort was largely tion for selected complex lesions as well as biased toward an open approach (greater than multiportal approaches [8]. 80%). In addition, the histological diversity of Though surgery is generally still the work- SNMT, which implies different tumours with horse of the therapeutic armamentarium, his- different biological behaviour, makes compar- tology-driven protocols are now recognized as isons tenuous [22–24]. The purpose of this state-of-the-art for management, which has comprehensive literature review is to present contributed to the reduction in surgical resec- the most current evidence on indications and tion as an upfront treatment strategy, contraindications for traditional open surgery. 2382 Adv Ther (2022) 39:2379–2397 This article is based on previously conducted ENDOSCOPIC APPROACHES studies and does not involve any new studies of human or animal subjects performed by any of The development of new endoscopic tech- the authors. niques, as well as the availability of specific instrumentation for the management of chal- lenging regions such as the frontal [26], maxil- SURGICAL TRENDS lary sinus [27, 28] and infratemporal fossa [29], and the increase in surgical expertise and skills The use of endoscopic techniques is rising, and have progressively reduced the need for exter- consequently the utility of open techniques has nal approaches to achieve radical SNMT resec- fallen. Husain et al. [25], in 2019, using the tion, even for locally advanced cancers. The National Cancer Database (NCDB), identified description of endoscopic approaches and their trends and outcomes associated with surgical indications is beyond of the scope of this management of SNMT. They reported that from manuscript. a total of 10,193 patients with SNMT treated between 2010 and 2015, about 71.9% of patients had an open approach (most of them INDICATIONS FOR OPEN with T3–T4 tumours) and 28.1% had a purely APPROACHES endoscopic procedure (most of them with T1–T2 tumours). This study included patients Infiltration of the dura over the orbital roof or treated between 2010 and 2015, so the fig- infiltration of the brain parenchyma is usually ures may well be different today. Hence, in a considered a contraindication to the purely more recent meta-analysis carried out by Lu endoscopic approach as craniotomy could pro- et al. in 2019 [24], the differences between the vide better control of surgical margins [30]. percentages of use of both approaches are However, limited dural infiltration has been smaller. They included 900 patients in total resected using purely endoscopic techniques, where endoscopic and open resections were but this needs to be undertaken with caution utilized in 399 (44%) and 501 (56%) cases, [31]. This paper underlines that invasion of the respectively. In another systematic review and dura is a more important factor to be considered meta-analysis, Jiang et al. [23] found that out of than limited brain invasion, as achieving free a sample of 1373 patients, 47.6% were operated margins in the dura mater is even more chal- on endoscopically (mainly early-stage tumours) lenging and a frequent site of local failure. This and 52.4% by an open approach (mainly exclusive endoscopic approach was associated advanced-stage tumours). These data seem to with limited morbidity, with few minor com- confirm the trend towards a more frequent use plications and no major postoperative prob- of endoscopic surgery mostly in early-stage lems. However, even Mattavelli et al.’s paper tumours. Nonetheless, open craniofacial or recommended an open approach in case of transfacial procedures still find indications in tumour invasion largely exceeding the rectus cases of advanced-stage disease. Table 1 shows gyrus, the medial orbital gyrus, or invading into indications and contraindications of surgical the sagittal sinus [31]. approaches according to the anatomical sites Infiltration of the orbital contents is a poor involved. These indications may not be accep- prognostic factor in terms of local control and ted by all head and neck surgeons, as personal survival [32]. Diagnosis can be challenging, and experience may affect these general recom- extrinsic compression can be difficult to distin- mendations. In addition, the anatomical char- guish from true invasion of orbital contents acteristics of each patient may influence the despite imaging techniques [32, 33]. In a study type of approach indicated. of 82 patients by Patel et al. [34], the positive predictive value (PPV) of computed tomography (CT) scanning for periorbital involvement from an experienced institution was only 33%, and Adv Ther (2022) 39:2379–2397 2383 Table 1 Indications and contraindications for surgical approaches based on anatomical sites involved Location Endoscopic approach Open approach Unresectable Maxillary sinus Medial maxillary wall and/or Lateral and/or inferior wall involvement orbital floor involvement Hard and/or soft palate involvement Sphenoid sinus Anterior wall involvement Planum sphenoidale involvementa