- Email: [email protected]
Endoscopic Endonasal Compared with Anterior Craniofacial and Combined Cranionasal Resection of Esthesioneuroblastomas
PEER-REVIEW REPORTS
Endoscopic Endonasal Compared with Anterior Craniofacial and Combined Cranionasal Resection of Esthesioneuroblastomas TUMOR
Ricardo J. Komotar1, Robert M. Starke2, Daniel M. S. Raper2 Vijay K. Anand3, Theodore H. Schwartz4
Key words Endonasal - Endoscopic - Esthesioneuroblastoma - Minimal access - Skull base - Surgery - Systematic review -
Abbreviations and Acronyms CFR: Craniofacial resection CN: Cranionasal CSF: Cerebrospinal fluid EE: Endoscopic endonasal RT: Radiotherapy From the 1Department of Neurological Surgery, University of Miami, Miami, Florida; 2 Department of Neurological Surgery, University of Virginia, Charlottesville, Virginia; and the Departments of 3 Otorhinolaryngology, and 4Neurological Surgery, Otorhinolaryngology, Neurology and Neuroscience, Weill Cornell Medical College, New York Presbyterian Hospital, New York, New York, USA To whom correspondence should be addressed: Daniel M. S. Raper, M.B.B.S. [E-mail: [email protected]] Citation: World Neurosurg. (2013) 80, 1/2:148-159. http://dx.doi.org/10.1016/j.wneu.2012.12.003 Journal homepage: www.WORLDNEUROSURGERY.org
- OBJECTIVE:
Esthesioneuroblastomas represent a surgical challenge because of their anatomical location, the necessity of achieving negative margins, and the often-cosmetically disfiguring transfacial approaches needed. Recently, expanded endonasal endoscopic approaches have been developed, either alone or in combination with a craniotomy. We conducted a systematic review of case series and case reports to compare outcomes between these various surgical approaches.
- METHODS:
A MEDLINE search was conducted of the modern literature (19852010) to identify open and endoscopic surgical series. Tumor and patient characteristics, Kadish stage, extent of resection, and progression-free and overall survival were recorded and analyzed by approach. Kaplan-Meier analysis was used to assess overall survival and progression-free survival.
- RESULTS:
Forty-seven studies comprising 453 patients were included. The endoscopic cohort had a greater proportion of Kadish Stage A tumors compared with the craniofacial group. Gross total resection was achieved in 98.1% of patients who underwent an endoscopic approach compared with 81.3% for the craniofacial and 100% for the cranionasal cohorts. Local recurrence occurred in 8.0% of patients in the endoscopic group compared with 22.1% in the craniofacial and 16.7% in the cranionasal cohorts.
- CONCLUSION:
In well-selected cases, cranionasal and endonasal approaches can be safe and effective. An ongoing evaluation of the benefits and limitations are necessary to better define the ideal patient population and patient-specific risk factors for the use of these minimal access techniques.
Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2013 Elsevier Inc. All rights reserved.
INTRODUCTION Esthesioneuroblastomas are rare, malignant tumors that arise from neurosecretory cells of the olfactory mucosa at the cribriform plate, upper third of the nasal septum, or superior turbinates (4). Despite advances in modern microsurgical techniques, the location of these lesions at the anterior cranial base often makes surgical resection challenging. The goal of esthesioneuroblastoma surgery is gross total resection with histologically negative margins. Adjuvant treatment with radiotherapy (RT), chemotherapy or both, often is used depending on the Kadish grade of the tumor (4, 18). In some circumstances neoadjuvant therapy is used (17, 18, 32, 33, 37, 42, 47, 48, 61, 62). Various surgical
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approaches are possible, with the traditional standard of care being anterior craniofacial surgery, a combined approach that incorporates lateral rhinotomy, maxillectomy, and/or sinusotomies, along with a bifrontal craniotomy (29, 47). For tumors confined to the nasal cavity or paranasal sinuses that have radiologic evidence of a normal cribriform plate and upper ethmoid sinuses, pure endonasal or transfacial approaches without craniotomy can be used to achieve negative margins (47). However, tumors with intracranial extension traditionally have required a bifrontal craniotomy with en-bloc resection of the tumor, surrounding dura, and the entire cribriform plate and crista galli (33, 47, 61). More recently, the lateral rhinotomy approach or combined craniofacial approach has been modified at certain centers, which now advocate either a purely
endonasal or combined cranionasal (CN) approach with the avoidance of a facial incision. In the endonasal approach, the entirety of the tumor is removed via an endonasal corridor (22, 43, 46, 48, 49, 51). The combined, or CN, approach incorporates endonasal endoscopic resection of accessible portions of the tumor from below with a bifrontal craniotomy for maximal resection of intracranial pathology. Philosophically, the endoscopic endonasal (EE) approach is suitable for all tumors, even those with intracranial extension, as long as the tumor does not extend lateral to the lamina papyracea. In this latter situation, a CN approach would be required, particularly if an orbital exenteration is indicated. Previous reports have indicated that, in combination with RT, endoscopic techniques may be effective in achieving local control even for
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2012.12.003
PEER-REVIEW REPORTS RICARDO J. KOMOTAR ET AL.
ENDOSCOPIC ENDONASAL ESTHESIONEUROBLASTOMA RESECTION
Table 1. Study Characteristics of Craniofacial Esthesioneuroblastoma Resection
Study Design
No. Pts
Male
Newbill et al., 1985 (45)
Retro
10
4
Meneses et al., 1990 (40)
Retro
3
0
Author and Year
Mean Age (years)
Previous Surgery
RT
CT
43
e
10
7
52
0
1
0
Schmidt et al., 1990 (60)
CR
1
0
54
0
0
10
Dulguerov and Calcaterra, 1992 (18)
Retro
19
9
40
e
1
0
Austin et al., 1996 (2)
Retro
6
5
43
0
1
0
Bilsky et al., 1997 (3)
Retro
4
e
e
e
e
e
Miyamoto et al., 2000 (41)
Retro
8
4
43
e
0
0
Resto et al., 2000 (57)
Retro
17
e
e
e
e
e
CR
1
0
66
0
0
0
Gondim et al., 2002 (24) Wei et al., 2002 (70)
CR
1
0
15
0
e
e
Argiris et al., 2003 (1)
Retro
13
6
40
e
4
3
Dias et al., 2003 (16)
Retro
19
e
e
e
0
0
Lund et al., 2003 (37)
Retro
42
28
46
5
7
1
Constantinidis et al., 2004 (11)
Retro
3
e
43
0
1
0
Diaz et al., 2005 (17)
Retro
30
19
47
e
1
0
Feiz-Erfan et al., 2005 (21) Loy et al., 2006 (35) Sampath et al., 2006 (59)
16
e
0
0
43.6
4
50
32
0
37
0
0
0
CR
1
0
Retro
50
26
CR
1
Kim et al., 2007 (28)
Retro
10
7
48
0
6
6
McLean et al., 2007 (39)
Retro
16
e
e
e
e
e
Nakao et al., 2007 (44)
Retro
6
4
49
0
0
3
Capelle and Krawitz, 2008 (6)
CR
1
e
e
0
0
0
Kim et al., 2008 (27)
Retro
10
5
41
e
0
0
Nichols et al., 2008 (46)
Retro
9
4
48
0
0
3
Zafereo et al., 2008 (73)
Retro
12
8
61
0
3
0
Nakamura et al., 2009 (43)
Retro
5
3
55
e
e
e
Smee et al., 2011 (62)
Retro
20
e
e
0
2
0
Pts, patients; RT, radiotherapy; CT, chemotherapy; NED, no evidence of disease; GTR, gross total resection; Retro, retrospective; CR, case report.
esthesioneuroblastomas with intracranial extension (Kadish Stage C) (22, 55, 67). The purpose of this investigation was to review the existing literature to compare the efficacy of craniofacial and transfacial with CN and pure endonasal surgery in the management of esthesioneuroblastoma. The goal was to assess whether the introduction of minimal-access, endonasal endoscopic techniques has compromised
outcomes compared with the previous standard of care (12, 22, 55, 67).
MATERIALS AND METHODS Study Selection and Data Extraction The methodology for our systematic review process has been described in detail in a previous report (30). In summary, we
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performed a modern literature search using the Ovid gateway of the MEDLINE database between the years of 1985 and 2010. The following keywords were queried singly and in combination: esthesioneuroblastoma, olfactory, neuroblastoma, resection, anterior, transfacial, craniofacial, cranionasal, transcranial, transnasal, open, endoscopic, outcome, skull base, surgery. The date of last search was December, 2010.
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Preoperative Treatment
PEER-REVIEW REPORTS RICARDO J. KOMOTAR ET AL.
ENDOSCOPIC ENDONASAL ESTHESIONEUROBLASTOMA RESECTION
Table 1. Continued Kadish Stage
Extent of Resection
Postoperative Treatment
Recurrence
TUMOR
A
B
C
GTR
Subtotal
RT
CT
Follow-up
Local
Regional
NED
1
4
5
e
e
0
0
38.9
0
1
7
0
0
2
3
0
2
1
e
0
2
2
0
0
1
1
0
1
0
e
1
0
0
8
5
4
e
e
11
1
e
7
1
6
0
0
6
e
e
4
1
65.0
0
4
3
e
e
e
4
0
e
e
e
1
e
e
0
2
6
e
e
6
2
e
3
1
3
e
e
e
10
7
9
5
66
2
1
13
0
0
1
1
0
1
0
12
0
0
1
0
0
1
1
0
e
e
24
0
0
1
2
2
9
11
2
6
0
e
8
3
6
e
e
e
18
1
19
e
e
8
5
15
4
7
31
e
e
16
1
57
7
e
25
0
2
1
e
e
1
0
62.3
2
1
1
1
10
19
23
1
23
3
88
4
4
e
e
e
e
1
0
e
e
e
e
e
0
4
14
32
e
e
e
e
93
4
8
33
0
0
1
1
0
1
0
e
0
0
1
0
0
7
e
e
7
2
e
2
2
7
e
e
e
16
0
e
e
e
e
e
e
1
1
4
e
e
4
0
e
4
1
3
e
e
e
1
0
e
e
20
e
1
0
0
0
10
e
e
7
1
28.8
e
e
3
0
3
6
4
5
9
4
56.2
2
2
7
0
6
6
10
2
e
e
84.7
2
1
9
e
e
e
4
1
e
e
e
e
e
e
e
e
e
e
e
17
2
e
6
e
16
Included studies were reviewed and carefully scrutinized for study design, methodology, patient characteristics, and primary findings. The anterior craniofacial cohort included lateral rhinotomy with medial maxillectomy, ethmoidectomy, frontal and sphenoid sinusotomies, and combined midfacial degloving; all cases included transfacial and craniotomy approaches. For studies with available information, gross
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total resection with negative margins was based on postoperative computed tomography or magnetic resonance imaging in seven papers, intraoperative surgeon’s assessment in 19 papers, and histological confirmation of clear margins in eight papers. Statistical Analysis Data from the individual studies were combined by cohort and then compared
by the use of c2 and Fisher exact tests as appropriate. Post hoc Bonferroni analysis was performed to increase stringency of significance and to account for repeated measures of analysis. Kaplan-Meier analysis was used to assess overall survival and tumor progression free survival. The log-rank test was used to assess differences in survival curves.
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2012.12.003
PEER-REVIEW REPORTS RICARDO J. KOMOTAR ET AL.
