- Email: [email protected]
Evaluation of Olfactory Outcome After Frontolateral Approach for Treatment of Suprasellar Tumors
Accepted Manuscript Title: Evaluation of the olfactory outcome after frontolateral approach for the treatment of suprasellar tumors Mario Giordano, MD, Venelin M. Gerganov, MD, Massimo Gallieni, MD, Amir Samii, MD, PhD, Prof., Madjid Samii, MD, PhD, Prof. PII:
S1878-8750(18)30613-2
DOI:
10.1016/j.wneu.2018.03.131
Reference:
WNEU 7743
To appear in:
World Neurosurgery
Received Date: 5 February 2018 Revised Date:
18 March 2018
Accepted Date: 19 March 2018
Please cite this article as: Giordano M, Gerganov VM, Gallieni M, Samii A, Samii M, Title: Evaluation of the olfactory outcome after frontolateral approach for the treatment of suprasellar tumors, World Neurosurgery (2018), doi: 10.1016/j.wneu.2018.03.131. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
1
ACCEPTED MANUSCRIPT
Title: Evaluation of the olfactory outcome after frontolateral approach for the treatment of suprasellar tumors
•
Gerganov, Venelin M., MD 1
•
Gallieni, Massimo, MD 1
•
Samii, Amir, MD, PhD; Prof. 1,2
•
Samii, Madjid, MD, PhD; Prof. 1
International Neuroscience Institute; Department of neurosurgery, Rudolf Pichlmayr Str. 4,
Hannover 30625, Germany 2
SC
Giordano, Mario, MD 1
M AN U
1
•
RI PT
Authors:
Leibniz Institute for Neurobiology, Brenneckestrasse 6, Magdeburg 39118, Germany
TE D
Corresponding author:
Giordano, Mario, MD; International Neuroscience Institute- Hannover, Germany Address: International Neuroscience Institute- Hannover, Rudolf Pichlmayr Str. 4, Hannover 30625, Germany
EP
Phone: ++49 (511) 27092865 Fax: ++49 (511) 27092706
AC C
E-mail address: [email protected]
Key words: Olfactory nerve, frontolateral approach, suprasellar tumor Running head: Olfactory outcome after frontolateral approach No financial and/or material support The paper has not been presented (nor published) previously
2
ACCEPTED MANUSCRIPT
Introduction
In modern neurosurgery the preservation of patient´s neurological status and quality of life has
RI PT
become mandatory. Olfaction has received less attention in comparison to other fundamental senses such as vision and hearing. However, sense of smell has an important impact on patient´s everyday life: its deficit may lead to decreased appreciation of food, exposure to dangers (gas)
24
. Common pathological conditions, such as nasal, endocrine and
neurodegenerative disorders
10
, may lead to olfactory dysfunction that can be also iatrogenic
M AN U
normal population
SC
and difficulty in personal relationship leading to a higher depression rate in comparison with the
consequent to extensive transcranial 4,8,11,18,19,26 or transnasal 3 surgical approaches to the anterior skull base.
One of the most frequently used approaches to the anterior skull base and the supra-/ parasellar
TE D
area in the recent years is the frontolateral. The risk for olfactory nerve damage, related to the approach, however, has not been systematically evaluated. In the manuscript, we present the findings of our prospectively designed and performed study, assessing olfactory function
AC C
EP
outcome in patients undergoing frontolateral approach for the resection of suprasellar lesions.
Material and methods
Eighteen consecutive non-randomized patients (7 females, 11 males) surgically treated at our Institute for suprasellar tumors were included in this prospective study. Lesions extending to the anterior skull base reaching directly the olfactory nerve were excluded. The mean age of the
3
ACCEPTED MANUSCRIPT
patients was 42 years (range 16-76 years). Exclusion criteria were: history of previous cranial surgery, radiotherapy or severe head trauma. Based on imaging and intraoperative findings every lesion was classified as cystic or solid. Maximal suprasellar (vertical) extension was calculated using the preoperative magnetic resonance imaging (MRI) scan on a plane perpendicular to the
RI PT
anterior skull base.
