Peer-Review Reports
From Craniofacial Resection to Endonasal Endoscopic Removal of Malignant Tumors of the Anterior Skull Base Boris Krischek1,2, Felipe G. Carvalho2, Bruno Loyola Godoy2, Rasmus Kiehl3, Gelareh Zadeh2, Fred Gentili2
Key words Anterior skull base surgery - Craniofacial resection - Expanded endoscopic endonasal approach -
Abbreviations and Acronyms CER: Cranio-endoscopic resection CFR: Craniofacial resection CSF: Cerebrospinal fluid PER: Pure endoscopic resection From the 1Department of Neurosurgery, University of Cologne, Germany; 2Department of Neurosurgery, Toronto Western Hospital, Toronto, Canada; and 3Department of Neuropathology, University Health Network, Toronto, Canada To whom correspondence should be addressed: Fred Gentili, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014) 82, 6S:S59-S65. http://dx.doi.org/10.1016/j.wneu.2014.07.026 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
- OBJECTIVE:
To review the current literature and provide our institutional approach and opinion on the indications and limitations of traditional open craniofacial resection (CFR) and a minimally invasive pure endonasal endoscopic approach for anterior skull base tumors concentrating primarily on malignant lesions.
- METHODS:
Based on 3 decades of experience with both open and more recently endoscopic techniques, we examined our current practice in treating tumors and other lesions involving the skull base and our current indications and limitations in the use of these techniques. We conducted a retrospective chart analysis to see which operative techniques were used for malignant tumors of the anterior skull base in the last 10 years at our institution.
- RESULTS:
There were 30 cases identified. Traditional CFR was performed in 16, a pure endoscopic resection was performed in 9, and an endoscopic procedure combined with a frontal craniotomy was performed in 5. Gross total resection was achieved in 83.3% in the CFR group and 75% in the pure endoscopic resection group. Near-total resection was 10% in the CFR group and 33.3% in pure endoscopic resection group. Of the 5 patients who underwent a combined approach, 80% had gross total resection, and 20% had near-total resection.
- CONCLUSIONS:
INTRODUCTION There have been significant developments in the area of skull base surgery in the last 3 decades. From the initial skepticism of the specialty to its widespread acceptance as well as the subsequent acknowledgment of the limitations, the techniques of open skull base surgery have had overall a very positive impact on management of many difficult tumors and other complex lesions involving the skull base. Many factors contributed to success in this field, including the application of microsurgical techniques, development of innovative surgical approaches based on improved knowledge of the relevant anatomy, improved imaging, improved anesthesia, and expert preoperative and postoperative care. An important factor was the novel development of multidiscilinary surgical teams. The original approach first described by Ketcham et al. in 1963 (10) combined a cranial (bifrontal craniotomy) and facial (lateral rhinotomy, maxillectomy, or
Both traditional CFR and the endonasal endoscopic approach offer advantages and disadvantages. Both approaches can achieve good results with appropriate patient selection. Numerous important factors, including location and the extent of tumor, should be taken into consideration when considering either approach. The most important determinant of outcome is the ability to achieve gross total resection with microscopic negative margins rather than the type of approach used. In the future, skull base surgeons will need to be familiar with and capable of offering both techniques to the patient.
sinusotomies) exposure performed by a team of neurosurgeons and otolaryngologists. This craniofacial resection (CFR) provided improved exposure of lesions in the paranasal sinuses and lesions involving both the intracranial and the extracranial compartments of the skull base. The subsequent addition of plastic and reconstructive surgeons and radiation and medical oncologists to the team provided a comprehensive approach to the management of lesions previously thought to be inoperable or associated with significant surgical morbidity. Craniofacial approaches helped facilitate more complete resection with significant improvement in
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overall and disease-specific survival as well as reduced recurrence rates in patients with anterior skull base cancer (2, 5). Patients with benign pathology could achieve long-term survival and, in many cases, cure. Likewise, even patients with aggressive pathologies such as squamous cell cancers of the paranasal sinuses previously associated with very poor prognosis and low survival (1) could achieve long-term survival (3, 6, 17). There are numerous advantages of the open approaches in skull base surgery. They have become well-known procedures incorporated into most residency training programs with no need for a learning curve.
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Likewise, there are no issues with regard to lack of binocular vision or the ability to use microsurgical technique and the required instrument manipulation. Wellrecognized and effective reconstruction techniques are available with low rates of cerebrospinal fluid (CSF) leakage. Lastly, long-term outcome data including overall and progression-free survival are known. Despite the development of newer, less invasive endoscopic techniques (discussed subsequently), traditional open techniques continue to play an important role in skull base surgery and remain primary strategies in the treatment of many anterior and anterolateral skull base malignancies. However, not all of the initial hopes and expectations of open skull base surgery were realized, and many sober lessons were learned. The extremely varied pathology of lesions involving the skull base made it difficult to accrue large series of patients with uniform pathologies. Although there were efforts to carry out multiinstitutional trials, few came to fruition, and most reports in the literature were individual personal series with a limited number of patients and short follow-up times, and results were difficult to interpret. It also became evident that ever larger incisions and exposures and more radical surgery, often associated with increased morbidity, were not always associated with improved outcomes and that tumor biology, not surgical technique, in many cases was the critical factor in survival. In addition, despite continued refinements in surgical technique, open approaches still required some degree of brain retraction and neurovascular manipulation and continued to carry significant perioperative risks and morbidity with prolonged recovery time. Complication rates of most published series of CFR, including more recent reports, are 40% with postoperative mortality approximating 5% (5, 9, 11, 14). Although outcomes in skull base surgery previously had focused primarily on survival and complications, a heightened awareness developed of functional outcome and quality of life and costs/benefit issues. Even ethical concerns were expressed by some of carrying out major resections with significant morbidity without hard scientific evidence of efficacy. In an attempt to address some of the shortcomings of open skull base surgery, surgeons sought less invasive
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FROM CRANIOFACIAL RESECTION TO ENDONASAL ENDOSCOPIC REMOVAL
techniques to approach the anterior skull base culminating in increasingly accepted and currently widely used endoscopic techniques. The endonasal endoscopic skull base approach, developed from concepts applied from the field of rhinology and functional endoscopic sinus surgery introduced in the 1980s (16), revolutionized the treatment of inflammatory diseases and lesions limited to the sinonasal tract. For tumors, the endoscopic approach was initially limited to benign pathologies and other nontumorous lesions involving the sinonasal tract that did not extend up to the anterior skull base. The first reports on pure endoscopic procedures alone or in combination with frontal craniotomy (the cranionasal approach) emerged in the late 1990s (18, 19). The approach subsequently was used for selected cases of malignant tumors. Following the publication of several series analyzing small and intermediate-size cohorts of patients, there was considerable criticism from physicians who believed that endoscopic surgery by its very nature did not adhere to the principles of oncologic surgery—that is, the tumor was removed in a piecemeal fashion, and an en bloc resection was not achieved (13). Likewise, numerous contraindications for the endoscopic approach were cited, including extension to the frontal sinus, involvement of the lacrimal pathway or of the bony walls of the maxillary sinus (with the exception of the medial wall), erosion of the nasal fossa floor, extension into the pterygopalatine or infratemporal fossa, involvement of the orbit, and erosion of the skull base (12). Criticism was countered by the acknowledgment that even in open procedures true en bloc resection is often difficult to achieve and that the critical and major determinant of a patient’s overall and progression-free survival was not the technique of removal but the ability to achieve a gross total resection with microscopic negative margins (4). More recent data have shown that in well-selected patients endoscopic resection of paranasal sinus malignancies, including tumors that extend to the anterior skull base, can be achieved with acceptable morbidity and outcomes (9). The determinants of success of endonasal endoscopic surgery of the skull base have been similar to the factors enumerated earlier for open skull base