ENDOSCOPIC ENDONASAL ESTHESIONEUROBLASTOMA RESECTION
Table 2. Study Characteristics of Endonasal Esthesioneuroblastoma Resection
Author and Year
Study Design
No. Pts
Male
Mean Age (years)
Previous Surgery
RT
CT
Walch et al., 2000 (69)
Retro
3
0
43
e
e
e
Casiano et al., 2001 (7)
Retro
5
2
64
3
0
0
Cakmak et al., 2002 (5) Liu et al., 2003 (34) Pasquini et al., 2003 (51) Constantinidis et al., 2004 (11) Roh et al., 2004 (57)
CR
1
0
12
0
0
0
Retro
1
1
74
1
0
0
CR
1
1
72
0
0
0
Retro
6
e
56
0
0
0
CR
1
0
40
0
0
0
Poetker et al., 2005 (55)
Retro
5
e
55
e
e
e
Unger et al., 2005 (67)
Retro
14
6
49
2
0
e
Castelnuovo et al., 2006 (8)
Retro
10
3
56.2
1
0
0
Dave et al., 2007 (12)
Retro
10
7
61.2
e
e
e
McLean et al., 2007 (39)
Retro
3
e
e
e
e
e
67
e
0
0
51.5
e
e
e
CR
1
0
Suriano et al., 2007 (65)
Podboj and Smid, 2007 (54)
Retro
9
e
Nichols et al., 2008 (46)
Retro
1
1
11
0
0
0
Zafereo et al., 2008 (74)
Retro
3
1
57
0
0
0
CR
1
1
79
0
0
0
Dehdashti et al., 2009 (13)
Retro
4
4
43
e
e
e
Folbe et al., 2009 (22)
Retro
23
16
57
4
0
0
Chan et al., 2009 (10)
Pts, patients; RT, radiotherapy; CT, chemotherapy; NED, no evidence of disease; GTR, gross total resection; Retro, retrospective; CR, case report.
RESULTS Study Selection A total of 99 published studies were identified through our initial MEDLINE database search. After careful scrutiny of these studies, 52 were rejected from our review because they did not include original data, were purely anatomical studies, did not report outcomes, did not differentiate endoscopic outcomes from a cohort that included a mixture of approaches, or repeated data reported elsewhere. Twenty-seven studies reported outcomes from craniofacial resection (CFR) or transfacial resection, 19 studies reported outcomes for endonasal approaches, and 10 studies reported outcomes for CN approaches. A total of 47 studies and 453 patients were included in this review. Study Characteristics Characteristics and primary findings of the 27 studies involving CFR are summarized in
Table 1. Regarding study design, 21 papers were retrospective (1-3, 11, 16, 17, 19, 27, 28, 35, 37, 39-41, 43-46, 57, 62, 74), and there were six case reports (6, 21, 23, 59, 60, 70). Characteristics and primary findings of the 19 studies involving endonasal resection are summarized in Table 2. Regarding study design, 14 papers were retrospective (7, 8, 11-13, 22, 34, 39, 46, 55, 65, 67, 69, 74), and there were five case reports (5, 10, 51, 54, 58). Characteristics and primary findings of the nine studies involving CN resection are summarized in Table 3. There were six retrospective series (11, 15, 27, 34, 72, 74) and three case reports (26, 49, 68). There were no randomized controlled trials. Patient Characteristics Patient characteristics for each cohort are reported in Table 4. There were 318 patients in the CFR cohort, 102 patients in the EE cohort, and 33 patients in the
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CN cohort. Regarding presenting symptoms, there were no differences between endonasal and craniofacial approaches. Compared with the CN cohort, patients treated via an endonasal approach had a lower incidence of epistaxis (P ¼ 0.05), olfactory dysfunction (P ¼ 0.01), and facial/sinus pain (P < 0.003). Compared with the craniofacial approach, patients in the CN group had a greater incidence of olfactory dysfunction (P < 0.003). Regarding tumor stage, compared with the CFR group, the EE group had a greater proportion of Kadish Stage A (P ¼ 0.003) and Kadish Stage B (P < 0.003), and a lower incidence of Kadish Stage C (P < 0.003) tumors. The endoscopic group had a greater proportion of Kadish Stage B tumors than the CN group (P ¼ 0.02), but no differences in the incidence of other tumor stages (Figure 1). There were no differences between the CN and CFR groups. Patients in the CFR group had
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ENDOSCOPIC ENDONASAL ESTHESIONEUROBLASTOMA RESECTION
Table 2. Continued Kadish Stage
TUMOR
A
B
Extent of Resection C
GTR
Subtotal
Postoperative Treatment RT
CT
Recurrence Follow-up
Local
Regional
NED
0
2
1
3
0
0
0
58.3
0
0
3
1
3
0
5
0
5
e
31
e
2
4
e
e
e
1
0
1
e
24
e
e
0
0
1
0
1
0
e
e
30
0
0
1
e
e
e
1
0
e
e
58
0
0
1
1
4
1
e
e
4
0
125.2
0
0
4
e
e
e
1
0
1
0
7
0
0
1
1
2
2
e
e
4
2
74.8
2
e
5
0
5
9
e
e
e
e
59.8
3
e
e
3
5
2
10
0
9
1
38.1
0
0
10
5
2
2
10
0
e
e
40.5
0
1
e
e
e
e
3
0
e
e
e
e
e
e
e
e
e
1
0
0
e
88
0
0
1
3
6
0
9
0
9
0
42.8
0
0
9
0
0
1
0
0
1
0
23
0
e
1
2
1
0
3
0
e
e
67.3
1
0
3
1
0
0
1
0
1
0
16
e
e
1
e
e
e
4
0
e
e
e
e
e
e
2
11
5
e
e
16
e
45.2
1
e
1
a lower rate of previous surgery than the endoscopic group (P ¼ 0.02) and greater rates of preoperative RT (P < 0.003) and preoperative chemotherapy (P < 0.003). The CN cohort had greater rates of preoperative RT (P ¼ 0.03) and computed tomography (P < 0.003) than the endoscopic group. The CN group had a lower rate of preoperative RT than the CFR group (P ¼ 0.03). There were no other significant differences in presenting or tumor characteristics between the groups. Outcomes and Complications Outcomes and complications for each cohort are reported in Tables 5 and 6. Extent of Resection In the CFR cohort, gross total resection was reported in 16 studies and achieved in 81.3% of patients (109/134); subtotal resection (>80%-90%) was achieved in 14.2% of patients (19/134); and partial
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resection not reported in any cases. Negative margins reported in 11 studies and were achieved in 85 of 110 cases (77.3%). In the EE cohort, gross total resection was reported in 15 studies and achieved in 98.1% of patients (53/54); subtotal resection was achieved in no case; and partial resection was achieved in 1.9% of patients (1/54). Negative margins were reported in 14 studies and achieved in 75 of 80 cases (93.8%). In the CN cohort, gross total resection was reported in 6 studies and achieved in all patients (12 of 12). Negative margins were reported in eight studies and achieved in 23 of 24 cases (95.8%; Figure 2). Postoperative Complications In the CFR cohort, the most common postoperative complications included cerebrospinal fluid (CSF) leak in 11 of 182 cases (6.0%), epidural hematoma in 3 of 54 cases (5.6%), epiphora in 7 of 132 cases (5.3%) and bone flap infection in 9 of 176
cases (5.1%). Meningitis occurred in 4 of 89 cases (4.5%). In the EE group, persistent nasal crusting was reported in 44 of 65 cases (67.7%) in seven studies, and epistaxis occurred in 2/11 cases (18.2%) in three studies. CSF leak was reported in 5 of 69 cases (7.2%) in nine studies and epidural abscess occurred in 1 of 24 cases in two studies (4.2%). In the CN group, CSF leak occurred in 18.2% of cases (2/11) in four studies. Postoperative venous thromboembolus occurred in one case in four studies (9.2%). No other postoperative complications were reported in the endoscopic or CN cohorts. Perioperative mortality occurred in 4 of 124 cases (3.2%) in 12 studies in the CFR group and in no cases in five studies in the EE group or in five studies in the CN group (Figure 3). Outcomes and Recurrence In the CFR group, mean follow-up was 71.0 months. Local recurrence was reported in 22 studies and occurred in 63 of
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PEER-REVIEW REPORTS RICARDO J. KOMOTAR ET AL.
ENDOSCOPIC ENDONASAL ESTHESIONEUROBLASTOMA RESECTION
Table 3. Study Characteristics of Cranionasal Esthesioneuroblastoma Resection
Author and Year Devaiah et al., 2003 (15) Kenmochi et al., 2003 (26)
Study Design
No. Pts
Male
Mean Age (years)
Previous Surgery
RT
CT
Retro
7
4
47
e
1
1
CR
1
0
44
0
0
0
Liu et al., 2003 (34)
Retro
2
1
47
0
1
2
Constantinidis et al., 2004 (11)
Retro
5
e
45
0
0
0
Yuen et al., 2005 (72)
Retro
6
4
51
0
1
0
Vergani et al., 2007 (68) Kim et al., 2008 (27) Park et al., 2008 (49) Zafereo et al., 2008 (74)
CR
1
1
36
0
e
e
Retro
9
3
48
e
0
8
CR
1
0
69
0
0
0
Retro
1
1
70
0
0
0
Pts, patients; RT, radiotherapy; CT, chemotherapy; NED, no evidence of disease; GTR, gross total resection; Retro, retrospective; CR, case report.