Posterior/lateral wall involvement Cavernous sinus involvement Optical chiasm involvement Internal carotid artery involvement Frontal sinus Lesions abutting into the sinus Erosion of the anterior or posteriora wall Lesions from the lower half of Lesions from the upper half of the sinusa the sinus Extensive involvement of the sinusa Skin or subcutaneous tissue involvement Lateral supraorbital attachment in laterally pneumatized sinusa Nasal bone Nasal bone involvement Orbit Erosion of the lamina Invasion of the anterior 2/3 orbit Orbital apex papyracea Extension beyond mid-plane of orbital roof involvement Invasion of periorbita and/or focal invasion of extraconal periorbital fat Dura and brain Limited dural infiltration Dural infiltration extended laterally over the Brain infiltration with Olfactory bulb involvement orbital roofs or posteriorly beyond planum vascular a sphenoidale involvement Focal midline brain invasion Brain infiltrationa Infratemporal and Pterygopalatine space Massive infratemporal fossa involvement Parapharyngeal pterygopalatine involvement Parapharyngeal space involvement internal carotid fossa Limited infratemporal fossa artery involvement Masticatory space involvement involvement Skin Facial skin involvement a A cranioendoscopic approach may be considered 2384 Adv Ther (2022) 39:2379–2397 the negative predictive value (NPV) was only exenteration may improve oncological out- 63%. The European Position Paper on Endo- comes of these conditions, considering that scopic Management of Tumours of Nose, Para- postoperative RT does not improve the results of nasal Sinus and Skull Base [11] noted that while radical surgery while increasing the risk of a MRI can correctly predict the presence of per- post-treatment non-functional eye [43]. Inva- ineural spread with 95% sensitivity, it can only sion of the extrinsic eye muscles, the orbital map the entire extent of spread in around 60% apex or the globe seems to be a clear indication of cases. Orbit management has been discussed for orbital exenteration [39]. However, the lack by several authors and various classifications of precision about the degree of orbital invasion have been proposed to establish performance on imaging often does not always allow a con- criteria [32, 35–39]. When necessary, surgical sensus for preoperative counselling so frozen removal of the orbital contents can be per- sections remain essential for the most accurate formed. Orbital exenteration involves removal intraoperative decision-making process. How- of the entire contents of the orbit and eyelids ever, the limitations of intraoperative biopsy whereas the term orbital clearance is used when must be also considered, as there are contents in the eyelids and palpebral conjunctiva are pre- the orbit that cannot be sampled without served. With respect to orbital invasion, the causing damage. Intraoperative assessment of surgical indications have evolved considerably periorbital invasion was only slightly better over time. Initially, invasion of the orbital than imaging, with a PPV of 34% and NPV of periosteum was an indication for orbital exen- 70% [34]. Tumour histology will also influence teration. However, since oncological outcomes the decision to undertake orbital exenteration were similar in cases where the orbit was pre- depending on whether the disease is otherwise served, indications for orbital exenteration resectable and patient curable. Castelnuovo became more limited [37, 40, 41]. Some authors et al. [39] have proposed an algorithm which argue that orbital preservation is oncologically stratifies by grade of orbital invasion, grade of safe even in case of periorbital and extraconal tumour and, in the case of high-grade tumours, fat invasion [42], while others argue that orbital the likely response to ChT. Fig. 1 Proposed surgical treatment algorithm according to anatomical location Adv Ther (2022) 39:2379–2397 2385 Induction ChT (mostly combinations of fossa or maxillary sinuses [49]. They are taxanes and platinum) has been considered an aggressive lesions with a tendency to local option for orbital preservation since the invasion and perineural spread, so open pioneering publication by Hanna et al. [44]. approaches are usually necessary. Involvement They reported a series of 46 patients with of the sinus walls, infratemporal fossa, masti- advanced squamous cell carcinoma of the catory and/or parapharyngeal spaces extension paranasal sinuses that underwent induction or to the orbit justify the use of open approa- ChT followed by surgery and RT or chemora- ches, at least in combination with an initial diotherapy (ChRT) or definitive RT/ChRT. The endonasal delineation of the nasal neoplastic overall response rate to induction ChT was 67%, component. Achieving free margins is essential and the 2-year overall survival (OS) was 67%. and confirmation of negative histologic mar- Conservative surgery with orbital preservation gins should be confirmed by frozen section was possible in 87% of the patients. These regardless of surgical