surgery—advances in endoscopic technology, improved understanding of endonasal skull base anatomy, and a multidisciplinary team approach. The collaboration of otolaryngologists and neurosurgeons using a 2-nostril, bimanual technique significantly advanced endoscopic techniques, and various surgical modules subsequently were described that encompassed the entire ventral skull base (8). Endoscopic techniques subsequently were expanded to include the removal of intradural pathology (3). These expanded endoscopic approaches, although a more recent addition, have become widely adopted and have had a dramatic impact not only on pituitary surgery but also on the entire field of skull base surgery. The advantages of this less invasive approach include a more direct anatomic route, no need for craniotomy or facial incisions, less trauma to the brain and neurovascular structures, early devascularization of the tumor blood supply, improved visualization of the relevant anatomy, and better cosmetic results with shorter recovery times. However, there are important prerequisites for success in using these approaches, including a detailed knowledge of anatomy, an interdisciplinary team of experienced endoscopists, use of a 2-nostril bimanual approach that allows for the use of microsurgical technique as employed in open procedures, advanced multiangled endoscopes, appropriate instrumentation, and high-definition cameras and screens. It is also important that the surgical team have adequate knowledge of the limitations of the endoscopic techniques as well as experience with the traditional open approaches so that the most appropriate surgical approach can be tailored to each individual patient. In addition, adequate training is required because there is a significant learning curve. In the last 3 decades, the authors have had experience with open skull base approaches (>2000 cases) and, more recently, increasing experience with endoscopic approaches (>850 cases). Most endoscopic procedures have been performed for pituitary surgery with expanded approaches to the skull base representing 22% of all endoscopic procedures. The types of lesions and pathologies are listed in Table 1. Although there is a role for the use of endoscopic techniques for more laterally placed lesions in the paranasal
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Table 1. Histology of Cases in Which an Expanded Endonasal Endoscopic Approach Was Used Diagnosis
Number of Cases
Craniopharyngioma
32
Chordoma
22
Meningioma
25
Esthesioneuroblastoma
10
Pituitary adenoma
11
Encephalocele
10
Other
54
Total
164
sinuses using transpterygoid and transcavernous approaches, we have used the endoscopic technique for lesions and pathologies that primarily involve the midline skull base. Based on this experience, in this article, we examine our current practice in dealing with tumors and other lesions involving the skull base and provide our current indications and limitations in the use of these techniques. Because of the breadth of the subject, we have limited our review to malignant lesions.
MATERIALS AND METHODS Retrospective chart analysis was conducted to identify patients undergoing resection of malignant anterior skull base tumors between January 2002 and January 2013 performed by the senior author (FG) at the Toronto Western Hospital. There were 30 patients identified. Demographic data, symptoms, follow-up, and tumor characteristics were collected from the records. Records were evaluated for patient age, sex, diagnosis, anatomic site, symptoms, surgical approach, extent of surgical resection, surgical complications, and recurrence. All patients included in this series underwent a traditional CFR, a pure endoscopic resection (PER), or in selected cases an endoscopic procedure combined with frontal craniotomy (cranioendoscopic resection [CER]). Operative Procedure There were 16 patients in the CFR group, and all underwent a standard bifrontal craniotomy. Tumor extirpation was
achieved via PER in 9 patients. Combined CER was performed in 5 patients for reasons discussed subsequently. RESULTS Demographic Data Tumor resection was performed in 30 patients (19 men and 11 women) with an overall mean age of 58.2 years (range, 20e78 years). The mean age was 49.8 years (range, 24e77 years) in the PER group and 56.4 years (range, 37e78 years) in the CFR group. The percentage of female patients in the PER group was 33% (3 of 9) compared with 37.5% (7 of 21) in the CFR and CER groups. The median followup for the PER group was 4.2 years (range, 0.3e7.3 years) and for the CFR and CER groups was 4.7 years (range, 0.2e10.7 years). Table 2 lists the presenting symptoms of the group as a whole. The primary presenting complaint in this group as a whole was nasal airway obstruction. Tumor Characteristics A wide variety of pathologies were treated with the most common diagnosis being esthesioneuroblastoma (53.3%), followed by squamous cell carcinoma (20%), adenocarcinoma (6.67%), undifferentiated sinonasal carcinoma (6.67%), and various other, less frequently diagnosed lesions (Table 3). Extent of Resection and Recurrence Gross total resection was achieved in 83.3% in the CFR group and 75% in the PER group. Near-total resection was 10% in the CFR group and 33.3% in the PER group. Of the 5 patients who underwent a
Table 2. Symptoms of 30 Treated Patients Symptom Sinusitis/nasal obstruction
Number of Patients (%) 17 (57)
Visual complaints
6 (20)
Epistaxis
5 (17)
Proptosis
5 (17)
Headache/local pain
4 (13)
Asymptomatic
1 (3)
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combined approach, 80% had gross total resection, and 20% had near-total resection. Recurrences were observed in 2 of 7 (29%) of the patients in the PER group and 5 of 13 (38%) of the patients in the CFR group. Of the 5 patients treated with the combined approach, none presented with recurrence. There were 5 patients lost to follow-up. Complications In the patients who underwent PER, there were 2 CSF leaks and 1 case of sinusitis. In the patients who underwent CFR, there were 2 wound infections, 1 flap infection, 1 pneumocephalus, 1 abscess, and 1 osteonecrotic bone flap. In the 5 patients who underwent the combined procedure (CER), 1 patient experienced a deep vein thrombosis. Illustrative Cases Case 1 (PER). A 59-year-old man who was a former smoker had been complaining of nasal obstruction for the past 6 months. Imaging examinations revealed a mass in the left nasal cavity with involvement of septal mucosa and extension to the nasopharynx and the left anterior skull base (Figure 1). The histopathology result from a biopsy procedure was sinonasal undifferentiated carcinoma). The patient underwent chemotherapy and radiotherapy before surgical resection. There was a satisfactory response to radiation, with a significant decrease in the tumor volume. The tumor resection was performed via an expanded endoscopic endonasal transsphenoidal approach. Because the tumor appeared to involve the septal mucosa, including the right side, no pedicled nasoseptal flap was planned for reconstruction of the anterior skull base. Fascia lata was harvested from the right thigh for the repair of the skull base defect. The main steps of the procedure involved bilateral middle turbinectomies, posterior septectomy, ethmoidectomy, wide bilateral sphenoidotomy, and bilateral maxillary antrostomies. After the resection of the tumor in the nasal cavity, the lamina papyracea was removed on both sides, carefully dissecting and coagulating the anterior and posterior ethmoidal arteries of both sides. The final stage of the procedure was osteotomy of the anterior fossa around the cribriform plate, resecting it together with the crista galli. The
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Table 3. Tumor Histology of Operated Cases PER
CFR
Combined
Total
Esthesioneuroblastoma
8
6
2
16
Squamous cell carcinoma
1
4
1
6
Adenocarcinoma
0
1
1
2
Undifferentiated sinonasal carcinoma
0
1
1
2
Ameloblastoma
0
1
0
1
Inverted papilloma
0
1
0
1
Metastatic clear cell carcinoma
0
1
0
1
Solitary fibrous tumor
0
1
0
1
Total
30
durotomy circumvented the infiltrating tumor and was followed by dividing the inferior portion of the falx cerebri. The exposed basal aspect of both frontal lobes and along the interhemispheric fissure showed no signs of brain invasion (Figure 2). The reconstruction of the skull base defect was accomplished in a multilayer fashion using synthetic dural substitute, fascia lata, and fibrin glue. The patient tolerated the procedure well, and there was no CSF leak postoperatively. All resection margins were negative in the final pathology report. Postoperative imaging showed the complete resection of the tumor (Figure 3).