285 cases (22.1%). Tumor progression-free survival was reported in nine studies. Regional metastasis was reported in 20 studies and occurred in 38 of 220 cases (17.3%). The mean time to regional metastasis was 50.7 months (range, 1496.1 months) and was reported in 11 studies. Among patients who were alive at last follow-up in 23 studies, 163 of 263 (61.9%) were reported to be free of disease. In the EE group, mean follow-up was 52.0 months. Local recurrence was reported in 14 studies and occurred in 7 of 88 cases (8.0%). Regional metastasis was reported in 14 studies and occurred in 3 of 50 cases (6.0%). The mean time to regional metastasis was not reported in any studies included in this review. Among patients who were alive at last follow-up in 15 studies, 45 of 71 (63.4%) were reported to be free of disease. In the CN group, mean follow-up was 43.1 months. Local recurrence was reported in seven studies and occurred in 3 of 18 cases (16.7%). Regional metastasis was reported in eight studies and occurred in 2 of 24 cases (8.3%). The mean time to regional metastasis was 40.0 months (range, 2-78.0 months) and was reported in two studies. Among patients who were alive at last follow-up in nine studies, 27 of 33 (81.8%) were reported to be free of disease. Tumor progression-free and overall survival for the combined cohorts are shown in Figures 4 and 5. The 1-, 3-, 5-, and 10-year progression-free survival rates
were 91.6%, 79.4%, 73.7%, and 60.5% respectively (Figure 4). The 1-, 3-, 5-, and 10-year overall survival rates were 92.2%, 83.4%, 81.5%, and 65.7%, respectively (Figures 5, 6, and 7). DISCUSSION Esthesioneuroblastomas are rare malignant neuroectodermal tumors that account for approximately 2% of all sinonasal tract neoplasms, with an incidence of approximately 0.4 per million population (66). The optimal goal of treatment is the achievement of gross total resection with negative margins followed by either RT, chemotherapy or both, depending on the extent of disease (4, 18). Using the gold standard of a CFR approach to achieve enbloc resection with negative margins (36, 53, 56, 71), multicenter international collaborative studies report 5-year overall survival rates between 60% and 90% and 10-year survival of 40%-80% (8, 16, 17, 19, 48, 57). In recent years, endonasal endoscopic approaches have been investigated as either a primary or adjuvant surgical approach to remove esthesioneuroblastomas, as well as a variety of other pathologies of the anterior skull base (14, 20). The advantage of this technique is that it avoids a facial incision and, in some circumstances, may also avoid a craniotomy via a more direct, anterior approach to the pathology. The endoscope also moves the lens and light source
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significantly closer to the tumor than conventional operative microscopy, providing superior visibility, with the ability to look around corners with the use of angled endoscopes. For tumor that extends lateral to the lamina papyracea, the endonasal approach can be combined with a craniotomy, also known as the “cranionasal” approach (15, 34). However, it is unclear whether the use of endonasal endoscopy results in compromised outcome with respect to extent of resection and the ability to achieve negative margins because, often, tumors cannot be removed en bloc. Likewise, the use of a purely endonasal approach to remove intracranial pathology risks a significant CSF leak since a pericranial flap, the mainstay of skull base closure, cannot be harvested, although a vascularized nasoseptal flap may be used as an alternative (21). Anterior Craniofacial and Combined CN Approaches Complete tumor resection, using a transfacial and/or bifrontal craniotomy (anterior craniofacial) approach, combined with postoperative RT, has traditionally been considered the “gold standard” treatment for esthesioneuroblastomas (4, 18, 45). Craniofacial approaches facilitate complete resection of bulky disease with significant intracranial extension (62). A number of series have demonstrated high rates of gross total resection with 5-year overall survival rates between 60% and
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Table 3. Continued Kadish Stage
Postoperative Treatment
Extent of Resection
TUMOR
A
B
C
GTR
Subtotal
RT
CT
3
1
3
e
e
5
0
0
0
1
1
0
1
0
0
0
2
2
0
e
e
0
3
2
e
e
4
0
3
2
1
6
0
1
0
0
1
1
0
1
1
7
e
e
0
0
1
1
0
0
0
0
1
1
0
e
90% and 10-year survival of 40%-80% (8, 16, 17, 19, 57). En-bloc resection, although conceptually appealing, is not always possible using a craniofacial approach, and piecemeal craniofacial surgery has been shown to provide equivalent survival outcomes to en bloc resection (38). Anterior craniofacial approaches are associated with a number of disadvantages,
Recurrence Follow-up
Local
Regional
NED
62.3
1
1
6
0
0
1
12.5
0
0
2
75.4
2
0
3
0
32.8
e
1
4
e
e
12
0
0
1
9
1
20.8
e
e
8
1
e
0
0
1
e
14
0
0
1
132
including scarring with lateral rhinotomy, limited superior access when the midface degloving approach is used, and limited access to the sphenoid sinus and frontal recess with the craniofacial approach (42, 55). Overall, postoperative morbidity has been reported to be approximately 35%, with mortality of 2%-5% (74). Furthermore, surgery alone is insufficient in controlling
esthesioneuroblastomas and would be recommended by most teams as the sole treatment strategy only in Kadish A tumors (37, 74). After the emergence of endoscopic techniques for removal of nasal and sinus neoplasia, combined endonasal and craniotomy approaches for esthesioneuroblastoma were reported in the late 1990s
Table 4. Patient and Tumor Characteristics in Craniofacial, Endonasal and Cranionasal Esthesioneuroblastoma Resection Craniofacial
P Value (CFR vs. EE)
Endonasal
P Value (EE vs. CN)
Cranionasal
P Value (CN vs. CFR)
Patient characteristics Total patients Mean age (range) Male (%)
318 45.3 (6-85)
102
33
54.5 (11-81)
48.5 (28-72)
132/238 (55.5)
1.00
43/79 (54.4)
1.00
14/28 (50.0)
1.00
120/157 (76.4)
0.90
53/64 (82.8)
1.00
9/12 (75.0)
1.00
Presenting symptoms Nasal obstruction (%) Epistaxis (%)
69/157 (43.9)
0.18
19/63 (30.2)
0.05*
8/12 (66.7)
0.38
Nasal discharge (%)
17/157 (10.8)
1.00
6/57 (10.5)
1.00
2/10 (20.0)
1.00
Olfactory dysfunction (%)
19/157 (12.1)
1.00
7/62 (11.3)
0.01*
5/10 (50.0)
<0.003*
Facial/sinus pain (%)
11/157 (7.0)
0.10
0/63 (0.0)
<0.003*
3/12 (25.0)
0.08
Tumor stage Kadish A
21/233 (9.0)
0.003*
19/85 (22.4)
1.00
7/33 (21.2)
0.10
Kadish B
56/233 (24.0)
<0.003*
42/85 (49.4)
0.02*
7/33 (21.2)
1.00
Kadish C
153/233 (65.7)
<0.003*
23/85 (27.1)
0.99
19/33 (57.6)
1.00
Kadish D Previous surgery (%)
3/233 (1.3)
1.00
1/85 (1.2)
1.00
0/33 (0.0)
1.00
9/166 (5.4)
0.02*
11/67 (16.4)
0.22
0/17 (0.0)
0.98
CFR, craniofacial resection; EE, endoscopic endonasal; CN, cranionasal. *Statistically significant.
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esthesioneuroblastomas confirmed satisfactory rates of complete excision without local recurrence (72). Kim et al. (27) found the CN approach to be equivalent to traditional CFR in their series of sinonasal tumors, and Devaiah et al. (15) demonstrated complete tumor control in their series, arguing that craniotomy provided more accurate resection of anterior cranial fossa disease than radiosurgery.
Figure 1. Kadish stage of each approach.
Endoscopic Endonasal Approach A purely EE approach for resection of esthesioneuroblastomas is a natural extension of the philosophy underlying the
and early 2000s. Yuen and colleagues first described this approach in 1997 (73), and their subsequent experience with a series of
combined CN approach and has been increasingly reported during the past 10 years. Unger et al. (67) used a combination of endoscopic surgery with radiosurgery to target intracranial extension and achieved complete tumor control at a follow- up of 58 months. However, four patients in this series (29%) required a second radiosurgical procedure. Stammberger et al. (64) and Walch et al. (69) likewise reported early series of patients treated with combined endoscopic and radiosurgical treatment. Most of these early cases did not breach the dura. Casiano et al. (7) described the first instance of an endoscopic en-bloc resection
Table 5. Outcomes and Complications in Craniofacial, Endonasal, and Cranionasal Esthesioneuroblastoma Resection Craniofacial
No. Studies
Occurrence/ Total Pts
Gross total
16
109/128
Subtotal
16
19/128
Partial
16
0/128
Negative margins
11
Positive margins
11
Neoadjuvant RT
Endonasal
Cranionasal
No. Studies
Occurrence/ Total Pts
%
No. Studies
Occurrence/ Total Pts
85.2
15
53/54
98.1
6
12/12
14.8
15
0/54
0.0
6
0/12
0.0
0
15
1/54
1.9
6
0/12
0.0
85/110
77.3
14
75/80
93.8
8
23/24
95.8
25/110
22.7
14
5/80
6.2
8
1/24
4.2
22
87/275
31.6
13
0/68
0.0
8
3/32
9.4
Neoadjuvant CT
22
56/275
20.4
12
0/54
0.0
8
11/32
34.4
Adjuvant RT
19
144/211
68.2
12
51/66
77.3
6
20/29
69.0
Adjuvant CT
19
23/211
10.9
8
3/36
8.3
6
2/29
6.9
Nasal crusting
5
2/51
3.9
7
46/65
70.8
1
0/2
0.0
Epistaxis
4
0/24
0.0
3
2/11
18.2
2
0/3
0.0
Epidural hematoma
5
3/54
5.6
1
0/1
0.0
3
0/4
0.0
Bone flap infection
11
9/176
5.1
1
0/1
0.0
3
0/4
0.0
Epidural abscess
9
3/134
2.2
2
1/24
4.2
3
0/4
0.0
DVT/PE
9
3/144
2.1
1
0/1
0.0
4
1/11
9.2
Meningitis
9
4/89
4.5
2
0/24
0.0
3
0/4
0.0
CSF leak
12
11/182
6.0
9
5/69
7.2
4
2/11
18.2
Anosmia
3
1/21
4.8
1
0/10
0.0
1
0/1
0.0
Seizure
7
3/97
3.1
1
0/1
0.0
2
0/3
0.0
6
7/132
5.3
1
0/1
0.0
2
0/3
0.0
12
4/124
3.2
5
0/24
0.0
5
0/6
0.0
%
%
Extent of resection 100
Adjuvant therapy
Complications
Epiphora Perioperative mortality Follow-up (months)
71.0 (12-93)
52.0 (7-125)
43.1 (12-132)
RT, radiotherapy; CT, chemotherapy; DVT, deep-vein thrombosis; PE, pulmonary embolism; CSF, cerebrospinal fluid.
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Table 6. Outcomes and Recurrence in Craniofacial, Endonasal, and Cranionasal Esthesioneuroblastoma Resection Craniofacial
Endonasal
Cranionasal
TUMOR
No. Studies
Occurrence/ Total Pts
%
No. Studies
Occurrence/ Total Pts
%
No. Studies
Occurrence/ Total Pts
%
22
63/285
22.1
14
7/88
8.0
7
3/18
16.7
Recurrence Local recurrence Time to local recurrence Regional metastasis
42.2 (12.6-70.8) 20
38/220
Time to metastasis NED at last follow-up
17.3
33.0 (14.5-43.7) 14
3/50
50.7 (14-96.1) 23
162/263
59.0 6.0
8
NR 61.6
15
45/71
2/24
8.3
40.0 (2-78) 63.4
9
27/33
81.8
Pts, patients; NR, not reported; NED, no evidence of disease.
of an esthesioneuroblastoma invading the dura and crista galli, via the use of a purely endoscopic approach. Castelnuovo et al. (8) found en-bloc resection to be feasible only for small tumors, but were able to achieve complete resection in all tumors without gross brain invasion. Dave et al. (12) cautioned that obtaining clear surgical margins is essential; if, during endoscopic surgery, areas of tumor extension beyond the surgical field are observed, conversion to a combined CN procedure has been considered essential (8, 12). The necessity of achieving resection with negative surgical margins is underscored by a 1307patient analysis of malignant skull base tumors, which demonstrated that survival was halved and recurrence doubled with positive surgical margins (52). Despite the necessity of removing tumor piecemeal, rather than en bloc, adherence to oncologic principles of tumor resection is still possible using endoscopic approaches (63) Folbe et al. (22) demonstrated that Kadish Stage C tumors could be completely excised through a purely EE approach.
Figure 2. Extent of resection for each approach.
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In older series of esthesioneuroblastomas that include tumors with significant intracranial involvement, postoperative CSF leak rates can occur in up to 29% (22, 55). Although postoperative CSF leak is still a major limitation to the widespread adoption of endoscopic techniques, methods of reconstruction of the dural defect have significantly improved, even over the short time that these approaches have been used (25, 31, 50). More recent series of endoscopically treated anterior skull base lesions report CSF leak rates of 0%-4% using more complex, multilayer reconstruction techniques (9, 22) and is echoed in our own experience (T. H. Schwartz, unpublished data, May 2011). One such technique, the multilayer “gasket seal” closure with an additional nasoseptal pedicled flap, has been used with zero incidence of CSF leak in a variety of anterior cranial base surgery (31). Overall and progression-free survival rates for endonasal surgery are as good or better than other reported survival
Figure 3. Complication rates for each approach.
analyses following esthesioneuroblastoma resection in the literature (14, 16, 35). In an analysis of 36 patients treated at a single institution, Dias et al. (16) demonstrated significantly greater progression-free survival among patients treated with CFR and RT, compared with limited transcranial resection and RT, or RT alone. A meta-analysis of the literature undertaken by Devaiah et al. in 2009, showed a significantly greater overall survival in patients treated with either an endoscopic or endoscope-assisted approach compared with open approaches (14). The role of surgery for esthesioneuroblastomas must be placed in the wider context of treatment for these difficult tumors, which may include adjuvant or neoadjuvant treatment with RT, radiosurgery, or chemotherapy (17, 18, 32, 33, 37, 42, 48, 61, 62). Neoadjuvant therapy
Figure 4. Tumor progression-free survival for patients with esthesioneuroblastoma. Kaplan-Meier survival analysis for the combined cohort of patients treated with either craniofacial, endoscopic, or CN approaches.