Olfactory function was evaluated at the admission and 14 days after the surgery using the standard 12-items “Sniffin´ Sticks” screening (SSS) test (Burghart Messtechnik, Wedel 14,15
. The test involves the presentation of 12 odorants in felt-tip pens. The pens
SC
Germany)
tampon is filled with different dissolved odorants. During the test, the pen cap is removed and
M AN U
presented to the patient for 3 seconds at a distance of 2 cm in front of the nostril. On a multiple choice task the identification of the odorants was done from a list of 4 for each pen. The interval between pens presentation was ca. 20 seconds. Both nostril were examined in all the subjects and the better nostril result was considered 14. The test result has a range from a minimum of 0 to a
TE D
maximum of 12. A difference between preoperative and postoperative value ≥ 3 was considered hyposmia. A patient with postoperative value of 0 was classified as anosmic. A subjective evaluation of the olfactory function was also performed before the administration of the
EP
postoperative SSS asking to the patient if a difference in smelling
AC C
The olfactory outcome was correlated to the following variables: tumor type, size, consistency and extent of vertical and lateral growth. Commercially available software (IBM SPSS Statistics for Mac, Version 23.0. Armonk, NY: IBM Corp) was used for data analysis. Descriptive statistic and t-test were performed with a significance ascribed in case of error probability of p<0.05.
Operative technique
4
ACCEPTED MANUSCRIPT
The frontolateral approach could be regarded as a modification of the frontotemporal approach, including only its frontal part or as a less invasive version of the unilateral subfrontal approach. The head of the patient is fixed with the Mayfield clamp, rotated slightly to the contralateral side and hyperextended so that the zygoma becomes be the highest point in the sagittal plane.
RI PT
Thus, due to gravity, less retraction of the frontal lobes is required. The skin incision is done behind the hairline, starting anterior to the tragus and reaching the midline. In bold patients, we prefer to place the incision at a skin crease in the forehead. Laterally a single burr hole is
SC
made at the key point and the craniotomy is performed with the craniotome. The size of the craniotomy is usually 25 to 35 mm in width and 20 to 25 mm in height; however, it extent is
M AN U
modified according to the size of the frontal sinus. The craniotomy should reach the supraorbital notch frontomedially preserving the supraorbital nerve. An attempt to avoid opening of the sinus is always made, unless it is very large. In case of opening, the mucosa is removed, the sinus is then treated with antiseptic solution and at the end isolated with
TE D
pericranial flap. The cranial base is flattened with a diamond drill in order to have a notobstructed basal view to the area of interest.
The dura is incised in a semicircular manner with an inferior base. The crucial step is the
EP
drainage of sufficient amount of CSF by creating a small opening of the Sylvain cistern. In
AC C
case of intrasellar extension of the tumor the tuberculum sellae is drilled off allowing to reach that portion. The application of angled endoscope may be useful in such cases. The frontal lobe has just to be held with a single self-retaining retractor. Importantly, the retractor should be placed along the olfactory nerve without crossing it to avoid pressure, exerting only moderate controlled traction of this nerve. In most cases there is no need of olfactory nerve dissection. If the nerve looks under tension, however, sharp dissection is performed, preserving its vascular supply. During tumor removal care is taken not to injure unintentionally the nerve or to cause its iatrogenic damage with the bipolar coagulation.
5
ACCEPTED MANUSCRIPT
Results
All patients underwent tumor removal via the frontolateral approach: 16 on the right and 2 on the
RI PT
left side. The histological diagnosis was: craniopharyngioma in 9 (Figure 1 A,B), meningioma in 6, adenoma in 2 and chordoma in 1 case. Six tumors were classified as cystic and 12 as solid. The mean suprasellar extension was 15.26 mm (sd ± 4.45 mm). Preoperative and postoperative
SC
SSS test mean value were respectively 9.11 and 8.72 (not significant: p=0.274). In only one case (5%) the difference between pre- and postoperative SSS was ≥ 3 (reduction of 5 points). At the
M AN U
subjective evaluation, no patient stated a deficit in smelling.
The case with postoperative olfactory deficit was subjected to further analysis in an attempt to identify factors that could correlate to the outcome. It was a solid tumor and a clear difference of the suprasellar extension was found: the extension was 20 mm versus a mean value of 14.98 mm
EP
AC C
Discussion
TE D
of the cases with favorable olfactory outcome.
Various transcranial surgical routes have been proposed for the treatment of suprasellar region tumors such as pterional, bifrontal and frontolateral craniotomy
20,25
. This last approach has the
advantage, in comparison with the classic pterional, to be less traumatic for the temporal muscle avoiding the risk of postoperative facial asymmetry and masticatory dysfunction 30. It requires a shorter skin incision, related to lower risk of injury to the frontotemporal branch of the facial nerve
2,29
. Still, it provides sufficient exposure of the sellar and supra-/ parasellar regions
25
.