PER, pure endoscopic resection; CFR, craniofacial resection.
Figure 1. Case 1 (endoscopic approach). Preoperative axial (A), coronal (B), and sagittal (C) T1-weighted magnetic resonance images with gadolinium showing tumor in the left nasal cavity. Coronal computed tomography image (D) shows bone infiltration of the left ethmoid and maxillary sinuses.
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Case 2 (CFR). A 30-year-old man presented with a 2-month complaint of nasal obstruction, right-sided progressive exophthalmos, and mild diplopia. Imaging examinations revealed a 6 cm 6 cm mass centered in the superior nasal cavity and cribriform plate, with extension to the right orbit and to the right frontal lobe (Figure 4). He had a remote history of a left frontal metastasis of a testis choriocarcinoma, which was resected and irradiated 12 years earlier, without signs of local or distant recurrence. A biopsy revealed a sinonasal undifferentiated carcinoma. Because of the significant intraorbital and transdural extension, an endoscopic approach did not seem favorable. Further irradiation to the region was not recommended so the patient received preoperative chemotherapy only. A reduction in tumor volume was documented. A combined craniofacial approach was performed. A bicoronal incision was made, and a bifrontal craniotomy provided subfrontal access to the superior portion of the tumor that invaded the brain as well as the upper nasal cavity portion. A circumferential orbit incision was made to proceed with the orbital exenteration. After gross total resection, a watertight duroplasty was performed with fascia lata, and a pedicled pericranial flap was layered over the skull base defect. The cavity of the facial resection was sealed with a vascularized left rectus abdominis free flap with skin graft. Negative margins were achieved with this approach, and the patient tolerated the procedure well.
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Figure 2. Case 1 (endoscopic approach). Intraoperative photos showing durotomy around the tumor (A) and the exposed frontal lobes (B).
DISCUSSION The use of and indications for endoscopic surgery of paranasal and skull base lesions have progressively expanded. The use of these techniques to treat benign paranasal sinus pathology has been widely accepted with equivalent or better results than open
approaches. Repairs of CSF leaks, encephaloceles, juvenile angiofibromas, capillary hemangiomas, solitary fibrous lesions, and osteomas, with some exceptions based on anatomic considerations are done exclusively using a pure endoscopic approach. Endoscopic techniques
Figure 3. Case 1 (endoscopic approach). Postoperative T1-weighted axial (A and C) and coronal (B and D) magnetic resonance images with gadolinium showing complete resection of the tumor.
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have also supplanted open approaches for midline clival extradural lesions such as chordomas. The indications for endoscopic surgery have also expanded to include resection of the anterior bony skull base with the adjacent dura mater that can be accessed from the frontal sinus, clivus to the foramen magnum. The lateral limitation of the approach for malignant disease is both laminae papyracea. Reconstruction, especially prevention of CSF leak, has proved to be a significant challenge and potentially a major limitation for this technique. Evolving techniques for repair, including the introduction of pedicled vascularized mucosal flaps for repair of dural defects and prevention of CSF leak, have had a positive impact and have helped to legitimize the technique (3, 7, 20). Also, interest in expanding the technique to the removal of intradural pathology such as meningiomas and craniopharyngiomas has developed. Although some controversy remains regarding the role of endoscopic techniques for the removal of intradural lesions, we and other authors believe that with increasing experience and careful patient selection these techniques will have an important role in the future. Despite the widespread acceptance of the endoscopic approach and early favorable results, concerns have remained about the long-term outcome results of patients undergoing endoscopic procedures for malignancies, especially with regard to the ability to achieve total resection with clear margins and the potential for increased risk of recurrence. After reviewing and comparing the results of combined traditional and endoscopic techniques in their own patient cohorts, Eloy et al. (4) concluded that the only absolute contraindication to the endoscopic approach was invasion of the facial soft tissues by the malignancy. Relative contraindications included highly vascular tumors, the need for orbital exenteration, lateral tumor extension with invasion of the pterygomaxillary space or infratemporal fossa, and extensive bilateral disease (4). The earlier retrospective comparison by the same authors between patients who were treated with transnasal endoscopic resection (n ¼ 18) or CFR (n ¼ 48) for tumors involving the anterior skull base
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Figure 4. Case 2 (craniofacial resection). Preoperative axial (A and C) and coronal (B and D) T1-weighted magnetic resonance images with gadolinium showing the tumor filling the nasal cavity and extending into the right orbit and right frontal lobe.
yielded a median hospital stay of 3.5 days versus 7.0 days and median operative time of 261.5 minutes versus 625.5 minutes. The perioperative complications were similar in the 2 groups: 27.8% versus 25%. The CFR group had a significant and much higher percentage of stage IV disease (60.4% vs. 11.1%) and histologically more aggressive tumors (52.1% squamous cell carcinoma in the CFR group compared with 55.6% olfactory neuroblastoma in the transnasal endoscopic resection group). The rate of recurrence was much higher in the CFR group almost reaching statistical significance (P ¼ 0.051). It is likely that the increased numbers of histologically more aggressive tumors may explain the higher recurrence rate in the CFR group. Use of advanced endoscopic equipment, improvement in lighting and optics, and the ability to navigate into spaces that the traditional open approach and microscopic angles do not allow may facilitate more
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complete removal of the pathology. Although the differences in histology and tumor staging in the 2 groups made it difficult to reach a definite conclusion, it was thought that early-stage and intermediate-stage anterior skull base malignancies can be safely and successfully treated with transnasal endoscopic resection (4). Raza et al. (15) summarized all studies assessing surgical resection of craniofacial malignancies over a period of 10 years looking at CFR and total endoscopic approach. By studying their table of study comparisons, it becomes apparent how diverse the data are: overall complication rates ranging from 9.7% using CFR on mainly esthesioneuroblastomas (29%) and squamous cell carcinomas (27%) achieving negative margins in 85% of the cases to an overall complication rate of 59.1% by CFR for mainly juvenile angiofibroma (21.9%) and esthesioneuroblastoma (9.8%)
achieving a gross total resection of 73% (15). In their table, Raza et al. mentioned the endoscopic complication rate (27.8%) reported by Eloy et al. (4), although they were able to cite the degree of extent of resection by Eloy et al. Batra et al. (2) compared the endoscopic experience with traditional CFR for the management of anterior skull base neoplasia looking at tumors of comparable extension into contiguous structures. They found that the endoscopic group (22%) had fewer complications than the traditional CFR group (44%). Our own experience suggests that the most important principle should be initially to determine the goal of the surgery regardless of technique. When the goal is established (i.e., total resection, partial resection, palliative), that goal should be the same and not altered because of the approach ultimately used. The goal of an endoscopic resection for any lesion should be identical to that of an open craniofacial approach—as complete and safe tumor removal as possible with minimal morbidity and the meticulous pursuit of negative margins. If both open and endoscopic approaches can achieve the stated goal, the more minimally invasive endoscopic approach is chosen. These principles and objectives should be tempered only when a conscious decision is made to leave residual disease based on a desire not to compromise critical neurovascular structures (optic nerves, internal carotid artery) that may result in unacceptable morbidity for the patient. Technical developments, intraoperative use of neuronavigational systems and small ultrasound Doppler probes, use of effective hemostatic agents, and advances in cross-sectional imaging all have increased the accuracy of preoperative diagnosis improving appropriate patient selection for these techniques. The decision of whether to use the traditional CFR or the (expanded) endoscopic approach for paranasal and anterior skull base malignancies must be based on a careful preoperative assessment of the location and extent and invasiveness of the tumor based on currently available sophisticated imaging techniques. In making this decision, the basic principles of oncologic surgery must be maintained—achieving gross total removal of the lesion with clear margins. In the case
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of esthesioneuroblastoma, the lateral extension of dural disease is a critical factor. If it is believed that the principles of oncologic surgery can be maintained by the endoscopic approach, the technique is a safe and viable alternative to an open procedure. When there is any doubt of the ability to achieve free margins, an open or combined approach should be considered. If there is clear uncertainty, the option is to use an open approach or begin with the endoscopic approach but be prepared to convert to an open approach. There is little question that these complex expanded endoscopic skull base techniques require an expert multidisciplinary team of oncologically trained ear, nose, and throat endoscopists and endoscopically trained neurosurgeons. Because of the relative rarity of these lesions, the team should have experience with and be able to offer, based on the nature and extent of the lesion, both the open and the endoscopic approach to the patient.