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Figure 5. Overall survival for patients with esthesioneuroblastoma. Kaplan-Meier survival analysis for the combined cohort of patients treated with either craniofacial, endonasal, or CN approaches.
has the potential to increase survival after incomplete or complete resection of esthesioneuroblastomas (11, 27, 39, 48, 65, 67). Radiation is generally accepted as providing an additional benefit to surgery alone (29, 57), although it has not been used in all cases in which a complete resection was achieved without an obvious decrease in survival (55, 58). Chemotherapy has a less well-established role and has found the most use in patients with incompletely resected tumors or for salvage therapy (29, 62). Newer technologies, such as intensity-modulated radiation therapy, have also been used with comparable 5-year disease-free and overall survival to traditional combined modality therapies after CFR (39). Adjuvant treatments are as essential after endoscopic surgery as for any other approach for esthesioneuroblastomas, and are widely used for most patients in order to prevent
Figure 6. Tumor progression-free survival for patients with esthesioneuroblastoma by surgical approach. Kaplan-Meier survival analysis of progression-free survival for the endonasal, craniofacial, and CN approaches.
ENDOSCOPIC ENDONASAL ESTHESIONEUROBLASTOMA RESECTION
Figure 7. Overall survival for patients with esthesioneuroblastoma by surgical approach. Kaplan-Meier survival analysis of overall survival for the endonasal, craniofacial, and CN approaches.
recurrence and increase progression-free survival, except perhaps for patients with Kadish Grade A tumors that are completely excised at operation (37). Unfortunately we were not able to include analysis of the effect of neoadjuvant treatment on outcomes following esthesioneuroblastoma resection due to inconsistency of reporting in primary studies. Further work is necessary to identify which esthesioneuroblastomas benefit from routine neoadjuvant therapy, and which may safely be observed, with adjuvant treatments reserved for relapse. Because of significant differences in the patient populations in the CFR, EE, and CN cohorts in this study, it is not possible to draw direct comparisons of outcomes, complications, or survival between the groups. Specifically, there were a greater proportion of lower-grade tumors, and a lower proportion of higher-grade tumors in the endoscopic cohort compared with the craniofacial cohort. To delineate the effect of Kadish grade on extent of resection and recurrence, we performed a Mann-Whitney U statistical analysis. This analysis demonstrated that there was no significant association between Kadish grade and extent of resection except for Kadish grade C tumors in the comparison between craniofacial and CN groups. There were no statistically significant differences between the surgical approaches with regard to other Kadish grades for extent of resection or with regard to any Kadish grade for recurrence. These analyses were limited by the number of individual patients with information stratified by Kadish grade for both resection and recurrence. An additional
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limitation is that further information regarding time dependent variables, such as time to recurrence, was not available. Despite these limitations, the literature does permit some overall observations about the suitability of different lesions for each approach. Esthesioneuroblastomas require an individualized approach to treatment. Endoscopic approaches have been more commonly used, and are likely best suited to, tumors with smaller volume, no or minimal intracranial extension and lower Kadish staging (Kadish A or B). In contrast, craniofacial or combined CN approaches may be more useful for larger, more extensive or higher grade tumors. For lesions extending lateral to the lamina papyracea, a craniotomy should be incorporated either in combination with a transfacial or endoscopic approach. The status of any previous surgical intervention may affect the choice of approach, with more aggressive approaches more likely to be used at the first intervention, followed by less-invasive approaches for recurrence. It is important to note that, though most esthesioneuroblastomas tend to recur within 5 years of initial treatment (4), recurrence continues to occur over time (32). Ongoing surveillance and multidisciplinary involvement are essential to improving long-term outcomes for these rare and difficult tumors. CONCLUSION The introduction of endoscopy for the treatment of esthesioneuroblastomas, in either a purely endonasal or combined CN approach, does not result in worse outcome with respect to extent of resection, negative margins, progression-free or overall survival rates compared with more traditional craniofacial approaches in tumors for which this approach is suitable. Careful selection of cases in the literature has likely contributed to these good reported outcomes. Nevertheless, the increased visibility afforded by the endoscope may provide an advantage for the resection of small, low-grade esthesioneuroblastomas compared with more traditional transfacial approaches. Indeed, outcomes are improved, which may either reflect careful selection of smaller tumors for the endonasal approach or increased visibility provided
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by the endoscope. Moreover, complication rates, particularly CSF leak, are not greater and may indeed be lower. Patients treated via the endonasal approach in the literature have smaller, lower-grade tumors, which may have significantly affected their observed outcomes. Nevertheless, for tumors with intracranial extension limited to the area between the lamina papyracea, a purely endonasal endoscopic approach may offer a safe and effective, minimal access surgical option. Ongoing evaluation of the benefits and limitations are necessary to better define the ideal patient population and patient-specific risk factors for the use of these minimal access techniques. REFERENCES 1. Argiris A, Dutra J, Tseke P, Haines K: Esthesioneuroblastoma: the Northwestern University Experience. Laryngoscope 113:155-160, 2003. 2. Austin JR, Cebrun H, Kershisnik MM, ElNaggar AK, Garden AS, DeMonte F, Ginsberg LE, Lippman SM, Goepfert H: Olfactory neuroblastoma and neuroendocrine carcinoma of the anterior skull base: treatment results at the M.D. Anderson Cancer Center. Skull Base Surg 6:1-8, 1996. 3. Bilsky MH, Kraus DH, Strong EW, Harrison LB, Gutin PH, Shah JP: Extended anterior craniofacial resection for intracranial extension of malignant tumors. Am J Surg 174:565-568, 1997. 4. Bragg TM, Scianna J, Kassam A, Emami B, Brown HG, Hacein-Bey L, Clark JI, Muzaffar K, Boulis N, Prabhu VC: Clinicopathological review: esthesioneuroblastoma. Neurosurgery 64:764-770, 2009. 5. Cakmak O, Ergin NT, Yilmazer C, Kayaselcuk F, Barutcu O: Endoscopic removal of esthesioneuroblastoma. Int J Pediatr Otolaryngol 64:233-238, 2002. 6. Capelle L, Krawitz H: Esthesioneuroblastoma: a case report of diffuse subdural recurrence and review of recently published studies. J Med Imaging Radiation Oncol 52:85-90, 2008. 7. Casiano RR, Numa WA, Falquez AM: Endoscopic resection of esthesioneuroblastoma. Am J Rhinology 15:271-279, 2001. 8. Castelnuovo PG, Delu G, Sberze F, Pistochini A, Cambria C, Battaglia P, Bignami M: Esthesioneuroblastoma: endonasal endoscopic treatment. Skull Base 16:25-29, 2006. 9. Cavallo LM, Prevedello D, Esposito F, Laws ER Jr, Dusick JR, Messina A, Jane JA Jr, Kelly DF, Cappabianca P: The role of the endoscope in the transsphenoidal management of cystic lesions of the sellar region. Neurosurg Rev 31:55-64, 2008. 10. Chan LP, Wang LF, Tai CF, Wu CC, Kuo WR: Huge sphenoid sinus olfactory neuroblastoma: a case report. Kaohsiung J Med Sci 25:87-92, 2009.
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53. Plinkert PK, Zenner HP: Transfacial approach, craniofacial resection and midface degloving in surgery of malignant tumors of the anterior cranial base and adjacent paranasal sinuses. HNO 44: 192-200, 1996.
67. Unger F, Haselberger K, Walch C, Stammberger H, Papaefthymiou G: Combined endoscopic surgery and radiosurgery as treatment modality for olfactory neuroblastoma (esthesioneuroblastoma). Acta Neurochir (Wien) 147: 595-602, 2005.
41. Miyamoto RC, Gleich LL, Biddinger PW, Gluckman JL: Esthesioneuroblastoma and sinonasal undifferentiated carcinoma: impact of histological grading and clinical staging on survival and prognosis. Laryngoscope 110:1262-1265, 2000. 42. Nabili V, Kelly DF, Fatemi N, St. John M, Calcaterra TC, Abemayor E: Transnasal, transfacial, anterior skull base resection of olfactory neuroblastoma. Am J Otolaryngol 32:279-285, 2011. 43. Nakamura M, Stover T, Rodt T, Majdani O, Lorenz M, Lenarz T, Krauss JK: Neuronavigational guidance in craniofacial approaches for large (para)nasal tumors involving the anterior skull base and upper clival lesions. Eur J Surg Oncol 35: 666-672, 2009. 44. Nakao K, Watanabe K, Fujishiro Y, Ebihara Y, Asakage T, Goto A, Kawahara N: Olfactory neuroblastoma: long-term clinical outcome at a single institute between 1979 and 2003. Acta Oto-Laryngol 127:113-117, 2007. 45. Newbill ET, Johns ME, Cantrell RW: Esthesioneuroblastoma: diagnosis and management. Southern Med J 78:275-282, 1985. 46. Nichols AC, Chan AW, Curry WT, Barker FG II, Deschler DG, Lin DT: Esthesioneuroblastoma: the Massachusetts Eye and Ear Infirmary and Massachusetts General Hospital experience with craniofacial resection, proton beam radiation, and chemotherapy. Skull Base 18:327-337, 2008. 47. Oskouian RJ Jr, Jane JA Sr, Dumont AS, Sheehan JM, Laurent JJ, Levine PA: Esthesioneuroblastoma: clinical presentation, radiological, and pathological features, treatment, review of the literature, and the University of Virginia experience. Neurosurg Focus 12(5), 2002; Article 4. 48. Ozsahin M, Gruber G, Olszyk O, KarakoyunCelik O, Pehlivan B, Azria D, Roelandts M, Kaanders JH, Cengiz M, Krengli M, Matzinger O, Zouhair A: Outcome and prognostic factors in olfactory neuroblastoma: a rare cancer network study. Int J Radiation Oncology Biol Phys 78: 992-997, 2010. 49. Park KJ, Kang SH, Lee HG, Chung YG: Olfactory neuroblastoma following treatment for pituitary adenoma. J Neurooncol 90:237-241, 2008.