approach. Endoscopic results are superior to some historical series that surgery is still useful in specific cases with lim- analysed the combination of surgery and post- ited extension [49–52]. operative RT [6, 45, 46]. Adenocarcinomas usually originate in the roof Finally, although an endoscopic endonasal of the ethmoid. The mainstay of treatment is approach may be a feasible surgical option for surgery with negative margins. In case of poor the management of selected recurrent SNMT prognostic features, adjuvant RT may be indi- [47], external approaches are the preferred sal- cated [53], although the role of RT is much vage treatment for local recurrences after pre- debated. Nicolai et al. [54] could not show vious surgery, because local failures often occur benefit for RT after endoscopic surgery whereas in sites no longer manageable with minimally Camp et al. [55] did, both looking at reasonable invasive techniques (e.g. orbital content, max- size cohorts with good long-term follow-up. illary sinus floor, critical areas of the skull base). Craniofacial resection (uni- or bilateral) is the The need to reconstruct with a microvascu- standard surgery and can be undertaken by an larised free flap is also an indication for an endoscopic, open, or combined approach external approach, especially in case of previous [19, 56, 57]. Endoscopic surgical excision has ChRT [15]. been shown to have comparable oncological Based on all these considerations, a proposed results to external approaches with less mor- surgical treatment algorithm according to bidity [19]. However, external or combined anatomical location is shown in Fig. 1. approaches are still indicated on certain occa- sions. Extensive invasion of the orbit, dura mater, brain, lacrimal system of the nasal bones SURGICAL STRATEGY ACCORDING or soft tissues of the face are still indications for TO HISTOLOGY the open approach to be discussed on an indi- vidual basis. One of the determining criteria in the election Adenoid cystic carcinomas originate in minor of surgical strategy is the histology of the salivary glands and are common in the maxil- tumour, given the differential biological beha- lary sinus. Their main characteristic is a ten- viour of the diverse SNMT and their different dency for perineural invasion, with frequent sites of origin. Although not always possible, extension to the skull base. They are tumours histological confirmation of the lesion should with a poor prognosis despite their slow pro- be carried out prior to selecting a particular gression [58]. Both open and endoscopic routes therapeutic approach. It is important to prop- appear to be useful for the treatment of these erly diagnose newer variants of SNMT that have tumours but endoscopic approach with adju- aggressive biological behaviour with poor vant RT offers similar survival with less mor- prognosis [48]. bidity to that reported by other studies Squamous cell carcinomas are aggressive (including open surgery) [59–62]. tumours usually originating from the nasal 2386 Adv Ther (2022) 39:2379–2397 Olfactory neuroblastoma or esthesioneuroblas- procedures, which are associated with less toma develops in the olfactory cleft. Treatment morbidity, can be proposed if they allow com- is multimodal, including surgery in combina- plete macroscopic removal [79]. Regardless of tion with postoperative RT [63–67]. For high- surgical approach, these patients remain at high grade olfactory neuroblastoma (Hyams 3–4), risk for local and distant failure. induction ChT could be considered, followed by Sinonasal undifferentiated (SNUC) and neu- ChRT in case of good response [68]. Uni- or roendocrine carcinomas (SNEC) are aggressive bilateral craniofacial resection is the technique malignancies usually diagnosed at a locally of choice. Endoscopic surgery can achieve sim- advanced stage [82–85]. Surgery alone for ilar or even better oncological results than open resectable well-differentiated SNEC, surgery surgery [20, 66, 69]. Endoscopic approaches followed by RT for moderately differentiated were also associated with fewer complications tumours, and induction ChT followed by local than open approaches [21]. Invasion of the therapy (surgery or consolidative RT/ChT) for maxillary infrastructure and facial structures, poorly differentiated SNEC may be a reasonable the orbital floor lateral to the infraorbital nerve, treatment strategy. SNUC are likely best man- the intraconal orbital compartment, invasion of aged by induction ChT with subsequent the dura mater laterally to the medial plane of definitive therapy (surgery versus ChRT) the orbit or extensive brain invasion would according to initial response. Within the mul- condition a purely endoscopic approach [70]. timodal management necessary for the treat- An external approach can then be combined to ment of these tumours, endoscopic surgery, complete such extended resections. Minimal when deemed feasible, gives good oncological invasion of the frontal lobe does not appear to results and with less morbidity [82–86]. be a poor