CONCLUSIONS CFR remains the “gold standard” for anterior skull base malignancy, and when combined with adjuvant radiation with or without chemotherapy, this technique has had a very positive impact on treatment results of paranasal sinus malignancies extending to the anterior cranial fossa. The search for innovative less invasive techniques that carry less morbidity and mortality has led to the use of endoscopic approaches to the paranasal sinuses and skull base. These techniques, which are becoming more widely accepted, are a valuable addition to the armamentarium of the skull base surgeon. The key to the appropriate use of these techniques is careful patient selection. Although it is unlikely a randomized trial will ever be feasible, careful ongoing evaluation of results including outcomes, morbidity, and recurrence rates in larger groups of patients with longer follow-up times is necessary to define better the appropriate indications and ideal patient population that would benefit from the use of these newer techniques.
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ACKNOWLEDGMENT We would like to acknowledge and thank the members of the Departments of Otolaryngology and Head and Neck Surgery of the University of Toronto who participated in the patients’ treatment. REFERENCES 1. Airoldi M, Garzaro M, Valente G, Mamo C, Bena A, Giordano C, Pecorari G, Gabriele P, Gabriele AM, Beatrice F: Clinical and biological prognostic factors in 179 cases with sinonasal carcinoma treated in the Italian Piedmont region. Oncology 76:262-269, 2009. 2. Batra PS, Citardi MJ, Worley S, Lee J, Lanza DC: Resection of anterior skull base tumors: comparison of combined traditional and endoscopic techniques. Am J Rhinol 19:521-528, 2005. 3. Carrau RL, Kassam AB, Snyderman CH, Duvvuri U, Mintz A, Gardner P: Endoscopic transnasal anterior skull base resection for the treatment of sinonasal malignancies. Oper Tech Otolaryngol Head Neck Surg 17:102-110, 2006. 4. Eloy JA, Vivero RJ, Hoang K, Civantos FJ, Weed DT, Morcos JJ, Casiano RR: Comparison of transnasal endoscopic and open craniofacial resection for malignant tumors of the anterior skull base. Laryngoscope 119:834-840, 2009. 5. Ganly I, Patel SG, Singh B, Bridger PG, Cantu G, Cheesman A, De Sa G, Donald P, Fliss D, Gullane P, Janecka I, Kamata SE, Kowalski LP, Levine P, Medina LR, Pradhan S, Schramm V, Snyderman C, Wei WI, Shah JP: Complications of craniofacial resection for malignant tumors of the skull base: report of an International Collaborative Study. Head Neck 27:445-451, 2005. 6. Gil Z, Fliss DM, Cavel O, Shah JP, Kraus DH: Improvement in survival during the past 4 decades among patients with anterior skull base cancer. Head Neck 34:1212-1219, 2012. 7. Hadad G, Bassagasteguy L, Carrau RL, Mataza JC, Kassam A, Snyderman CH, Mintz A: A novel reconstructive technique after endoscopic expanded endonasal approaches: vascular pedicle nasoseptal flap. Laryngoscope 116:1882-1886, 2006. 8. Kassam A, Snyderman CH, Mintz A, Gardner P, Carrau RL: Expanded endonasal approach: the rostrocaudal axis. Part I: crista galli to the sella turcica. Neurosurg Focus 19:E3, 2005. 9. Komotar RJ, Starke RM, Raper DM, Anand VJ, Schwartz TH: Endoscopic endonasal compared with anterior craniofacial and combined cranionasal resection of esthesioneuroblastomas. World Neurosurg 80:148-159, 2013. 10. Ketcham S, Wilkins RH, Vanburen JM, Smith RR: A combined intracranial facial approach to the paranasal sinuses. Am J Surg 106:698-703, 1963. 11. Kraus DH, Shah JP, Arbit E, Galicich JH, Strong EW: Complications of craniofacial
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resection for tumors involving the anterior skull base. Head Neck 16:307-312, 1994. 12. Nicolai P, Castelnuovo P, Lombardi D, Battaglia P, Bignami M, Pianta L, Tomenzoli D: Role of endoscopic surgery in the management of selected malignant epithelial neoplasms of the nasoethmoidal complex. Head Neck 29:1075-1082, 2007. 13. Nicolai P, Castelnuovo P, Bolzoni Villaret A: Endoscopic resection of sinonasal malignancies. Curr Oncol Rep 13:138-144, 2011. 14. Patel SG, Singh B, Polluri A, Bridger PG, Cantu G, Cheesman AD, deSa GM, Donald P, Fliss D, Gullane P, Janecka I, Kamata SE, Kowalski LP, Kraus DH, Levine PA, dos Santos LR, Pradhan S, Schramm V, Snyderman C, Wei WI, Shah JP: Craniofacial surgery for malignant skull base tumors: report of an international collaborative study. Cancer 15:1179-1187, 2003. 15. Raza SM, Garzon-Muvdi T, Gallia GL, Tamargo RJ: Craniofacial resection of midline anterior skull base malignancies: a reassessment of outcomes in the modern era. World Neurosurg 25:1-9, 2012. 16. Stammberger H: Endoscopic endonasal surgery— concepts in treatment of recurring rhinosinusitis. Part II: surgical technique. Otolaryngol Head Neck Surg 94:147-156, 1986. 17. Suh JD, Ramakrishnan VR, Chi JJ, Palmer JN, Chiu AG: Outcomes and complications of endoscopic approaches for malignancies of the paranasal sinuses and anterior skull base. Ann Otol Rhinol Laryngol 122:54-59, 2013. 18. Thaler ER, Kotapka M, Lanza DC, Kennedy DW: Endoscopically assisted anterior cranial skull base resection of sinonasal tumors. Am J Rhinol 13: 303-310, 1999. 19. Yuen AP, Fung CF, Hung KN: Endoscopic cranionasal resection of anterior skull base tumor. Am J Otolaryngol 18:431-433, 1997. 20. Zanation AM, Carrau RL, Snyderman CH, Germanwala AV, Gardner PA, Prevedello DM, Kassam AB: Nasoseptal flap reconstruction of high flow intraoperative cerebral spinal fluid leaks during endoscopic skull base surgery. Am J Rhinol Allergy 23:518-521, 2009.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 18 September 2013; accepted 25 July 2014 Citation: World Neurosurg. (2014) 82, 6S:S59-S65. http://dx.doi.org/10.1016/j.wneu.2014.07.026 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
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From Craniofacial Resection to Endonasal Endoscopic Removal of Malignant Tumors of the Anterior Skull Base Boris Krischek1,2, Felipe G. Carvalho2, Bruno Loyola Godoy2, Rasmus Kiehl3, Gelareh Zadeh2, Fred Gentili2
Key words Anterior skull base surgery - Craniofacial resection - Expanded endoscopic endonasal approach -
Abbreviations and Acronyms CER: Cranio-endoscopic resection CFR: Craniofacial resection CSF: Cerebrospinal fluid PER: Pure endoscopic resection From the 1Department of Neurosurgery, University of Cologne, Germany; 2Department of Neurosurgery, Toronto Western Hospital, Toronto, Canada; and 3Department of Neuropathology, University Health Network, Toronto, Canada To whom correspondence should be addressed: Fred Gentili, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014) 82, 6S:S59-S65. http://dx.doi.org/10.1016/j.wneu.2014.07.026 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
- OBJECTIVE:
To review the current literature and provide our institutional approach and opinion on the indications and limitations of traditional open craniofacial resection (CFR) and a minimally invasive pure endonasal endoscopic approach for anterior skull base tumors concentrating primarily on malignant lesions.