54. Podboj J, Smid L: Endoscopic surgery with curative intent for malignant tumors of the nose and paranasal sinuses. Eur J Surg Oncol 33:1081-1086, 2007. 55. Poetker DM, Toohill RJ, Loehrl TA, Smith TL: Endoscopic management of sinonasal tumors: A preliminary report. Am J Rhinology 19:307-315, 2005. 56. Raveh J, Turk JB, Ladrach K, Seiler R, Goday N, Chen J, Paladino J, Virag M, Leibinger K: Extended anterior subcranial approach for skull base tumors: long-term results. J Neurosurg 82: 1002-1010, 1995. 57. Resto VA, Eisele DW, Forastiere A, Zahurak M, Lee DJ, Westra WH: Esthesioneuroblastoma: the Johns Hopkins experience. Head Neck 22:550-558, 2000. 58. Roh HJ, Batra PS, Citardi MJ, Lee J, Bolger WE, Lanza DC: Endoscopic resection of sinonasal malignancies: a preliminary report. Am J Rhinol 18:239-246, 2004. 59. Sampath P, Park MC, Huang D, Deville C, Cortez S, Chougule P: Esthesioneuroblastoma (olfactory neuroblastoma) with hemorrhage: an unusual presentation. Skull Base 16:169-174, 2006. 60. Schmidt JL, Zarbo RJ, Clark JL: Olfactory neuroblastoma: clinicopathologic and immunohistochemical characterization of four representative cases. Laryngoscope 100:1052-1058, 1990. 61. Shah JP, Kraus DH, Bilsky MH, Gutin PH, Harrison LH, Strong EW: Craniofacial resection for malignant tumors involving the anterior skull base. Arch Otolaryngol Head Neck Surg 123: 1312-1317, 1997. 62. Smee RI, Broadley K, Williams JR, Meagher NS, Bridger GP: Retained role of surgery for olfactory neuroblastoma. Head Neck 33:1486-1492, 2011.
50. Patel MR, Shah RN, Snyderman CH, Carrau RL, Germanwalla AV, Kassam AB, Zanation AM: Pericranial flap for endoscopic anterior skull-base reconstruction: clinical outcomes and radioanatomic analysis of preoperative planning. Neurosurgery 66:506-512, 2010.
63. Snyderman CH, Carrau RL, Kassam AB, Zanation A, Prevedello D, Gardner P, Mintz A: Endoscopic skull base surgery: principles of endonasal oncological surgery. J Surg Oncol 97: 658-664, 2008.
51. Pasquini E, Sciarretta V, Compadretti GC, Cantaroni C: A case report of inverted papilloma associated with esthesioneuroblastoma treated by
64. Stammberger H, Anderhuber W, Walch C, Papaefthymiou G: Possibilities and limitations of endoscopic management of nasal and paranasal
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66. Thompson LDR: Olfactory neuroblastoma. Head & Neck Pathol 3:252-259, 2009.
68. Vergani F, Pirola E, Fiori L, Pagni F, Parmigiani F, Sganzerla EP: Combined transcranial and endoscopic nasal resection for esthesioneuroblastoma. J Neurosurg Sci 51:99-102, 2007. 69. Walch C, Stammberger H, Anderhuber W, Unger F, Kole W, Feichtinger K: The minimally invasive approach to olfactory neuroblastoma: combined endoscopic and stereotactic treatment. Laryngoscope 110:635-640, 2000. 70. Wei JL, Scheithauer BW, Smith JS, Jenkins RB, Passe SM, Arndt CAS, Strome SE: Primary neuroblastoma of the maxillary sinus. Int J Pediatr Otorhinolaryngol 63:155-162, 2002. 71. Wellman BJ, Traynelis VC, McCulloch TM, Funk GF, Menezes AH, Hoffman HT: Midline anterior craniofacial approach for malignancy: results of en bloc versus piecemeal resections. Skull Base Surg 9:41-46, 1999. 72. Yuen APW, Fan YW, Fung CF, Hung KN: Endoscopic-assisted cranionasal resection of olfactory neuroblastoma. Head Neck 27:488-493, 2005. 73. Yuen APW, Hung KN, Fung CF: Endoscopic cranionasal resection for anterior skull base tumor. Am J Otolaryngol 18:431-433, 1997. 74. Zafereo ME, Fakhri S, Prayson R, Batra PS, Lee J, Lanza DC, Citardi MJ: Esthesioneuroblastoma: 25year experience at a single institution. Otolaryngol-Head Neck Surg 138:452-458, 2008.
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 6 November 2011; accepted 6 December 2012; published online 5 January 2013 Citation: World Neurosurg. (2013) 80, 1/2:148-159. http://dx.doi.org/10.1016/j.wneu.2012.12.003 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2013 Elsevier Inc. All rights reserved.
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RICARDO J. KOMOTAR ET AL.
Endoscopic Endonasal Compared with Anterior Craniofacial and Combined Cranionasal Resection of Esthesioneuroblastomas TUMOR
Ricardo J. Komotar1, Robert M. Starke2, Daniel M. S. Raper2 Vijay K. Anand3, Theodore H. Schwartz4
Key words Endonasal - Endoscopic - Esthesioneuroblastoma - Minimal access - Skull base - Surgery - Systematic review -
Abbreviations and Acronyms CFR: Craniofacial resection CN: Cranionasal CSF: Cerebrospinal fluid EE: Endoscopic endonasal RT: Radiotherapy From the 1Department of Neurological Surgery, University of Miami, Miami, Florida; 2 Department of Neurological Surgery, University of Virginia, Charlottesville, Virginia; and the Departments of 3 Otorhinolaryngology, and 4Neurological Surgery, Otorhinolaryngology, Neurology and Neuroscience, Weill Cornell Medical College, New York Presbyterian Hospital, New York, New York, USA To whom correspondence should be addressed: Daniel M. S. Raper, M.B.B.S. [E-mail: [email protected]] Citation: World Neurosurg. (2013) 80, 1/2:148-159. http://dx.doi.org/10.1016/j.wneu.2012.12.003 Journal homepage: www.WORLDNEUROSURGERY.org
- OBJECTIVE:
Esthesioneuroblastomas represent a surgical challenge because of their anatomical location, the necessity of achieving negative margins, and the often-cosmetically disfiguring transfacial approaches needed. Recently, expanded endonasal endoscopic approaches have been developed, either alone or in combination with a craniotomy. We conducted a systematic review of case series and case reports to compare outcomes between these various surgical approaches.
- METHODS:
A MEDLINE search was conducted of the modern literature (19852010) to identify open and endoscopic surgical series. Tumor and patient characteristics, Kadish stage, extent of resection, and progression-free and overall survival were recorded and analyzed by approach. Kaplan-Meier analysis was used to assess overall survival and progression-free survival.
- RESULTS:
Forty-seven studies comprising 453 patients were included. The endoscopic cohort had a greater proportion of Kadish Stage A tumors compared with the craniofacial group. Gross total resection was achieved in 98.1% of patients who underwent an endoscopic approach compared with 81.3% for the craniofacial and 100% for the cranionasal cohorts. Local recurrence occurred in 8.0% of patients in the endoscopic group compared with 22.1% in the craniofacial and 16.7% in the cranionasal cohorts.
- CONCLUSION:
In well-selected cases, cranionasal and endonasal approaches can be safe and effective. An ongoing evaluation of the benefits and limitations are necessary to better define the ideal patient population and patient-specific risk factors for the use of these minimal access techniques.
Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2013 Elsevier Inc. All rights reserved.
INTRODUCTION Esthesioneuroblastomas are rare, malignant tumors that arise from neurosecretory cells of the olfactory mucosa at the cribriform plate, upper third of the nasal septum, or superior turbinates (4). Despite advances in modern microsurgical techniques, the location of these lesions at the anterior cranial base often makes surgical resection challenging. The goal of esthesioneuroblastoma surgery is gross total resection with histologically negative margins. Adjuvant treatment with radiotherapy (RT), chemotherapy or both, often is used depending on the Kadish grade of the tumor (4, 18). In some circumstances neoadjuvant therapy is used (17, 18, 32, 33, 37, 42, 47, 48, 61, 62). Various surgical
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approaches are possible, with the traditional standard of care being anterior craniofacial surgery, a combined approach that incorporates lateral rhinotomy, maxillectomy, and/or sinusotomies, along with a bifrontal craniotomy (29, 47). For tumors confined to the nasal cavity or paranasal sinuses that have radiologic evidence of a normal cribriform plate and upper ethmoid sinuses, pure endonasal or transfacial approaches without craniotomy can be used to achieve negative margins (47). However, tumors with intracranial extension traditionally have required a bifrontal craniotomy with en-bloc resection of the tumor, surrounding dura, and the entire cribriform plate and crista galli (33, 47, 61). More recently, the lateral rhinotomy approach or combined craniofacial approach has been modified at certain centers, which now advocate either a purely
endonasal or combined cranionasal (CN) approach with the avoidance of a facial incision. In the endonasal approach, the entirety of the tumor is removed via an endonasal corridor (22, 43, 46, 48, 49, 51). The combined, or CN, approach incorporates endonasal endoscopic resection of accessible portions of the tumor from below with a bifrontal craniotomy for maximal resection of intracranial pathology. Philosophically, the endoscopic endonasal (EE) approach is suitable for all tumors, even those with intracranial extension, as long as the tumor does not extend lateral to the lamina papyracea. In this latter situation, a CN approach would be required, particularly if an orbital exenteration is indicated. Previous reports have indicated that, in combination with RT, endoscopic techniques may be effective in achieving local control even for
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PEER-REVIEW REPORTS RICARDO J. KOMOTAR ET AL.
ENDOSCOPIC ENDONASAL ESTHESIONEUROBLASTOMA RESECTION
Table 1. Study Characteristics of Craniofacial Esthesioneuroblastoma Resection
Study Design
No. Pts
Male
Newbill et al., 1985 (45)
Retro
10
4
Meneses et al., 1990 (40)
Retro
3
0
Author and Year
Mean Age (years)
Previous Surgery
RT
CT
43
e
10
7
52
0
1
0
Schmidt et al., 1990 (60)
CR
1
0
54
0
0
10
Dulguerov and Calcaterra, 1992 (18)
Retro
19
9
40
e
1
0
Austin et al., 1996 (2)
Retro
6
5
43
0
1
0
Bilsky et al., 1997 (3)
Retro
4
e
e
e
e
e
Miyamoto et al., 2000 (41)
Retro
8
4
43
e
0
0
Resto et al., 2000 (57)
Retro
17
e
e
e
e
e
CR
1
0
66
0
0
0
Gondim et al., 2002 (24) Wei et al., 2002 (70)
CR
1
0
15
0
e
e
Argiris et al., 2003 (1)
Retro
13
6
40
e
4
3
Dias et al., 2003 (16)
Retro
19
e
e
e
0
0
Lund et al., 2003 (37)
Retro
42
28
46
5
7
1
Constantinidis et al., 2004 (11)
Retro
3
e
43
0
1
0
Diaz et al., 2005 (17)
Retro
30
19
47
e
1
0
Feiz-Erfan et al., 2005 (21) Loy et al., 2006 (35) Sampath et al., 2006 (59)
16
e
0
0
43.6
4
50
32
0
37
0
0
0
CR
1
0
Retro
50
26
CR
1
Kim et al., 2007 (28)
Retro
10
7
48
0
6
6
McLean et al., 2007 (39)
Retro
16
e
e
e
e
e
Nakao et al., 2007 (44)
Retro
6
4
49
0
0
3
Capelle and Krawitz, 2008 (6)
CR
1
e
e
0
0
0
Kim et al., 2008 (27)
Retro
10
5
41
e
0
0
Nichols et al., 2008 (46)
Retro
9
4
48
0
0
3
Zafereo et al., 2008 (73)
Retro
12
8
61
0
3
0
Nakamura et al., 2009 (43)
Retro
5
3
55
e
e
e
Smee et al., 2011 (62)
Retro
20
e
e
0
2
0
Pts, patients; RT, radiotherapy; CT, chemotherapy; NED, no evidence of disease; GTR, gross total resection; Retro, retrospective; CR, case report.
esthesioneuroblastomas with intracranial extension (Kadish Stage C) (22, 55, 67). The purpose of this investigation was to review the existing literature to compare the efficacy of craniofacial and transfacial with CN and pure endonasal surgery in the management of esthesioneuroblastoma. The goal was to assess whether the introduction of minimal-access, endonasal endoscopic techniques has compromised
outcomes compared with the previous standard of care (12, 22, 55, 67).