prognostic factor for these patients, Soft tissue sarcomas are rare tumours fre- and endoscopic resection combined with RT quently arising in the maxillary sinus. Tumour could be an effective therapeutic method [71]. resection with wide margins, recommended in Mucosal melanomas are one of the SNMTs other anatomical locations, is frequently not with the worst prognosis [72]. They originate achievable because of the anatomical proximity most frequently from the lateral nasal wall, of the brain and the orbit but it should always followed by the septum and maxillary sinus be performed when feasible [87]. The recom- [72]. Melanomas should be surgically removed mended wide resection is hardly ever achieved whenever possible. RT, or less frequently adju- with an endoscopic approach [88]. vant ChT or immunotherapy, may be indicated [73–76]. Endoscopic surgery has been associated with similar oncologic outcomes compared to WHICH OPEN APPROACHES ARE more invasive surgery [77–79]. Some studies CURRENTLY AVAILABLE? have found better survival and improved local control in patients treated endoscopically There are multiple open approaches, and their compared to those managed by open craniofa- description is beyond the scope of this review. cial surgery [80, 81], but these results remain Nowadays, as a result of the implementation of controversial and may reflect a selection bias or endoscopic surgery and the technical refine- may be related to the lower morbidity associ- ments developed, open approaches can be ated with this surgery. Resection with clear reduced to two main surgical routes, with some margins does not provide a survival benefit in technical variations. The modifications intro- these tumours [75] and, therefore, potentially duced in these approaches are aimed at reduc- aggressive procedures such as orbital exentera- ing morbidity and improving cosmesis. tion, amputation of the nasal pyramid, or maxillectomy should be limited [73]. These indications must therefore be discussed indi- vidually, according to the presentation of the tumour and the patient’s wishes. Endoscopic Adv Ther (2022) 39:2379–2397 2387 Transfacial Approaches Craniofacial Resection These surgical procedures expose the bony When SNMT extend to the skull base, with or structure of the midface. They can be used to without intracranial invasion, a combined resect tumours in all sinonasal regions even transfacial and coronal approach allows access with a limited extension to the skull base. There to the sinonasal part of the tumour and its are two main types of transfacial surgery: the intracranial component, as well as orbital lateral rhinotomy approach with its variations, resection if necessary [92–94]. Craniofacial and the sublabial approach. They can be com- resection is contraindicated when there is bined with a coronal incision for a more bilateral involvement of the orbital apex, inva- extended craniofacial approach or an infratem- sion of the optic chiasm, the sella turcica and poral fossa approach. Their indications have cavernous sinus or extensive disease in the floor significantly decreased in favour of less invasive of the anterior fossa or brain, as in these cases endoscopic resections. the prognosis is extremely poor and non-surgi- Lateral rhinotomy [89] primarily provides cal (palliative) treatment remains the rule rather access to the maxilla, ethmoid, sphenoid, and than the exception [95]. may also provide access to the frontal sinus and Through a lateral rhinotomy approach, the anterior skull base when combined with other portion of the tumour involving the nose and incisions. By performing various osteotomies, it paranasal sinuses is resected and the cribriform is possible to expose the ventral skull base, the plate is exposed from below. Subsequently, a infratemporal fossa and to control the internal frontal craniotomy is performed through a carotid artery [90]. Lip-splitting incision, which coronal incision, the frontal lobe is retracted, does not seem to be of great advantage, should and the floor of the anterior cranial fossa is be avoided whenever possible to avoid cosmetic exposed up to the dorsum of the sella turcica. sequelae. Transfrontal craniotomy may include resection In the sublabial approach, an incision is made of the anterior and posterior frontal walls, or a at the level of the mucosa of the upper vesti- frontal osteoplastic flap may be performed, bule, directly to the bone, elevating the facial which decreases the risk of osteomyelitis [90]. soft tissues and exposing the midfacial bony To avoid frontal cerebral lobe retraction, a sub- skeleton. Access is limited, especially to the cranial approach can be used. In this type of upper facial territory, but the main advantage is approach, the inferior transfrontal osteotomy is the avoidance of skin incisions. The sublabial performed by including the nasal bones in approaches are essentially the Rouge-Denker continuity with the superior orbital rims. This and degloving approaches. In the Rouge-Denker allows access to the base of the