Bifrontal craniotomy has also been described in the past as an option to reach this area. This
6
ACCEPTED MANUSCRIPT
approach may lead to major complications due to the ligation of superior sagittal sinus such as venous infarction and bifrontal edema 21 or minor complications due to the opening of the frontal sinus. Therefore, during the last years its use in our institution has been very limited. A less invasive alternative is the basal interhemispheric approach which allows to reach the lesion from
RI PT
different angles. Drawbacks of this route are opening of the frontal sinus and the risk of venous complications.
Previous researches have addressed the problem of postoperative anosmia in anterior skull base
SC
surgery 8,18. The percentage of deficit using pterional craniotomy, mainly for aneurysm surgery, reaches up to 31.8% of the cases in the published literature 1,11,18,19,26. The studies on the bifrontal 12,13,18 7
M AN U
interhemispheric approach report even higher anosmia rate
. Due to this high number of
postoperative olfactory deficit using the above-mentioned approaches many methods have been proposed to preserve the nerve including its dissection 22, reinforcement with fibrin glue 9 or with gelfoam
18
. It is important to notice that previous studies are retrospective without any
TE D
preoperative olfactory testing and don´t use a systematic method for the evaluation of olfactory function. Actually, some of them are based on subjective judgment of the patient
7,18,28
or on
hyposmia.
EP
using a limited number of scents 6, with the risk to underestimate the number of patients having
AC C
The endoscopic endonasal approach has been increasingly utilized for the treatment of sellar and suprasellar lesions, such as pituitary adenomas, craniopharyngiomas and tuberculum sellae meningiomas. This route has the advantage to avoid craniotomy and brain manipulation, allowing - in selected cases- the complete removal of the lesion with minimal morbidity 3. On the other hand recent studies have shown a high rates of postoperative cerebrospinal fluid leak and anosmia 3 after endonasal approach compared to the transcranial route, which is probably due to the surgical trauma to the nasal structures, including the mucosa of nasal septum, medial side of the superior turbinate and the anterior wall of the sphenoid sinus 16-18,27. The goal of our paper
7
ACCEPTED MANUSCRIPT
is not to directly compare frontolateral and other approaches, but to prove if the frontolateral approach allows for olfactory preservation. Our experience using the minimal invasive frontolateral approach shows a high rate of postoperative preservation of the olfactory function. As explained above at surgery the nerve is not protected with any material.
RI PT
Nevertheless, the deficit rate is only 5% (1 patient) and is thus much lower than the rate reported in the literature using alternative approaches, despite the nerves' dissection or the application of nerve reinforcement techniques. Moreover, the single patient with hyposmia in our study group
SC
did not report any subjective worsening of the olfaction- the deficit was revealed only at the postoperative SSS test.
M AN U
The improvement of olfactory outcome necessitates evaluation of the possible risk factors correlating to postoperative hypo-/anosmia. One previous study regarding aneurysm surgery showed that larger size and location (anterior cerebral and anterior communicating artery) of the aneurysm are risk factor for postoperative olfactory deficit after clipping via pterional approach . In our series we analyzed two possible tumor-related factors influencing the olfactory
TE D
19,23
outcome: suprasellar extension and consistency of the lesion. Interestingly, we observed that the mean suprasellar tumor extension in the case with postoperative deficit of the smell is higher
EP
than the other patients. Furthermore the patient with postoperative hyposmia had a large calcified
AC C
meningioma with significant bilateral extension and the surgical corridor crossed the midline. The small numbers do not allow statistical evaluation of the predictive value of these tumor characteristics. It has been reported in the literature that the postoperative olfactory deficit rate in patients harboring cerebral aneurysms is higher if treated if the midline is crossed using a contralateral approach 20. Three mechanism of olfactory nerve damage have been postulated 5: avulsion from the cribriform plate, injury during dissection and vascular damage due to pressure or tearing of the nerve (i.e. retractor). Our surgical concept, after exposing the tumor through frontolateral
8
ACCEPTED MANUSCRIPT
approach, is to perform sufficient enucleation and only after this step starting tumor dissection from the surrounding structures. We avoid going around the tumor before sufficient debulking, which even in cases of large tumors obviate the need of significant retraction.
RI PT
Conclusion
The frontolateral craniotomy is a minimal invasive route to treat suprasellar tumors and has a
SC
low approach-related morbidity. It allows tumor resection with very low risk for the olfactory
M AN U
function. A risk factor for postoperative olfactory deficit could be significant brain retraction
References
1.
Aydin IH, Kadioglu HH, Tuzun Y, Kayaoglu CR, Takci E, Ozturk M: Postoperative anosmia after anterior communicating artery aneurysms surgery by the pterional
2.