- METHODS:
Based on 3 decades of experience with both open and more recently endoscopic techniques, we examined our current practice in treating tumors and other lesions involving the skull base and our current indications and limitations in the use of these techniques. We conducted a retrospective chart analysis to see which operative techniques were used for malignant tumors of the anterior skull base in the last 10 years at our institution.
- RESULTS:
There were 30 cases identified. Traditional CFR was performed in 16, a pure endoscopic resection was performed in 9, and an endoscopic procedure combined with a frontal craniotomy was performed in 5. Gross total resection was achieved in 83.3% in the CFR group and 75% in the pure endoscopic resection group. Near-total resection was 10% in the CFR group and 33.3% in pure endoscopic resection group. Of the 5 patients who underwent a combined approach, 80% had gross total resection, and 20% had near-total resection.
- CONCLUSIONS:
INTRODUCTION There have been significant developments in the area of skull base surgery in the last 3 decades. From the initial skepticism of the specialty to its widespread acceptance as well as the subsequent acknowledgment of the limitations, the techniques of open skull base surgery have had overall a very positive impact on management of many difficult tumors and other complex lesions involving the skull base. Many factors contributed to success in this field, including the application of microsurgical techniques, development of innovative surgical approaches based on improved knowledge of the relevant anatomy, improved imaging, improved anesthesia, and expert preoperative and postoperative care. An important factor was the novel development of multidiscilinary surgical teams. The original approach first described by Ketcham et al. in 1963 (10) combined a cranial (bifrontal craniotomy) and facial (lateral rhinotomy, maxillectomy, or
Both traditional CFR and the endonasal endoscopic approach offer advantages and disadvantages. Both approaches can achieve good results with appropriate patient selection. Numerous important factors, including location and the extent of tumor, should be taken into consideration when considering either approach. The most important determinant of outcome is the ability to achieve gross total resection with microscopic negative margins rather than the type of approach used. In the future, skull base surgeons will need to be familiar with and capable of offering both techniques to the patient.
sinusotomies) exposure performed by a team of neurosurgeons and otolaryngologists. This craniofacial resection (CFR) provided improved exposure of lesions in the paranasal sinuses and lesions involving both the intracranial and the extracranial compartments of the skull base. The subsequent addition of plastic and reconstructive surgeons and radiation and medical oncologists to the team provided a comprehensive approach to the management of lesions previously thought to be inoperable or associated with significant surgical morbidity. Craniofacial approaches helped facilitate more complete resection with significant improvement in
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overall and disease-specific survival as well as reduced recurrence rates in patients with anterior skull base cancer (2, 5). Patients with benign pathology could achieve long-term survival and, in many cases, cure. Likewise, even patients with aggressive pathologies such as squamous cell cancers of the paranasal sinuses previously associated with very poor prognosis and low survival (1) could achieve long-term survival (3, 6, 17). There are numerous advantages of the open approaches in skull base surgery. They have become well-known procedures incorporated into most residency training programs with no need for a learning curve.
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Likewise, there are no issues with regard to lack of binocular vision or the ability to use microsurgical technique and the required instrument manipulation. Wellrecognized and effective reconstruction techniques are available with low rates of cerebrospinal fluid (CSF) leakage. Lastly, long-term outcome data including overall and progression-free survival are known. Despite the development of newer, less invasive endoscopic techniques (discussed subsequently), traditional open techniques continue to play an important role in skull base surgery and remain primary strategies in the treatment of many anterior and anterolateral skull base malignancies. However, not all of the initial hopes and expectations of open skull base surgery were realized, and many sober lessons were learned. The extremely varied pathology of lesions involving the skull base made it difficult to accrue large series of patients with uniform pathologies. Although there were efforts to carry out multiinstitutional trials, few came to fruition, and most reports in the literature were individual personal series with a limited number of patients and short follow-up times, and results were difficult to interpret. It also became evident that ever larger incisions and exposures and more radical surgery, often associated with increased morbidity, were not always associated with improved outcomes and that tumor biology, not surgical technique, in many cases was the critical factor in survival. In addition, despite continued refinements in surgical technique, open approaches still required some degree of brain retraction and neurovascular manipulation and continued to carry significant perioperative risks and morbidity with prolonged recovery time. Complication rates of most published series of CFR, including more recent reports, are 40% with postoperative mortality approximating 5% (5, 9, 11, 14). Although outcomes in skull base surgery previously had focused primarily on survival and complications, a heightened awareness developed of functional outcome and quality of life and costs/benefit issues. Even ethical concerns were expressed by some of carrying out major resections with significant morbidity without hard scientific evidence of efficacy. In an attempt to address some of the shortcomings of open skull base surgery, surgeons sought less invasive
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techniques to approach the anterior skull base culminating in increasingly accepted and currently widely used endoscopic techniques. The endonasal endoscopic skull base approach, developed from concepts applied from the field of rhinology and functional endoscopic sinus surgery introduced in the 1980s (16), revolutionized the treatment of inflammatory diseases and lesions limited to the sinonasal tract. For tumors, the endoscopic approach was initially limited to benign pathologies and other nontumorous lesions involving the sinonasal tract that did not extend up to the anterior skull base. The first reports on pure endoscopic procedures alone or in combination with frontal craniotomy (the cranionasal approach) emerged in the late 1990s (18, 19). The approach subsequently was used for selected cases of malignant tumors. Following the publication of several series analyzing small and intermediate-size cohorts of patients, there was considerable criticism from physicians who believed that endoscopic surgery by its very nature did not adhere to the principles of oncologic surgery—that is, the tumor was removed in a piecemeal fashion, and an en bloc resection was not achieved (13). Likewise, numerous contraindications for the endoscopic approach were cited, including extension to the frontal sinus, involvement of the lacrimal pathway or of the bony walls of the maxillary sinus (with the exception of the medial wall), erosion of the nasal fossa floor, extension into the pterygopalatine or infratemporal fossa, involvement of the orbit, and erosion of the skull base (12). Criticism was countered by the acknowledgment that even in open procedures true en bloc resection is often difficult to achieve and that the critical and major determinant of a patient’s overall and progression-free survival was not the technique of removal but the ability to achieve a gross total resection with microscopic negative margins (4). More recent data have shown that in well-selected patients endoscopic resection of paranasal sinus malignancies, including tumors that extend to the anterior skull base, can be achieved with acceptable morbidity and outcomes (9). The determinants of success of endonasal endoscopic surgery of the skull base have been similar to the factors enumerated earlier for open skull base