skull in the same approach, the lateral border of the piriform plane. Although scarring on the face due to the aperture and the lateral nasal wall are resected transfacial incision is not prominent, it can be to gain extended access to the maxillary sinus avoided in cases of tumours with moderate and ethmoid. The midfacial degloving approach intranasal progression by using a midfacial [91] allows the anterior aspect of one or both degloving approach instead of lateral rhino- maxillary sinuses to be exposed from one max- tomy or by resection using the intracranial illary tuberosity to the other. Through various route, through a subfrontal transcranial osteotomies, the ethmoid, sphenoid, and max- approach, with or without the aid of an endo- illary sinuses can be approached. A disadvan- scope [10]. tage of this approach is the relatively poor After the craniotomy is performed, the access to the skull base behind the tumour. frontal lobes are retracted, allowing exposure of the frontal sinus, the floor of the anterior cra- nial fossa, the roof of both orbits and the sphenoid planum. This manoeuvre allows exposure of the intracranial tumour component and, depending on the degree of dural invasion, 2388 Adv Ther (2022) 39:2379–2397 dissection is performed extradurally or appears evident that endoscopic approach is intradurally, removing the dura mater and, associated with a significantly shorter hospital possibly, the invaded brain tissue. The dura stay than open surgery, with average lengths of must be reconstructed to achieve an airtight seal stay of 3–6 days vs. 6–12 days for open surgery and avoid cerebrospinal fluid (CSF) leak. [20, 21, 48, 99–101]. This reduction in hospital All these different approaches can be exten- stay should be associated with a reduction in ded to other regions depending on the specific costs, but this has yet to be shown with statis- tumour extensions. They can be enlarged to tical significance, particularly when considering involve the orbit and even to allow its exen- the high costs of state-of-the-art technologies teration [30], or to complete an anterolateral routinely needed for modern endoscopic approach to the skull base [96]. approaches [13, 102]. The endoscopic approach was also associated with a better postoperative quality of life compared to patients operated on COMPLICATIONS OF OPEN with traditional open techniques [103–106]. APPROACHES In a pivotal study, among 1193 patients who underwent a craniofacial resection, Ganly et al. Open craniofacial surgery is definitively a major [45] reported a postoperative mortality rate of head and neck procedure and thus carries 5% and a morbidity rate of 36.3%. The main potential for considerable postoperative mor- complications were postoperative CSF leak, bidity and mortality. This type of surgery is in pneumocephalus, intracranial infectious and fact associated with significant rates of compli- haemorrhagic complications, and frontal lobe cations [45, 97], ranging between 12% and 47%, syndrome due to frontal lobe retraction. Further with an average mortality of 4% as demon- ophthalmological complications were observed. strated by the systematic review of König et al. Osteoradionecrosis of the frontal flap has also [98]. The morbidity associated with open been described after RT. Main factors associated resections and the extent of cranial base defects with the development of complications were may also delay adjuvant treatments. These the presence of medical comorbidities, previous aspects have been receiving growing attention RT, dural and/or brain tumour invasion. It is in the last decades and reduced morbidity has important to note that the complication rate in been advocated as one of the main advantages open surgery may also increase if free flap of endoscopic resection over external proce- reconstruction is required [15]. These data dures [18]. Meccariello et al. [19] observed that highlight that expanding the surgical field can endoscopic and endoscopic-assisted surgery had increase the chances to obtain radical removal low rates of major complications (6.6% and of tumours not amenable to endoscopic endo- 25.9%, respectively) compared to open approa- nasal resection, but this comes at a cost of ches alone (36.4%; p \ 0.01). Abdelmeguid increased risk of mortality and morbidity, et al. [13] reported a complication rate of 29% which should always be discussed preopera- for endoscopic resections, mainly minor (ser- tively with the patient, and balanced consider- oma, sinusitis, etc.) and Lund et al. [99] reported ing his/her performance status, comorbidities, resolvable complications in 11%. However, the and expected residual quality of life. different studies directly comparing the com- Some authors highlight the specific inci- plication rates between open and endoscopic dence of CSF leak in the endoscopic vs. open approaches did not find any significant differ- approach [20, 21]. While this represented an ence [20, 100]. Lu et al. [24] observed that, issue a few years ago, there have been