TE D
approach. Minim Invasive Neurosurg 39:71-73, 1996
Aydin IH, Takci E, Kadioglu HH, Kayaoglu CR, Tuzun Y: Pitfalls in the pterional approach to the parasellar area (review). Minim Invasive Neurosurg 38:146-152, 1995
3.
Bander ED, Singh H, Ogilvie CB, Cusic RC, Pisapia DJ, Tsiouris AJ, et al: Endoscopic
EP
endonasal versus transcranial approach to tuberculum sellae and planum sphenoidale meningiomas in a similar cohort of patients. J Neurosurg:1-9, 2017 Browne JD, Mims JW: Preservation of olfaction in anterior skull base surgery.
AC C
4.
Laryngoscope 110:1317-1322, 2000 5.
Cardali S, Romano A, Angileri FF, Conti A, La Torre D, de Divitiis O, et al: Microsurgical anatomic features of the olfactory nerve: relevance to olfaction preservation in the pterional approach. Neurosurgery 57:17-21; discussion 17-21, 2005
6.
Cho H, Jo KI, Yeon JY, Hong SC, Kim JS: Feasibility and Efficacy of Olfactory Protection Using Gelfoam and Fibrin Glue during Anterior Communicating Artery Aneurysm Surgery. J Korean Neurosurg Soc 58:107-111, 2015
7.
Curey S, Derrey S, Hannequin P, Hannequin D, Freger P, Muraine M, et al: Validation of the superior interhemispheric approach for tuberculum sellae meningioma: clinical article. J Neurosurg 117:1013-1021, 2012
9
ACCEPTED MANUSCRIPT 8.
Dare AO, Balos LL, Grand W: Olfaction preservation in anterior cranial base approaches: an anatomic study. Neurosurgery 48:1142-1145; discussion 1145-1146, 2001
9.
Dehdashti AR, de Tribolet N: Frontobasal interhemispheric trans-lamina terminalis approach for suprasellar lesions. Neurosurgery 56:418-424; discussion 418-424, 2005 Eibenstein A, Fioretti AB, Lena C, Rosati N, Ottaviano I, Fusetti M: Olfactory screening
RI PT
10.
test: experience in 102 Italian subjects. Acta Otorhinolaryngol Ital 25:18-22, 2005 11.
Eriksen KD, Boge-Rasmussen T, Kruse-Larsen C: Anosmia following operation for cerebral aneurysms in the anterior circulation. J Neurosurg 72:864-865, 1990
Fujiwara H, Yasui N, Nathal-Vera E, Suzuki A: Anosmia after anterior communicating
SC
12.
artery aneurysm surgery: comparison between the anterior interhemispheric and basal interhemispheric approaches. Neurosurgery 38:325-328, 1996
Ganna A, Dehdashti AR, Karabatsou K, Gentili F: Fronto-basal interhemispheric
M AN U
13.
approach for tuberculum sellae meningiomas; long-term visual outcome. Br J Neurosurg 23:422-430, 2009 14.
Hummel T, Konnerth CG, Rosenheim K, Kobal G: Screening of olfactory function with a four-minute odor identification test: reliability, normative data, and investigations in
15.
TE D
patients with olfactory loss. Ann Otol Rhinol Laryngol 110:976-981, 2001 Hummel T, Sekinger B, Wolf SR, Pauli E, Kobal G: 'Sniffin' sticks': olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chem Senses 22:39-52, 1997 Kim BY, Kang SG, Kim SW, Hong YK, Jeun SS, Kim SW, et al: Olfactory changes after
EP
16.
endoscopic endonasal transsphenoidal approach for skull base tumors. Laryngoscope
17.
AC C
124:2470-2475, 2014
Kim DH, Hong YK, Jeun SS, Park JS, Lim DJ, Kim SW, et al: Endoscopic Endonasal Transsphenoidal Approach From the Otolaryngologist Point of View. J Craniofac Surg, 2017
18.
Matano F, Murai Y, Mizunari T, Tateyama K, Kobayashi S, Adachi K, et al: Olfactory preservation during anterior interhemispheric approach for anterior skull base lesions: technical note. Neurosurg Rev 39:63-68; discussion 69, 2016
19.
Moman MR, Verweij BH, Buwalda J, Rinkel GJ: Anosmia after endovascular and open surgical treatment of intracranial aneurysms. J Neurosurg 110:482-486, 2009
10
ACCEPTED MANUSCRIPT 20.
Nakamura M, Roser F, Struck M, Vorkapic P, Samii M: Tuberculum sellae meningiomas: clinical outcome considering different surgical approaches. Neurosurgery 59:1019-1028; discussion 1028-1019, 2006
21.