surgery—advances in endoscopic technology, improved understanding of endonasal skull base anatomy, and a multidisciplinary team approach. The collaboration of otolaryngologists and neurosurgeons using a 2-nostril, bimanual technique significantly advanced endoscopic techniques, and various surgical modules subsequently were described that encompassed the entire ventral skull base (8). Endoscopic techniques subsequently were expanded to include the removal of intradural pathology (3). These expanded endoscopic approaches, although a more recent addition, have become widely adopted and have had a dramatic impact not only on pituitary surgery but also on the entire field of skull base surgery. The advantages of this less invasive approach include a more direct anatomic route, no need for craniotomy or facial incisions, less trauma to the brain and neurovascular structures, early devascularization of the tumor blood supply, improved visualization of the relevant anatomy, and better cosmetic results with shorter recovery times. However, there are important prerequisites for success in using these approaches, including a detailed knowledge of anatomy, an interdisciplinary team of experienced endoscopists, use of a 2-nostril bimanual approach that allows for the use of microsurgical technique as employed in open procedures, advanced multiangled endoscopes, appropriate instrumentation, and high-definition cameras and screens. It is also important that the surgical team have adequate knowledge of the limitations of the endoscopic techniques as well as experience with the traditional open approaches so that the most appropriate surgical approach can be tailored to each individual patient. In addition, adequate training is required because there is a significant learning curve. In the last 3 decades, the authors have had experience with open skull base approaches (>2000 cases) and, more recently, increasing experience with endoscopic approaches (>850 cases). Most endoscopic procedures have been performed for pituitary surgery with expanded approaches to the skull base representing 22% of all endoscopic procedures. The types of lesions and pathologies are listed in Table 1. Although there is a role for the use of endoscopic techniques for more laterally placed lesions in the paranasal
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Table 1. Histology of Cases in Which an Expanded Endonasal Endoscopic Approach Was Used Diagnosis
Number of Cases
Craniopharyngioma
32
Chordoma
22
Meningioma
25
Esthesioneuroblastoma
10
Pituitary adenoma
11
Encephalocele
10
Other
54
Total
164
sinuses using transpterygoid and transcavernous approaches, we have used the endoscopic technique for lesions and pathologies that primarily involve the midline skull base. Based on this experience, in this article, we examine our current practice in dealing with tumors and other lesions involving the skull base and provide our current indications and limitations in the use of these techniques. Because of the breadth of the subject, we have limited our review to malignant lesions.
MATERIALS AND METHODS Retrospective chart analysis was conducted to identify patients undergoing resection of malignant anterior skull base tumors between January 2002 and January 2013 performed by the senior author (FG) at the Toronto Western Hospital. There were 30 patients identified. Demographic data, symptoms, follow-up, and tumor characteristics were collected from the records. Records were evaluated for patient age, sex, diagnosis, anatomic site, symptoms, surgical approach, extent of surgical resection, surgical complications, and recurrence. All patients included in this series underwent a traditional CFR, a pure endoscopic resection (PER), or in selected cases an endoscopic procedure combined with frontal craniotomy (cranioendoscopic resection [CER]). Operative Procedure There were 16 patients in the CFR group, and all underwent a standard bifrontal craniotomy. Tumor extirpation was
achieved via PER in 9 patients. Combined CER was performed in 5 patients for reasons discussed subsequently. RESULTS Demographic Data Tumor resection was performed in 30 patients (19 men and 11 women) with an overall mean age of 58.2 years (range, 20e78 years). The mean age was 49.8 years (range, 24e77 years) in the PER group and 56.4 years (range, 37e78 years) in the CFR group. The percentage of female patients in the PER group was 33% (3 of 9) compared with 37.5% (7 of 21) in the CFR and CER groups. The median followup for the PER group was 4.2 years (range, 0.3e7.3 years) and for the CFR and CER groups was 4.7 years (range, 0.2e10.7 years). Table 2 lists the presenting symptoms of the group as a whole. The primary presenting complaint in this group as a whole was nasal airway obstruction. Tumor Characteristics A wide variety of pathologies were treated with the most common diagnosis being esthesioneuroblastoma (53.3%), followed by squamous cell carcinoma (20%), adenocarcinoma (6.67%), undifferentiated sinonasal carcinoma (6.67%), and various other, less frequently diagnosed lesions (Table 3). Extent of Resection and Recurrence Gross total resection was achieved in 83.3% in the CFR group and 75% in the PER group. Near-total resection was 10% in the CFR group and 33.3% in the PER group. Of the 5 patients who underwent a
Table 2. Symptoms of 30 Treated Patients Symptom Sinusitis/nasal obstruction
Number of Patients (%) 17 (57)
Visual complaints
6 (20)
Epistaxis
5 (17)
Proptosis
5 (17)
Headache/local pain
4 (13)
Asymptomatic
1 (3)
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combined approach, 80% had gross total resection, and 20% had near-total resection. Recurrences were observed in 2 of 7 (29%) of the patients in the PER group and 5 of 13 (38%) of the patients in the CFR group. Of the 5 patients treated with the combined approach, none presented with recurrence. There were 5 patients lost to follow-up. Complications In the patients who underwent PER, there were 2 CSF leaks and 1 case of sinusitis. In the patients who underwent CFR, there were 2 wound infections, 1 flap infection, 1 pneumocephalus, 1 abscess, and 1 osteonecrotic bone flap. In the 5 patients who underwent the combined procedure (CER), 1 patient experienced a deep vein thrombosis. Illustrative Cases Case 1 (PER). A 59-year-old man who was a former smoker had been complaining of nasal obstruction for the past 6 months. Imaging examinations revealed a mass in the left nasal cavity with involvement of septal mucosa and extension to the nasopharynx and the left anterior skull base (Figure 1). The histopathology result from a biopsy procedure was sinonasal undifferentiated carcinoma). The patient underwent chemotherapy and radiotherapy before surgical resection. There was a satisfactory response to radiation, with a significant decrease in the tumor volume. The tumor resection was performed via an expanded endoscopic endonasal transsphenoidal approach. Because the tumor appeared to involve the septal mucosa, including the right side, no pedicled nasoseptal flap was planned for reconstruction of the anterior skull base. Fascia lata was harvested from the right thigh for the repair of the skull base defect. The main steps of the procedure involved bilateral middle turbinectomies, posterior septectomy, ethmoidectomy, wide bilateral sphenoidotomy, and bilateral maxillary antrostomies. After the resection of the tumor in the nasal cavity, the lamina papyracea was removed on both sides, carefully dissecting and coagulating the anterior and posterior ethmoidal arteries of both sides. The final stage of the procedure was osteotomy of the anterior fossa around the cribriform plate, resecting it together with the crista galli. The
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Table 3. Tumor Histology of Operated Cases PER
CFR
Combined
Total
Esthesioneuroblastoma
8
6
2
16
Squamous cell carcinoma
1
4
1
6
Adenocarcinoma
0
1
1
2
Undifferentiated sinonasal carcinoma
0
1
1
2
Ameloblastoma
0
1
0
1
Inverted papilloma
0
1
0
1
Metastatic clear cell carcinoma
0
1
0
1
Solitary fibrous tumor
0
1
0
1
Total
30
durotomy circumvented the infiltrating tumor and was followed by dividing the inferior portion of the falx cerebri. The exposed basal aspect of both frontal lobes and along the interhemispheric fissure showed no signs of brain invasion (Figure 2). The reconstruction of the skull base defect was accomplished in a multilayer fashion using synthetic dural substitute, fascia lata, and fibrin glue. The patient tolerated the procedure well, and there was no CSF leak postoperatively. All resection margins were negative in the final pathology report. Postoperative imaging showed the complete resection of the tumor (Figure 3).