important although a reduction in complications has been technical advances in the reconstruction of associated with endoscopic resections, no sta- skull base defects and, as a consequence, post- tistical difference was observed when the com- operative CSF leak rates have significantly parative studies were pooled overall (with dropped [107]. The use of multilayer techniques incidences of 18% and 24% in endoscopic and with pedicled mucosal flaps and ‘‘minimally open approaches, respectively). However, it invasive’’ pericranial flaps [108] to close the Adv Ther (2022) 39:2379–2397 2389 endoscopic dural defects has greatly con- these are selected patients suitable for endo- tributed to the observed decreases of the CSF scopic resection with limited extent or early- leak rate, which now come close to those stage disease. observed after open approaches [109, 110]. This Some authors have conducted studies com- underlines that the ability to perform an ade- paring open and endoscopic approaches quate reconstruction of the skull base is critical [19, 22, 24, 48, 101, 113–115]. Higgins et al. [22] in the indication for endoscopic resection. conducted a systematic review with a pooled- data analysis to compare outcomes of endo- scopic vs. craniofacial resection of SNMT. The COMPARING OUTCOMES OF OPEN 5-year OS was 87.4% (SE ± 5.3) in the endo- AND ENDOSCOPIC APPROACHES scopic group vs. 76.8% (SE ± 8.3) for open REVISITED approaches (p = 0.351); DSS was 94.7% (SE ± 3.7) vs. 87.7% (SE ± 6.7; p = 0.258); and The current data are insufficient to draw robust locoregional control rate was 89.5% (SE ± 5.0) conclusions regarding any potential differences vs. 77.2% (SE ± 10.4; p = 0.251). One of the in OS between various resection approaches for weaknesses of this study is that the number of SNMT. However, the available evidence suggests papers involving endoscopic resection of high- at least equivalent survival outcomes between grade tumours remains only moderate. There- open and endoscopic approaches for patients fore, the authors concluded that although with similar early-stage tumours. Five-year OS endoscopic resection is a reasonable alternative and disease-specific survival (DSS) rates from the to open approaches in the management of largest series reporting on craniofacial resection, early-stage SNMT, open surgery remains an which analysed a total of 1307 patients in 2003, alternative to achieve complete resection in were 53.6% and 59.9% for open and endoscopic high-grade tumours. Lu et al. [24] conducted a approaches, respectively [111]. A recent review meta-analysis based on comparative studies of patients treated by open craniofacial or only to critically evaluate endoscopic vs. open transfacial surgery shows similar outcomes, approaches, and to identify and compare clini- reporting 5-year OS ranging from 46% to 72% cal outcomes between both approaches in the (median 54%) and 5-year DSS rates from 46% to treatment of SNMT. The results showed that, 78% (median 60%). These same authors carried with respect to various surgical outcomes and out a meta-analysis in which they analysed recurrence rate, the current literature does not 2603 patients and the results confirmed a trend indicate either endoscopic or open approaches with the 5-year OS rate ranging from 46% to as statistically superior. Therefore, until a more 72% (median 54%) and the 5-year DSS rates sound validation of these associations can be ranged from 46% to 78% (median 60%) [98]. All proven, according to these authors, expecta- these data corroborate the appropriateness of tions that endoscopic resection for SNMT con- the modern open approaches, but also empha- fers superior surgical outcomes compared to size that there is still space for improvement of open approaches should be tempered. Mecca- outcomes, considering that only small riello et al. [19] performed a pooled analysis of advancements in survival rates have been 1826 patients comparing endoscopic vs. open observed in the last decades when considering approach for the management of sinonasal advanced-stage SNMT. These results are in adenocarcinoma. They observed that the inci- accordance with those observed in meta-analy- dence of local failure was lower in the endo- ses of endoscopic approaches. Rawal et al. [112], scopic surgery group as compared with open for example, demonstrated that optimal sur- approach patients (17.8% vs. 38.5%; p \ 0.01, vival outcomes could also be achieved with an respectively). However, worse survival was endoscopic approach. A 5-year OS rate of 72.3% observed in advanced stage tumours with an was observed, which is comparable and even open approach, which likely represents a selec- greater than that from open craniofacial resec- tion bias in favour of endoscopic approaches. tions. However, one must bear in mind that To control the possible influence of 2390 Adv Ther (2022) 39:2379–2397 confounding factors, Farquhar et al. [101] uti- factors, histological grade also plays an impor- lized a propensity score matching approach to tant role. Significant