MATERIALS AND METHODS Study Selection and Data Extraction The methodology for our systematic review process has been described in detail in a previous report (30). In summary, we
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performed a modern literature search using the Ovid gateway of the MEDLINE database between the years of 1985 and 2010. The following keywords were queried singly and in combination: esthesioneuroblastoma, olfactory, neuroblastoma, resection, anterior, transfacial, craniofacial, cranionasal, transcranial, transnasal, open, endoscopic, outcome, skull base, surgery. The date of last search was December, 2010.
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TUMOR
Preoperative Treatment
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ENDOSCOPIC ENDONASAL ESTHESIONEUROBLASTOMA RESECTION
Table 1. Continued Kadish Stage
Extent of Resection
Postoperative Treatment
Recurrence
TUMOR
A
B
C
GTR
Subtotal
RT
CT
Follow-up
Local
Regional
NED
1
4
5
e
e
0
0
38.9
0
1
7
0
0
2
3
0
2
1
e
0
2
2
0
0
1
1
0
1
0
e
1
0
0
8
5
4
e
e
11
1
e
7
1
6
0
0
6
e
e
4
1
65.0
0
4
3
e
e
e
4
0
e
e
e
1
e
e
0
2
6
e
e
6
2
e
3
1
3
e
e
e
10
7
9
5
66
2
1
13
0
0
1
1
0
1
0
12
0
0
1
0
0
1
1
0
e
e
24
0
0
1
2
2
9
11
2
6
0
e
8
3
6
e
e
e
18
1
19
e
e
8
5
15
4
7
31
e
e
16
1
57
7
e
25
0
2
1
e
e
1
0
62.3
2
1
1
1
10
19
23
1
23
3
88
4
4
e
e
e
e
1
0
e
e
e
e
e
0
4
14
32
e
e
e
e
93
4
8
33
0
0
1
1
0
1
0
e
0
0
1
0
0
7
e
e
7
2
e
2
2
7
e
e
e
16
0
e
e
e
e
e
e
1
1
4
e
e
4
0
e
4
1
3
e
e
e
1
0
e
e
20
e
1
0
0
0
10
e
e
7
1
28.8
e
e
3
0
3
6
4
5
9
4
56.2
2
2
7
0
6
6
10
2
e
e
84.7
2
1
9
e
e
e
4
1
e
e
e
e
e
e
e
e
e
e
e
17
2
e
6
e
16
Included studies were reviewed and carefully scrutinized for study design, methodology, patient characteristics, and primary findings. The anterior craniofacial cohort included lateral rhinotomy with medial maxillectomy, ethmoidectomy, frontal and sphenoid sinusotomies, and combined midfacial degloving; all cases included transfacial and craniotomy approaches. For studies with available information, gross
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total resection with negative margins was based on postoperative computed tomography or magnetic resonance imaging in seven papers, intraoperative surgeon’s assessment in 19 papers, and histological confirmation of clear margins in eight papers. Statistical Analysis Data from the individual studies were combined by cohort and then compared
by the use of c2 and Fisher exact tests as appropriate. Post hoc Bonferroni analysis was performed to increase stringency of significance and to account for repeated measures of analysis. Kaplan-Meier analysis was used to assess overall survival and tumor progression free survival. The log-rank test was used to assess differences in survival curves.
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PEER-REVIEW REPORTS RICARDO J. KOMOTAR ET AL.
ENDOSCOPIC ENDONASAL ESTHESIONEUROBLASTOMA RESECTION
Table 2. Study Characteristics of Endonasal Esthesioneuroblastoma Resection
Author and Year
Study Design
No. Pts
Male
Mean Age (years)
Previous Surgery
RT
CT
Walch et al., 2000 (69)
Retro
3
0
43
e
e
e
Casiano et al., 2001 (7)
Retro
5
2
64
3
0
0
Cakmak et al., 2002 (5) Liu et al., 2003 (34) Pasquini et al., 2003 (51) Constantinidis et al., 2004 (11) Roh et al., 2004 (57)
CR
1
0
12
0
0
0
Retro
1
1
74
1
0
0
CR
1
1
72
0
0
0
Retro
6
e
56
0
0
0
CR
1
0
40
0
0
0
Poetker et al., 2005 (55)
Retro
5
e
55
e
e
e
Unger et al., 2005 (67)
Retro
14
6
49
2
0
e
Castelnuovo et al., 2006 (8)
Retro
10
3
56.2
1
0
0
Dave et al., 2007 (12)
Retro
10
7
61.2
e
e
e
McLean et al., 2007 (39)
Retro
3
e
e
e
e
e
67
e
0
0
51.5
e
e
e
CR
1
0
Suriano et al., 2007 (65)
Podboj and Smid, 2007 (54)
Retro
9
e
Nichols et al., 2008 (46)
Retro
1
1
11
0
0
0
Zafereo et al., 2008 (74)
Retro
3
1
57
0
0
0
CR
1
1
79
0
0
0
Dehdashti et al., 2009 (13)
Retro
4
4
43
e
e
e
Folbe et al., 2009 (22)
Retro
23
16
57
4
0
0
Chan et al., 2009 (10)
Pts, patients; RT, radiotherapy; CT, chemotherapy; NED, no evidence of disease; GTR, gross total resection; Retro, retrospective; CR, case report.
RESULTS Study Selection A total of 99 published studies were identified through our initial MEDLINE database search. After careful scrutiny of these studies, 52 were rejected from our review because they did not include original data, were purely anatomical studies, did not report outcomes, did not differentiate endoscopic outcomes from a cohort that included a mixture of approaches, or repeated data reported elsewhere. Twenty-seven studies reported outcomes from craniofacial resection (CFR) or transfacial resection, 19 studies reported outcomes for endonasal approaches, and 10 studies reported outcomes for CN approaches. A total of 47 studies and 453 patients were included in this review. Study Characteristics Characteristics and primary findings of the 27 studies involving CFR are summarized in
Table 1. Regarding study design, 21 papers were retrospective (1-3, 11, 16, 17, 19, 27, 28, 35, 37, 39-41, 43-46, 57, 62, 74), and there were six case reports (6, 21, 23, 59, 60, 70). Characteristics and primary findings of the 19 studies involving endonasal resection are summarized in Table 2. Regarding study design, 14 papers were retrospective (7, 8, 11-13, 22, 34, 39, 46, 55, 65, 67, 69, 74), and there were five case reports (5, 10, 51, 54, 58). Characteristics and primary findings of the nine studies involving CN resection are summarized in Table 3. There were six retrospective series (11, 15, 27, 34, 72, 74) and three case reports (26, 49, 68). There were no randomized controlled trials. Patient Characteristics Patient characteristics for each cohort are reported in Table 4. There were 318 patients in the CFR cohort, 102 patients in the EE cohort, and 33 patients in the
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CN cohort. Regarding presenting symptoms, there were no differences between endonasal and craniofacial approaches. Compared with the CN cohort, patients treated via an endonasal approach had a lower incidence of epistaxis (P ¼ 0.05), olfactory dysfunction (P ¼ 0.01), and facial/sinus pain (P < 0.003). Compared with the craniofacial approach, patients in the CN group had a greater incidence of olfactory dysfunction (P < 0.003). Regarding tumor stage, compared with the CFR group, the EE group had a greater proportion of Kadish Stage A (P ¼ 0.003) and Kadish Stage B (P < 0.003), and a lower incidence of Kadish Stage C (P < 0.003) tumors. The endoscopic group had a greater proportion of Kadish Stage B tumors than the CN group (P ¼ 0.02), but no differences in the incidence of other tumor stages (Figure 1). There were no differences between the CN and CFR groups. Patients in the CFR group had
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TUMOR
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PEER-REVIEW REPORTS RICARDO J. KOMOTAR ET AL.
ENDOSCOPIC ENDONASAL ESTHESIONEUROBLASTOMA RESECTION
Table 2. Continued Kadish Stage
TUMOR
A
B
Extent of Resection C
GTR
Subtotal
Postoperative Treatment RT
CT
Recurrence Follow-up
Local
Regional
NED
0
2
1
3
0
0
0
58.3
0
0
3
1
3
0
5
0
5
e
31
e
2
4
e
e
e
1
0
1
e
24
e
e
0
0
1
0
1
0
e
e
30
0
0
1
e
e
e
1
0
e
e
58
0
0
1
1
4
1
e
e
4
0
125.2
0
0
4
e
e
e
1
0
1
0
7
0
0
1
1
2
2
e
e
4
2
74.8
2
e
5
0
5
9
e
e
e
e
59.8
3
e
e
3
5
2
10
0
9
1
38.1
0
0
10
5
2
2
10
0
e
e
40.5
0
1
e
e
e
e
3
0
e
e
e
e
e
e
e
e
e
1
0
0
e
88
0
0
1
3
6
0
9
0
9
0
42.8
0
0
9
0
0
1
0
0
1
0
23
0
e
1
2
1
0
3
0
e
e
67.3
1
0
3
1
0
0
1
0
1
0
16
e
e
1
e
e
e
4
0
e
e
e
e
e
e
2
11
5
e
e
16
e
45.2
1
e
1
a lower rate of previous surgery than the endoscopic group (P ¼ 0.02) and greater rates of preoperative RT (P < 0.003) and preoperative chemotherapy (P < 0.003). The CN cohort had greater rates of preoperative RT (P ¼ 0.03) and computed tomography (P < 0.003) than the endoscopic group. The CN group had a lower rate of preoperative RT than the CFR group (P ¼ 0.03). There were no other significant differences in presenting or tumor characteristics between the groups. Outcomes and Complications Outcomes and complications for each cohort are reported in Tables 5 and 6. Extent of Resection In the CFR cohort, gross total resection was reported in 16 studies and achieved in 81.3% of patients (109/134); subtotal resection (>80%-90%) was achieved in 14.2% of patients (19/134); and partial
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resection not reported in any cases. Negative margins reported in 11 studies and were achieved in 85 of 110 cases (77.3%). In the EE cohort, gross total resection was reported in 15 studies and achieved in 98.1% of patients (53/54); subtotal resection was achieved in no case; and partial resection was achieved in 1.9% of patients (1/54). Negative margins were reported in 14 studies and achieved in 75 of 80 cases (93.8%). In the CN cohort, gross total resection was reported in 6 studies and achieved in all patients (12 of 12). Negative margins were reported in eight studies and achieved in 23 of 24 cases (95.8%; Figure 2). Postoperative Complications In the CFR cohort, the most common postoperative complications included cerebrospinal fluid (CSF) leak in 11 of 182 cases (6.0%), epidural hematoma in 3 of 54 cases (5.6%), epiphora in 7 of 132 cases (5.3%) and bone flap infection in 9 of 176
cases (5.1%). Meningitis occurred in 4 of 89 cases (4.5%). In the EE group, persistent nasal crusting was reported in 44 of 65 cases (67.7%) in seven studies, and epistaxis occurred in 2/11 cases (18.2%) in three studies. CSF leak was reported in 5 of 69 cases (7.2%) in nine studies and epidural abscess occurred in 1 of 24 cases in two studies (4.2%). In the CN group, CSF leak occurred in 18.2% of cases (2/11) in four studies. Postoperative venous thromboembolus occurred in one case in four studies (9.2%). No other postoperative complications were reported in the endoscopic or CN cohorts. Perioperative mortality occurred in 4 of 124 cases (3.2%) in 12 studies in the CFR group and in no cases in five studies in the EE group or in five studies in the CN group (Figure 3). Outcomes and Recurrence In the CFR group, mean follow-up was 71.0 months. Local recurrence was reported in 22 studies and occurred in 63 of
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Table 3. Study Characteristics of Cranionasal Esthesioneuroblastoma Resection
Author and Year Devaiah et al., 2003 (15) Kenmochi et al., 2003 (26)
Study Design
No. Pts
Male
Mean Age (years)
Previous Surgery
RT
CT
Retro
7
4
47
e
1
1
CR
1
0
44
0
0
0
Liu et al., 2003 (34)
Retro
2
1
47
0
1
2
Constantinidis et al., 2004 (11)
Retro
5
e
45
0
0
0
Yuen et al., 2005 (72)
Retro
6
4
51
0
1
0
Vergani et al., 2007 (68) Kim et al., 2008 (27) Park et al., 2008 (49) Zafereo et al., 2008 (74)
CR
1
1
36
0
e
e
Retro
9
3
48
e
0
8
CR
1
0
69
0
0
0
Retro
1
1
70
0
0
0
Pts, patients; RT, radiotherapy; CT, chemotherapy; NED, no evidence of disease; GTR, gross total resection; Retro, retrospective; CR, case report.