PER, pure endoscopic resection; CFR, craniofacial resection.
Figure 1. Case 1 (endoscopic approach). Preoperative axial (A), coronal (B), and sagittal (C) T1-weighted magnetic resonance images with gadolinium showing tumor in the left nasal cavity. Coronal computed tomography image (D) shows bone infiltration of the left ethmoid and maxillary sinuses.
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Case 2 (CFR). A 30-year-old man presented with a 2-month complaint of nasal obstruction, right-sided progressive exophthalmos, and mild diplopia. Imaging examinations revealed a 6 cm 6 cm mass centered in the superior nasal cavity and cribriform plate, with extension to the right orbit and to the right frontal lobe (Figure 4). He had a remote history of a left frontal metastasis of a testis choriocarcinoma, which was resected and irradiated 12 years earlier, without signs of local or distant recurrence. A biopsy revealed a sinonasal undifferentiated carcinoma. Because of the significant intraorbital and transdural extension, an endoscopic approach did not seem favorable. Further irradiation to the region was not recommended so the patient received preoperative chemotherapy only. A reduction in tumor volume was documented. A combined craniofacial approach was performed. A bicoronal incision was made, and a bifrontal craniotomy provided subfrontal access to the superior portion of the tumor that invaded the brain as well as the upper nasal cavity portion. A circumferential orbit incision was made to proceed with the orbital exenteration. After gross total resection, a watertight duroplasty was performed with fascia lata, and a pedicled pericranial flap was layered over the skull base defect. The cavity of the facial resection was sealed with a vascularized left rectus abdominis free flap with skin graft. Negative margins were achieved with this approach, and the patient tolerated the procedure well.
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Figure 2. Case 1 (endoscopic approach). Intraoperative photos showing durotomy around the tumor (A) and the exposed frontal lobes (B).
DISCUSSION The use of and indications for endoscopic surgery of paranasal and skull base lesions have progressively expanded. The use of these techniques to treat benign paranasal sinus pathology has been widely accepted with equivalent or better results than open
approaches. Repairs of CSF leaks, encephaloceles, juvenile angiofibromas, capillary hemangiomas, solitary fibrous lesions, and osteomas, with some exceptions based on anatomic considerations are done exclusively using a pure endoscopic approach. Endoscopic techniques
Figure 3. Case 1 (endoscopic approach). Postoperative T1-weighted axial (A and C) and coronal (B and D) magnetic resonance images with gadolinium showing complete resection of the tumor.
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have also supplanted open approaches for midline clival extradural lesions such as chordomas. The indications for endoscopic surgery have also expanded to include resection of the anterior bony skull base with the adjacent dura mater that can be accessed from the frontal sinus, clivus to the foramen magnum. The lateral limitation of the approach for malignant disease is both laminae papyracea. Reconstruction, especially prevention of CSF leak, has proved to be a significant challenge and potentially a major limitation for this technique. Evolving techniques for repair, including the introduction of pedicled vascularized mucosal flaps for repair of dural defects and prevention of CSF leak, have had a positive impact and have helped to legitimize the technique (3, 7, 20). Also, interest in expanding the technique to the removal of intradural pathology such as meningiomas and craniopharyngiomas has developed. Although some controversy remains regarding the role of endoscopic techniques for the removal of intradural lesions, we and other authors believe that with increasing experience and careful patient selection these techniques will have an important role in the future. Despite the widespread acceptance of the endoscopic approach and early favorable results, concerns have remained about the long-term outcome results of patients undergoing endoscopic procedures for malignancies, especially with regard to the ability to achieve total resection with clear margins and the potential for increased risk of recurrence. After reviewing and comparing the results of combined traditional and endoscopic techniques in their own patient cohorts, Eloy et al. (4) concluded that the only absolute contraindication to the endoscopic approach was invasion of the facial soft tissues by the malignancy. Relative contraindications included highly vascular tumors, the need for orbital exenteration, lateral tumor extension with invasion of the pterygomaxillary space or infratemporal fossa, and extensive bilateral disease (4). The earlier retrospective comparison by the same authors between patients who were treated with transnasal endoscopic resection (n ¼ 18) or CFR (n ¼ 48) for tumors involving the anterior skull base
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Figure 4. Case 2 (craniofacial resection). Preoperative axial (A and C) and coronal (B and D) T1-weighted magnetic resonance images with gadolinium showing the tumor filling the nasal cavity and extending into the right orbit and right frontal lobe.
yielded a median hospital stay of 3.5 days versus 7.0 days and median operative time of 261.5 minutes versus 625.5 minutes. The perioperative complications were similar in the 2 groups: 27.8% versus 25%. The CFR group had a significant and much higher percentage of stage IV disease (60.4% vs. 11.1%) and histologically more aggressive tumors (52.1% squamous cell carcinoma in the CFR group compared with 55.6% olfactory neuroblastoma in the transnasal endoscopic resection group). The rate of recurrence was much higher in the CFR group almost reaching statistical significance (P ¼ 0.051). It is likely that the increased numbers of histologically more aggressive tumors may explain the higher recurrence rate in the CFR group. Use of advanced endoscopic equipment, improvement in lighting and optics, and the ability to navigate into spaces that the traditional open approach and microscopic angles do not allow may facilitate more
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complete removal of the pathology. Although the differences in histology and tumor staging in the 2 groups made it difficult to reach a definite conclusion, it was thought that early-stage and intermediate-stage anterior skull base malignancies can be safely and successfully treated with transnasal endoscopic resection (4). Raza et al. (15) summarized all studies assessing surgical resection of craniofacial malignancies over a period of 10 years looking at CFR and total endoscopic approach. By studying their table of study comparisons, it becomes apparent how diverse the data are: overall complication rates ranging from 9.7% using CFR on mainly esthesioneuroblastomas (29%) and squamous cell carcinomas (27%) achieving negative margins in 85% of the cases to an overall complication rate of 59.1% by CFR for mainly juvenile angiofibroma (21.9%) and esthesioneuroblastoma (9.8%)
achieving a gross total resection of 73% (15). In their table, Raza et al. mentioned the endoscopic complication rate (27.8%) reported by Eloy et al. (4), although they were able to cite the degree of extent of resection by Eloy et al. Batra et al. (2) compared the endoscopic experience with traditional CFR for the management of anterior skull base neoplasia looking at tumors of comparable extension into contiguous structures. They found that the endoscopic group (22%) had fewer complications than the traditional CFR group (44%). Our own experience suggests that the most important principle should be initially to determine the goal of the surgery regardless of technique. When the goal is established (i.e., total resection, partial resection, palliative), that goal should be the same and not altered because of the approach ultimately used. The goal of an endoscopic resection for any lesion should be identical to that of an open craniofacial approach—as complete and safe tumor removal as possible with minimal morbidity and the meticulous pursuit of negative margins. If both open and endoscopic approaches can achieve the stated goal, the more minimally invasive endoscopic approach is chosen. These principles and objectives should be tempered only when a conscious decision is made to leave residual disease based on a desire not to compromise critical neurovascular structures (optic nerves, internal carotid artery) that may result in unacceptable morbidity for the patient. Technical developments, intraoperative use of neuronavigational systems and small ultrasound Doppler probes, use of effective hemostatic agents, and advances in cross-sectional imaging all have increased the accuracy of preoperative diagnosis improving appropriate patient selection for these techniques. The decision of whether to use the traditional CFR or the (expanded) endoscopic approach for paranasal and anterior skull base malignancies must be based on a careful preoperative assessment of the location and extent and invasiveness of the tumor based on currently available sophisticated imaging techniques. In making this decision, the basic principles of oncologic surgery must be maintained—achieving gross total removal of the lesion with clear margins. In the case
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of esthesioneuroblastoma, the lateral extension of dural disease is a critical factor. If it is believed that the principles of oncologic surgery can be maintained by the endoscopic approach, the technique is a safe and viable alternative to an open procedure. When there is any doubt of the ability to achieve free margins, an open or combined approach should be considered. If there is clear uncertainty, the option is to use an open approach or begin with the endoscopic approach but be prepared to convert to an open approach. There is little question that these complex expanded endoscopic skull base techniques require an expert multidisciplinary team of oncologically trained ear, nose, and throat endoscopists and endoscopically trained neurosurgeons. Because of the relative rarity of these lesions, the team should have experience with and be able to offer, based on the nature and extent of the lesion, both the open and the endoscopic approach to the patient.