OS difference is found account for disease stage, locoregional spread, between low- and high-grade cancers [112], and and presenting comorbidities, and found that in these high-grade tumours more extensive OS outcomes were comparable between both approaches could be necessary, taking into approaches. This highlighted the high likeli- account the potential morbidity caused by the hood that variations in the reported OS were surgery. However, some studies [49, 116] have confounded by those parameters Farquhar et al. observed no differences between the outcomes accounted for, confirming the decision not to of open or endoscopic resections in patients pool the OS data in the case studies. Povolotskiy with a high-grade tumour. et al.’s study [115], which included 1595 It is universally accepted that a free-margins patients with non-squamous sinonasal carcino- resection should be achievable in patients con- mas, found an OS of 65.2% in patients treated sidered suitable for surgery to reduce the risk of by endoscopic surgery and 65.4% in those recurrence rates and maximize oncologic out- treated via an external route (p = 0.59). Finally, comes. Achieving negative surgical margins Kılıç et al. [49] using the National Cancer seems to be the most important prognostic Database analysed all cases of sinonasal squa- factor regarding survival, regardless of surgical mous cell carcinoma included, dividing them techniques [98]. However, resection of SNMT according to the surgical approach adopted: with wide margins is not always possible open or endoscopic. A total of 1483 patients because of the adjacent cranial nerves, orbit, were identified, of which 23.8% received an internal carotid artery, or brain. Thus, attempts endoscopic and 76.2% an open surgical proce- to remove a tumour with wider surgical margins dure. The authors found that open surgery was could cause unacceptable morbidity and would more common in academic centres (62.8% vs. be technically difficult, if not impossible, either 54.2%; p = 0.004), less common for tumours of by open or endoscopic techniques. Moreover, the ethmoid and sphenoid sinus (p \ 0.0001), no evidence suggests that a mutilating less common for stage IVB tumours, and asso- approach would substantially increase survival. ciated with longer hospital stay (mean 4.67 days Radical resection correlates with improved vs. 2.50 days; p \ 0.0001). Five-year OS was not prognosis both for tumours resected through an significantly different between the two approa- endoscopic or open approach [17, 98, 111]. ches (p = 0.953; open: 5-year OS, 56.5%; 95% Some authors have compared the rate of posi- confidence interval, 51.3–61.6%; endoscopic: tive margins between tumours operated by 5-year OS, 46.0%; 95% confidence interval, open and those operated by endoscopic surgery, 33.2–58.8%). Endoscopic surgery appears to be and most have found no difference between an effective alternative to open surgery, even these techniques [20, 101, 117]. Endoscopic after taking into account confounding factors approaches allow complete resection of that may favour its use. However, the afore- tumours in most cases and avoid an excessive mentioned meta-analyses cannot exclude resection of healthy tissue. However, some important selection biases, such as endoscopic authors criticise piecemeal tumour removal and surgery being more frequently chosen for argue that a significantly higher proportion of smaller tumours, tumours with different his- gross total resection with negative microscopic tologies being compared with each other, etc. In margins is obtained when resection is per- addition, as this is highly specialised surgery, formed in a truly en bloc fashion, as opposed to pooling and comparing results from surgical piecemeal technique [98]. Although piecemeal teams with different expertise may not be resection adheres to oncological principles [14], appropriate. it requires close collaboration with pathologists Although almost all survival analysis con- to ensure accurate analysis of the histological firmed the role of pT classification, surgical margins [118]. An en bloc unfragmented resec- margins status, dural invasion and orbital apex tion through an open approach in high-grade infiltration as the most important prognostic tumours and in complex locations has the Adv Ther (2022) 39:2379–2397 2391 potential to achieve a higher rate of free mar- clinical centres for skull base pathology; such gins [98], so, in certain cases, open approaches centres should include a multidisciplinary team continue to play an important role in skull base including the key professional figures of surgery. However, it should be acknowledged otorhinolaryngologists, maxillofacial surgeons, that removing an en bloc specimen may not neurosurgeons, plastic and reconstructive sur- always be possible. In conclusion, achieving geons, neuroradiologists, radiation and medical negative surgical margins is significantly more oncologists as well as specialised histopatholo- important than the way a tumour is removed