285 cases (22.1%). Tumor progression-free survival was reported in nine studies. Regional metastasis was reported in 20 studies and occurred in 38 of 220 cases (17.3%). The mean time to regional metastasis was 50.7 months (range, 1496.1 months) and was reported in 11 studies. Among patients who were alive at last follow-up in 23 studies, 163 of 263 (61.9%) were reported to be free of disease. In the EE group, mean follow-up was 52.0 months. Local recurrence was reported in 14 studies and occurred in 7 of 88 cases (8.0%). Regional metastasis was reported in 14 studies and occurred in 3 of 50 cases (6.0%). The mean time to regional metastasis was not reported in any studies included in this review. Among patients who were alive at last follow-up in 15 studies, 45 of 71 (63.4%) were reported to be free of disease. In the CN group, mean follow-up was 43.1 months. Local recurrence was reported in seven studies and occurred in 3 of 18 cases (16.7%). Regional metastasis was reported in eight studies and occurred in 2 of 24 cases (8.3%). The mean time to regional metastasis was 40.0 months (range, 2-78.0 months) and was reported in two studies. Among patients who were alive at last follow-up in nine studies, 27 of 33 (81.8%) were reported to be free of disease. Tumor progression-free and overall survival for the combined cohorts are shown in Figures 4 and 5. The 1-, 3-, 5-, and 10-year progression-free survival rates
were 91.6%, 79.4%, 73.7%, and 60.5% respectively (Figure 4). The 1-, 3-, 5-, and 10-year overall survival rates were 92.2%, 83.4%, 81.5%, and 65.7%, respectively (Figures 5, 6, and 7). DISCUSSION Esthesioneuroblastomas are rare malignant neuroectodermal tumors that account for approximately 2% of all sinonasal tract neoplasms, with an incidence of approximately 0.4 per million population (66). The optimal goal of treatment is the achievement of gross total resection with negative margins followed by either RT, chemotherapy or both, depending on the extent of disease (4, 18). Using the gold standard of a CFR approach to achieve enbloc resection with negative margins (36, 53, 56, 71), multicenter international collaborative studies report 5-year overall survival rates between 60% and 90% and 10-year survival of 40%-80% (8, 16, 17, 19, 48, 57). In recent years, endonasal endoscopic approaches have been investigated as either a primary or adjuvant surgical approach to remove esthesioneuroblastomas, as well as a variety of other pathologies of the anterior skull base (14, 20). The advantage of this technique is that it avoids a facial incision and, in some circumstances, may also avoid a craniotomy via a more direct, anterior approach to the pathology. The endoscope also moves the lens and light source
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significantly closer to the tumor than conventional operative microscopy, providing superior visibility, with the ability to look around corners with the use of angled endoscopes. For tumor that extends lateral to the lamina papyracea, the endonasal approach can be combined with a craniotomy, also known as the “cranionasal” approach (15, 34). However, it is unclear whether the use of endonasal endoscopy results in compromised outcome with respect to extent of resection and the ability to achieve negative margins because, often, tumors cannot be removed en bloc. Likewise, the use of a purely endonasal approach to remove intracranial pathology risks a significant CSF leak since a pericranial flap, the mainstay of skull base closure, cannot be harvested, although a vascularized nasoseptal flap may be used as an alternative (21). Anterior Craniofacial and Combined CN Approaches Complete tumor resection, using a transfacial and/or bifrontal craniotomy (anterior craniofacial) approach, combined with postoperative RT, has traditionally been considered the “gold standard” treatment for esthesioneuroblastomas (4, 18, 45). Craniofacial approaches facilitate complete resection of bulky disease with significant intracranial extension (62). A number of series have demonstrated high rates of gross total resection with 5-year overall survival rates between 60% and
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Table 3. Continued Kadish Stage
Postoperative Treatment
Extent of Resection
TUMOR
A
B
C
GTR
Subtotal
RT
CT
3
1
3
e
e
5
0
0
0
1
1
0
1
0
0
0
2
2
0
e
e
0
3
2
e
e
4
0
3
2
1
6
0
1
0
0
1
1
0
1
1
7
e
e
0
0
1
1
0
0
0
0
1
1
0
e
90% and 10-year survival of 40%-80% (8, 16, 17, 19, 57). En-bloc resection, although conceptually appealing, is not always possible using a craniofacial approach, and piecemeal craniofacial surgery has been shown to provide equivalent survival outcomes to en bloc resection (38). Anterior craniofacial approaches are associated with a number of disadvantages,
Recurrence Follow-up
Local
Regional
NED
62.3
1
1
6
0
0
1
12.5
0
0
2
75.4
2
0
3
0
32.8
e
1
4
e
e
12
0
0
1
9
1
20.8
e
e
8
1
e
0
0
1
e
14
0
0
1
132
including scarring with lateral rhinotomy, limited superior access when the midface degloving approach is used, and limited access to the sphenoid sinus and frontal recess with the craniofacial approach (42, 55). Overall, postoperative morbidity has been reported to be approximately 35%, with mortality of 2%-5% (74). Furthermore, surgery alone is insufficient in controlling
esthesioneuroblastomas and would be recommended by most teams as the sole treatment strategy only in Kadish A tumors (37, 74). After the emergence of endoscopic techniques for removal of nasal and sinus neoplasia, combined endonasal and craniotomy approaches for esthesioneuroblastoma were reported in the late 1990s
Table 4. Patient and Tumor Characteristics in Craniofacial, Endonasal and Cranionasal Esthesioneuroblastoma Resection Craniofacial
P Value (CFR vs. EE)
Endonasal
P Value (EE vs. CN)
Cranionasal
P Value (CN vs. CFR)
Patient characteristics Total patients Mean age (range) Male (%)
318 45.3 (6-85)
102
33
54.5 (11-81)
48.5 (28-72)
132/238 (55.5)
1.00
43/79 (54.4)
1.00
14/28 (50.0)
1.00
120/157 (76.4)
0.90
53/64 (82.8)
1.00
9/12 (75.0)
1.00
Presenting symptoms Nasal obstruction (%) Epistaxis (%)
69/157 (43.9)
0.18
19/63 (30.2)
0.05*
8/12 (66.7)
0.38
Nasal discharge (%)
17/157 (10.8)
1.00
6/57 (10.5)
1.00
2/10 (20.0)
1.00
Olfactory dysfunction (%)
19/157 (12.1)
1.00
7/62 (11.3)
0.01*
5/10 (50.0)
<0.003*
Facial/sinus pain (%)
11/157 (7.0)
0.10
0/63 (0.0)
<0.003*
3/12 (25.0)
0.08
Tumor stage Kadish A
21/233 (9.0)
0.003*
19/85 (22.4)
1.00
7/33 (21.2)
0.10
Kadish B
56/233 (24.0)
<0.003*
42/85 (49.4)
0.02*
7/33 (21.2)
1.00
Kadish C
153/233 (65.7)
<0.003*
23/85 (27.1)
0.99
19/33 (57.6)
1.00
Kadish D Previous surgery (%)
3/233 (1.3)
1.00
1/85 (1.2)
1.00
0/33 (0.0)
1.00
9/166 (5.4)
0.02*
11/67 (16.4)
0.22
0/17 (0.0)
0.98
CFR, craniofacial resection; EE, endoscopic endonasal; CN, cranionasal. *Statistically significant.
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esthesioneuroblastomas confirmed satisfactory rates of complete excision without local recurrence (72). Kim et al. (27) found the CN approach to be equivalent to traditional CFR in their series of sinonasal tumors, and Devaiah et al. (15) demonstrated complete tumor control in their series, arguing that craniotomy provided more accurate resection of anterior cranial fossa disease than radiosurgery.
Figure 1. Kadish stage of each approach.
Endoscopic Endonasal Approach A purely EE approach for resection of esthesioneuroblastomas is a natural extension of the philosophy underlying the
and early 2000s. Yuen and colleagues first described this approach in 1997 (73), and their subsequent experience with a series of
combined CN approach and has been increasingly reported during the past 10 years. Unger et al. (67) used a combination of endoscopic surgery with radiosurgery to target intracranial extension and achieved complete tumor control at a follow- up of 58 months. However, four patients in this series (29%) required a second radiosurgical procedure. Stammberger et al. (64) and Walch et al. (69) likewise reported early series of patients treated with combined endoscopic and radiosurgical treatment. Most of these early cases did not breach the dura. Casiano et al. (7) described the first instance of an endoscopic en-bloc resection
Table 5. Outcomes and Complications in Craniofacial, Endonasal, and Cranionasal Esthesioneuroblastoma Resection Craniofacial
No. Studies
Occurrence/ Total Pts
Gross total
16
109/128
Subtotal
16
19/128
Partial
16
0/128
Negative margins
11
Positive margins
11
Neoadjuvant RT
Endonasal
Cranionasal
No. Studies
Occurrence/ Total Pts
%
No. Studies
Occurrence/ Total Pts
85.2
15
53/54
98.1
6
12/12
14.8
15
0/54
0.0
6
0/12
0.0
0
15
1/54
1.9
6
0/12
0.0
85/110
77.3
14
75/80
93.8
8
23/24
95.8
25/110
22.7
14
5/80
6.2
8
1/24
4.2
22
87/275
31.6
13
0/68
0.0
8
3/32
9.4
Neoadjuvant CT
22
56/275
20.4
12
0/54
0.0
8
11/32
34.4
Adjuvant RT
19
144/211
68.2
12
51/66
77.3
6
20/29
69.0
Adjuvant CT
19
23/211
10.9
8
3/36
8.3
6
2/29
6.9
Nasal crusting
5
2/51
3.9
7
46/65
70.8
1
0/2
0.0
Epistaxis
4
0/24
0.0
3
2/11
18.2
2
0/3
0.0
Epidural hematoma
5
3/54
5.6
1
0/1
0.0
3
0/4
0.0
Bone flap infection
11
9/176
5.1
1
0/1
0.0
3
0/4
0.0
Epidural abscess
9
3/134
2.2
2
1/24
4.2
3
0/4
0.0
DVT/PE
9
3/144
2.1
1
0/1
0.0
4
1/11
9.2
Meningitis
9
4/89
4.5
2
0/24
0.0
3
0/4
0.0
CSF leak
12
11/182
6.0
9
5/69
7.2
4
2/11
18.2
Anosmia
3
1/21
4.8
1
0/10
0.0
1
0/1
0.0
Seizure
7
3/97
3.1
1
0/1
0.0
2
0/3
0.0
6
7/132
5.3
1
0/1
0.0
2
0/3
0.0
12
4/124
3.2
5
0/24
0.0
5
0/6
0.0
%
%
Extent of resection 100
Adjuvant therapy
Complications
Epiphora Perioperative mortality Follow-up (months)
71.0 (12-93)
52.0 (7-125)
43.1 (12-132)
RT, radiotherapy; CT, chemotherapy; DVT, deep-vein thrombosis; PE, pulmonary embolism; CSF, cerebrospinal fluid.