CONCLUSIONS CFR remains the “gold standard” for anterior skull base malignancy, and when combined with adjuvant radiation with or without chemotherapy, this technique has had a very positive impact on treatment results of paranasal sinus malignancies extending to the anterior cranial fossa. The search for innovative less invasive techniques that carry less morbidity and mortality has led to the use of endoscopic approaches to the paranasal sinuses and skull base. These techniques, which are becoming more widely accepted, are a valuable addition to the armamentarium of the skull base surgeon. The key to the appropriate use of these techniques is careful patient selection. Although it is unlikely a randomized trial will ever be feasible, careful ongoing evaluation of results including outcomes, morbidity, and recurrence rates in larger groups of patients with longer follow-up times is necessary to define better the appropriate indications and ideal patient population that would benefit from the use of these newer techniques.
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ACKNOWLEDGMENT We would like to acknowledge and thank the members of the Departments of Otolaryngology and Head and Neck Surgery of the University of Toronto who participated in the patients’ treatment. REFERENCES 1. Airoldi M, Garzaro M, Valente G, Mamo C, Bena A, Giordano C, Pecorari G, Gabriele P, Gabriele AM, Beatrice F: Clinical and biological prognostic factors in 179 cases with sinonasal carcinoma treated in the Italian Piedmont region. Oncology 76:262-269, 2009. 2. Batra PS, Citardi MJ, Worley S, Lee J, Lanza DC: Resection of anterior skull base tumors: comparison of combined traditional and endoscopic techniques. Am J Rhinol 19:521-528, 2005. 3. Carrau RL, Kassam AB, Snyderman CH, Duvvuri U, Mintz A, Gardner P: Endoscopic transnasal anterior skull base resection for the treatment of sinonasal malignancies. Oper Tech Otolaryngol Head Neck Surg 17:102-110, 2006. 4. Eloy JA, Vivero RJ, Hoang K, Civantos FJ, Weed DT, Morcos JJ, Casiano RR: Comparison of transnasal endoscopic and open craniofacial resection for malignant tumors of the anterior skull base. Laryngoscope 119:834-840, 2009. 5. Ganly I, Patel SG, Singh B, Bridger PG, Cantu G, Cheesman A, De Sa G, Donald P, Fliss D, Gullane P, Janecka I, Kamata SE, Kowalski LP, Levine P, Medina LR, Pradhan S, Schramm V, Snyderman C, Wei WI, Shah JP: Complications of craniofacial resection for malignant tumors of the skull base: report of an International Collaborative Study. Head Neck 27:445-451, 2005. 6. Gil Z, Fliss DM, Cavel O, Shah JP, Kraus DH: Improvement in survival during the past 4 decades among patients with anterior skull base cancer. Head Neck 34:1212-1219, 2012. 7. Hadad G, Bassagasteguy L, Carrau RL, Mataza JC, Kassam A, Snyderman CH, Mintz A: A novel reconstructive technique after endoscopic expanded endonasal approaches: vascular pedicle nasoseptal flap. Laryngoscope 116:1882-1886, 2006. 8. Kassam A, Snyderman CH, Mintz A, Gardner P, Carrau RL: Expanded endonasal approach: the rostrocaudal axis. Part I: crista galli to the sella turcica. Neurosurg Focus 19:E3, 2005. 9. Komotar RJ, Starke RM, Raper DM, Anand VJ, Schwartz TH: Endoscopic endonasal compared with anterior craniofacial and combined cranionasal resection of esthesioneuroblastomas. World Neurosurg 80:148-159, 2013. 10. Ketcham S, Wilkins RH, Vanburen JM, Smith RR: A combined intracranial facial approach to the paranasal sinuses. Am J Surg 106:698-703, 1963. 11. Kraus DH, Shah JP, Arbit E, Galicich JH, Strong EW: Complications of craniofacial
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resection for tumors involving the anterior skull base. Head Neck 16:307-312, 1994. 12. Nicolai P, Castelnuovo P, Lombardi D, Battaglia P, Bignami M, Pianta L, Tomenzoli D: Role of endoscopic surgery in the management of selected malignant epithelial neoplasms of the nasoethmoidal complex. Head Neck 29:1075-1082, 2007. 13. Nicolai P, Castelnuovo P, Bolzoni Villaret A: Endoscopic resection of sinonasal malignancies. Curr Oncol Rep 13:138-144, 2011. 14. Patel SG, Singh B, Polluri A, Bridger PG, Cantu G, Cheesman AD, deSa GM, Donald P, Fliss D, Gullane P, Janecka I, Kamata SE, Kowalski LP, Kraus DH, Levine PA, dos Santos LR, Pradhan S, Schramm V, Snyderman C, Wei WI, Shah JP: Craniofacial surgery for malignant skull base tumors: report of an international collaborative study. Cancer 15:1179-1187, 2003. 15. Raza SM, Garzon-Muvdi T, Gallia GL, Tamargo RJ: Craniofacial resection of midline anterior skull base malignancies: a reassessment of outcomes in the modern era. World Neurosurg 25:1-9, 2012. 16. Stammberger H: Endoscopic endonasal surgery— concepts in treatment of recurring rhinosinusitis. Part II: surgical technique. Otolaryngol Head Neck Surg 94:147-156, 1986. 17. Suh JD, Ramakrishnan VR, Chi JJ, Palmer JN, Chiu AG: Outcomes and complications of endoscopic approaches for malignancies of the paranasal sinuses and anterior skull base. Ann Otol Rhinol Laryngol 122:54-59, 2013. 18. Thaler ER, Kotapka M, Lanza DC, Kennedy DW: Endoscopically assisted anterior cranial skull base resection of sinonasal tumors. Am J Rhinol 13: 303-310, 1999. 19. Yuen AP, Fung CF, Hung KN: Endoscopic cranionasal resection of anterior skull base tumor. Am J Otolaryngol 18:431-433, 1997. 20. Zanation AM, Carrau RL, Snyderman CH, Germanwala AV, Gardner PA, Prevedello DM, Kassam AB: Nasoseptal flap reconstruction of high flow intraoperative cerebral spinal fluid leaks during endoscopic skull base surgery. Am J Rhinol Allergy 23:518-521, 2009.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 18 September 2013; accepted 25 July 2014 Citation: World Neurosurg. (2014) 82, 6S:S59-S65. http://dx.doi.org/10.1016/j.wneu.2014.07.026 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
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