gists, radiologists, cancer nurses, and (en bloc vs. piecemeal resection), and it should prosthodontists. Decision-making is often quite be the surgical goal regardless of the technique complex and based on multiple factors such as chosen, whenever possible. tumour location, extent and stage of disease, Dural and intracranial extension have been histology, orbit and skull base involvement, as recognized as the most adverse prognostic fac- well as institutional practice and multidisci- tors in malignant SNMT [119, 120]. Although plinary board preference. dural and intracranial resections are possible Progress in multimodal treatment strategies through an endoscopic approach, open routes as well as refinements in endoscopic techniques allow, in certain cases, safer removal and better have progressively reduced the role of cranio- control of possible intraoperative complica- facial and transfacial resections during the last tions. Orbital invasion results in a high-risk decades; the latter are still associated with sig- negative prognostic factor for almost all the nificant rates of perioperative morbidity and survival endpoints, with decreased 5-year OS significant impact on postoperative quality of from 65–55% to 20–30% [107]. In particular, life. Moreover, there appears to be no difference orbital apex infiltration significantly worsens in risk of unfavourable outcomes with endo- outcomes because a free-margin resection is scopic compared to open approaches in appro- virtually impossible, regardless of the type of priately selected patients. surgery performed [14]. Nevertheless, there is still a role for open Local recurrence often occurs within 2 years surgery which remains an important part of the of follow-up and is the main contributor to surgical arsenal of the head and neck surgeon to SNMT mortality, followed by distant failure increase the chances of obtaining radical resec- [111, 121]. Patel et al. [111] reported 3- and tion in advanced stage diseases not amenable to 5-year recurrence-free survival (RFS) rates of exclusive endoscopic approach. Maintaining 50.4% and 45.8%, with a median time to training and expertise in these techniques may recurrence of 7 months, using open surgery. prove an issue in the future. Recurrence was not significantly different Open approaches could be also used to treat between endoscopic and open approaches with selected cases of local recurrences involving incidences of 42% (n = 399) and 50% (n = 501), areas not amenable to salvage endoscopic sur- respectively, according to Lu et al. [22]. Dural gical resection, which are nowadays increas- infiltration and pT classification are factors ingly observed in view of the growing associated with increased risk of recurrence and population of survivors following multidisci- systemic dissemination of disease [119]. This plinary treatment strategies. was also the case with histological classification, In conclusion, selected surgical approaches as poorly differentiated tumours or melanomas for SNMT are patient- and surgeon-dependent, are more prone to develop distant metastasis which argues that both approaches continue to [79, 122, 123]. have a place in the management of SNMT. CONCLUSIONS To provide the best possible care, patients with SNMT should be treated at specialised referral 2392 Adv Ther (2022) 39:2379–2397 ACKNOWLEDGEMENTS a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are Funding. No funding or sponsorship was included in the article’s Creative Commons received for this study or publication of this licence, unless indicated otherwise in a credit article. line to the material. If material is not included in the article’s Creative Commons licence and Authorship. All named authors meet the your intended use is not permitted by statutory International Committee of Medical Journal regulation or exceeds the permitted use, you Editors (ICMJE) criteria for authorship for this will need to obtain permission directly from the manuscript, take responsibility for the integrity copyright holder. To view a copy of this licence, of the work as a whole, and have given final visit http://creativecommons.org/licenses/by- approval for the version to be published. nc/4.0/. Author Contributions. All authors con- tributed to the study conception and design. Material preparation, data collection and anal- REFERENCES ysis were performed by Fernando López. The first draft of the manuscript was written by 1. JL Llorente F López C Suárez MA Hermsen 2014 Fernando López, and all authors commented on Sinonasal carcinoma: clinical, pathological, genetic and therapeutic advances Nat Rev Clin Oncol 11 previous versions of the manuscript. All authors 460 472 read and approved the final manuscript. 2. S Sjöstedt C Buchwald von TK Agander K Aanaes Disclosures. Fernando López, Jatin P. Shah, 2021 Impact of human papillomavirus in sinonasal Jonathan J Beitler, Carl H. Snyderman, Valerie cancer—a systematic review Acta Oncol 60 1175 1191 Lund, Cesare Piazza, Antti A. 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