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Table 6. Outcomes and Recurrence in Craniofacial, Endonasal, and Cranionasal Esthesioneuroblastoma Resection Craniofacial
Endonasal
Cranionasal
TUMOR
No. Studies
Occurrence/ Total Pts
%
No. Studies
Occurrence/ Total Pts
%
No. Studies
Occurrence/ Total Pts
%
22
63/285
22.1
14
7/88
8.0
7
3/18
16.7
Recurrence Local recurrence Time to local recurrence Regional metastasis
42.2 (12.6-70.8) 20
38/220
Time to metastasis NED at last follow-up
17.3
33.0 (14.5-43.7) 14
3/50
50.7 (14-96.1) 23
162/263
59.0 6.0
8
NR 61.6
15
45/71
2/24
8.3
40.0 (2-78) 63.4
9
27/33
81.8
Pts, patients; NR, not reported; NED, no evidence of disease.
of an esthesioneuroblastoma invading the dura and crista galli, via the use of a purely endoscopic approach. Castelnuovo et al. (8) found en-bloc resection to be feasible only for small tumors, but were able to achieve complete resection in all tumors without gross brain invasion. Dave et al. (12) cautioned that obtaining clear surgical margins is essential; if, during endoscopic surgery, areas of tumor extension beyond the surgical field are observed, conversion to a combined CN procedure has been considered essential (8, 12). The necessity of achieving resection with negative surgical margins is underscored by a 1307patient analysis of malignant skull base tumors, which demonstrated that survival was halved and recurrence doubled with positive surgical margins (52). Despite the necessity of removing tumor piecemeal, rather than en bloc, adherence to oncologic principles of tumor resection is still possible using endoscopic approaches (63) Folbe et al. (22) demonstrated that Kadish Stage C tumors could be completely excised through a purely EE approach.
Figure 2. Extent of resection for each approach.
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In older series of esthesioneuroblastomas that include tumors with significant intracranial involvement, postoperative CSF leak rates can occur in up to 29% (22, 55). Although postoperative CSF leak is still a major limitation to the widespread adoption of endoscopic techniques, methods of reconstruction of the dural defect have significantly improved, even over the short time that these approaches have been used (25, 31, 50). More recent series of endoscopically treated anterior skull base lesions report CSF leak rates of 0%-4% using more complex, multilayer reconstruction techniques (9, 22) and is echoed in our own experience (T. H. Schwartz, unpublished data, May 2011). One such technique, the multilayer “gasket seal” closure with an additional nasoseptal pedicled flap, has been used with zero incidence of CSF leak in a variety of anterior cranial base surgery (31). Overall and progression-free survival rates for endonasal surgery are as good or better than other reported survival
Figure 3. Complication rates for each approach.
analyses following esthesioneuroblastoma resection in the literature (14, 16, 35). In an analysis of 36 patients treated at a single institution, Dias et al. (16) demonstrated significantly greater progression-free survival among patients treated with CFR and RT, compared with limited transcranial resection and RT, or RT alone. A meta-analysis of the literature undertaken by Devaiah et al. in 2009, showed a significantly greater overall survival in patients treated with either an endoscopic or endoscope-assisted approach compared with open approaches (14). The role of surgery for esthesioneuroblastomas must be placed in the wider context of treatment for these difficult tumors, which may include adjuvant or neoadjuvant treatment with RT, radiosurgery, or chemotherapy (17, 18, 32, 33, 37, 42, 48, 61, 62). Neoadjuvant therapy
Figure 4. Tumor progression-free survival for patients with esthesioneuroblastoma. Kaplan-Meier survival analysis for the combined cohort of patients treated with either craniofacial, endoscopic, or CN approaches.
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Figure 5. Overall survival for patients with esthesioneuroblastoma. Kaplan-Meier survival analysis for the combined cohort of patients treated with either craniofacial, endonasal, or CN approaches.
has the potential to increase survival after incomplete or complete resection of esthesioneuroblastomas (11, 27, 39, 48, 65, 67). Radiation is generally accepted as providing an additional benefit to surgery alone (29, 57), although it has not been used in all cases in which a complete resection was achieved without an obvious decrease in survival (55, 58). Chemotherapy has a less well-established role and has found the most use in patients with incompletely resected tumors or for salvage therapy (29, 62). Newer technologies, such as intensity-modulated radiation therapy, have also been used with comparable 5-year disease-free and overall survival to traditional combined modality therapies after CFR (39). Adjuvant treatments are as essential after endoscopic surgery as for any other approach for esthesioneuroblastomas, and are widely used for most patients in order to prevent
Figure 6. Tumor progression-free survival for patients with esthesioneuroblastoma by surgical approach. Kaplan-Meier survival analysis of progression-free survival for the endonasal, craniofacial, and CN approaches.
ENDOSCOPIC ENDONASAL ESTHESIONEUROBLASTOMA RESECTION
Figure 7. Overall survival for patients with esthesioneuroblastoma by surgical approach. Kaplan-Meier survival analysis of overall survival for the endonasal, craniofacial, and CN approaches.
recurrence and increase progression-free survival, except perhaps for patients with Kadish Grade A tumors that are completely excised at operation (37). Unfortunately we were not able to include analysis of the effect of neoadjuvant treatment on outcomes following esthesioneuroblastoma resection due to inconsistency of reporting in primary studies. Further work is necessary to identify which esthesioneuroblastomas benefit from routine neoadjuvant therapy, and which may safely be observed, with adjuvant treatments reserved for relapse. Because of significant differences in the patient populations in the CFR, EE, and CN cohorts in this study, it is not possible to draw direct comparisons of outcomes, complications, or survival between the groups. Specifically, there were a greater proportion of lower-grade tumors, and a lower proportion of higher-grade tumors in the endoscopic cohort compared with the craniofacial cohort. To delineate the effect of Kadish grade on extent of resection and recurrence, we performed a Mann-Whitney U statistical analysis. This analysis demonstrated that there was no significant association between Kadish grade and extent of resection except for Kadish grade C tumors in the comparison between craniofacial and CN groups. There were no statistically significant differences between the surgical approaches with regard to other Kadish grades for extent of resection or with regard to any Kadish grade for recurrence. These analyses were limited by the number of individual patients with information stratified by Kadish grade for both resection and recurrence. An additional
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limitation is that further information regarding time dependent variables, such as time to recurrence, was not available. Despite these limitations, the literature does permit some overall observations about the suitability of different lesions for each approach. Esthesioneuroblastomas require an individualized approach to treatment. Endoscopic approaches have been more commonly used, and are likely best suited to, tumors with smaller volume, no or minimal intracranial extension and lower Kadish staging (Kadish A or B). In contrast, craniofacial or combined CN approaches may be more useful for larger, more extensive or higher grade tumors. For lesions extending lateral to the lamina papyracea, a craniotomy should be incorporated either in combination with a transfacial or endoscopic approach. The status of any previous surgical intervention may affect the choice of approach, with more aggressive approaches more likely to be used at the first intervention, followed by less-invasive approaches for recurrence. It is important to note that, though most esthesioneuroblastomas tend to recur within 5 years of initial treatment (4), recurrence continues to occur over time (32). Ongoing surveillance and multidisciplinary involvement are essential to improving long-term outcomes for these rare and difficult tumors. CONCLUSION The introduction of endoscopy for the treatment of esthesioneuroblastomas, in either a purely endonasal or combined CN approach, does not result in worse outcome with respect to extent of resection, negative margins, progression-free or overall survival rates compared with more traditional craniofacial approaches in tumors for which this approach is suitable. Careful selection of cases in the literature has likely contributed to these good reported outcomes. Nevertheless, the increased visibility afforded by the endoscope may provide an advantage for the resection of small, low-grade esthesioneuroblastomas compared with more traditional transfacial approaches. Indeed, outcomes are improved, which may either reflect careful selection of smaller tumors for the endonasal approach or increased visibility provided
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by the endoscope. Moreover, complication rates, particularly CSF leak, are not greater and may indeed be lower. Patients treated via the endonasal approach in the literature have smaller, lower-grade tumors, which may have significantly affected their observed outcomes. Nevertheless, for tumors with intracranial extension limited to the area between the lamina papyracea, a purely endonasal endoscopic approach may offer a safe and effective, minimal access surgical option. Ongoing evaluation of the benefits and limitations are necessary to better define the ideal patient population and patient-specific risk factors for the use of these minimal access techniques. REFERENCES 1. Argiris A, Dutra J, Tseke P, Haines K: Esthesioneuroblastoma: the Northwestern University Experience. Laryngoscope 113:155-160, 2003. 2. Austin JR, Cebrun H, Kershisnik MM, ElNaggar AK, Garden AS, DeMonte F, Ginsberg LE, Lippman SM, Goepfert H: Olfactory neuroblastoma and neuroendocrine carcinoma of the anterior skull base: treatment results at the M.D. Anderson Cancer Center. Skull Base Surg 6:1-8, 1996. 3. Bilsky MH, Kraus DH, Strong EW, Harrison LB, Gutin PH, Shah JP: Extended anterior craniofacial resection for intracranial extension of malignant tumors. Am J Surg 174:565-568, 1997. 4. Bragg TM, Scianna J, Kassam A, Emami B, Brown HG, Hacein-Bey L, Clark JI, Muzaffar K, Boulis N, Prabhu VC: Clinicopathological review: esthesioneuroblastoma. Neurosurgery 64:764-770, 2009. 5. Cakmak O, Ergin NT, Yilmazer C, Kayaselcuk F, Barutcu O: Endoscopic removal of esthesioneuroblastoma. Int J Pediatr Otolaryngol 64:233-238, 2002. 6. Capelle L, Krawitz H: Esthesioneuroblastoma: a case report of diffuse subdural recurrence and review of recently published studies. J Med Imaging Radiation Oncol 52:85-90, 2008. 7. Casiano RR, Numa WA, Falquez AM: Endoscopic resection of esthesioneuroblastoma. Am J Rhinology 15:271-279, 2001. 8. Castelnuovo PG, Delu G, Sberze F, Pistochini A, Cambria C, Battaglia P, Bignami M: Esthesioneuroblastoma: endonasal endoscopic treatment. Skull Base 16:25-29, 2006. 9. Cavallo LM, Prevedello D, Esposito F, Laws ER Jr, Dusick JR, Messina A, Jane JA Jr, Kelly DF, Cappabianca P: The role of the endoscope in the transsphenoidal management of cystic lesions of the sellar region. Neurosurg Rev 31:55-64, 2008. 10. Chan LP, Wang LF, Tai CF, Wu CC, Kuo WR: Huge sphenoid sinus olfactory neuroblastoma: a case report. Kaohsiung J Med Sci 25:87-92, 2009.
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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 6 November 2011; accepted 6 December 2012; published online 5 January 2013 Citation: World Neurosurg. (2013) 80, 1/2:148-159. http://dx.doi.org/10.1016/j.wneu.2012.12.003 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2013 Elsevier Inc. All rights reserved.
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