Nakamura M, Struck M, Roser F, Vorkapic P, Samii M: Olfactory groove meningiomas: clinical outcome and recurrence rates after tumor removal through the frontolateral and
22.
RI PT
bifrontal approach. Neurosurgery 60:844-852; discussion 844-852, 2007 Nakayama H, Ishikawa T, Yamashita S, Fukui I, Mutoh T, Hikichi K, et al: [CSF leakage and anosmia in aneurysm clipping of anterior communicating artery by basal interhemispheric approach]. No Shinkei Geka 39:263-268, 2011
Park J, Lee SH, Kang DH, Kim JS: Olfactory dysfunction after ipsilateral and
SC
23.
contralateral pterional approaches for cerebral aneurysms. Neurosurgery 65:727-732; discussion 732, 2009
Philpott CM, Boak D: The impact of olfactory disorders in the United kingdom. Chem Senses 39:711-718, 2014
25.
M AN U
24.
Salma A, Alkandari A, Sammet S, Ammirati M: Lateral supraorbital approach vs pterional approach: an anatomic qualitative and quantitative evaluation. Neurosurgery 68:364-372; discussion 371-362, 2011
Suzuki J, Yoshimoto T, Mizoi K: Preservation of the olfactory tract in bifrontal
TE D
26.
craniotomy for anterior communicating artery aneurysms, and the functional prognosis. J Neurosurg 54:342-345, 1981 27.
Wang S, Chen Y, Li J, Wei L, Wang R: Olfactory function and quality of life following
2015
Wermer MJ, Donswijk M, Greebe P, Verweij BH, Rinkel GJ: Anosmia after aneurysmal
AC C
28.
EP
microscopic endonasal transsphenoidal pituitary surgery. Medicine (Baltimore) 94:e465,
subarachnoid hemorrhage. Neurosurgery 61:918-922; discussion 922-913, 2007 29.
Yasargil MG, Reichman MV, Kubik S: Preservation of the frontotemporal branch of the facial nerve using the interfascial temporalis flap for pterional craniotomy. Technical article. J Neurosurg 67:463-466, 1987
30.
Yasuda CL, Costa AL, Franca M, Jr., Pereira FR, Tedeschi H, de Oliveira E, et al: Postcraniotomy temporalis muscle atrophy: a clinical, magnetic resonance imaging volumetry and electromyographic investigation. J Orofac Pain 24:391-397, 2010
11
SC
RI PT
ACCEPTED MANUSCRIPT
M AN U
Legends
Figure 1. A: image showing the performed right frontolateral craniotomy before the dura incision. The size of bone flap is ca. 30x25 mm and the cranial base is flattened with a
TE D
diamond drill in order to have a not-obstructed basal view to the area of interest. B: The dura is incised in a semicircular shape and the drainage of CSF is obtained by creating a small
AC C
EP
opening of the Sylvain cistern.
ACCEPTED MANUSCRIPT Table 1: Patient´s population including characteristics of the lesion and the values of preoperative and postoperative “Sniffin´ Sticks” screening (SSS) test.
16,4 24,6 15,1 9,7 11,9 14 17,1 12,3 15 16 19,5 13,5 20 10,3 14,6 7 22,7 15
SSS Preoperative
SSS Postoperative
10 2 10 8 10 9 11 9 12 12 9 7 12 9 10 8 5 11
10 4 10 7 10 9 10 10 11 12 9 6 7 10 10 8 3 11
RI PT
Solid Cystic Cystic Solid Solid Solid Solid Cystic Solid Cystic Cystic Solid Solid Solid Solid Solid Solid Cystic
Suprasellar tumor extension (mm)
SC
Meningioma Craniopharyngioma Craniopharyngioma Pituitary Adenoma Chordoma Meningioma Meningioma Craniopharyngioma Craniopharyngioma Craniopharyngioma Craniopharyngioma Craniopharyngioma Meningioma Meningioma Craniopharyngioma Meningioma Pituitary Adenoma Craniopharyngioma
TE D
63 43 16 27 48 35 37 44 23 66 19 19 50 49 56 29 76 55
Consistency
EP
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
Histology
M AN U
AGE
AC C
Case
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
ACCEPTED MANUSCRIPT Highlights • •
AC C
EP
TE D
M AN U
SC
RI PT
•
We present the findings of our prospective study assessing olfactory function outcome in patients undergoing frontolateral approach The olfactory outcome was correlated to the following variables: tumor type, size, consistency and extent of vertical and lateral growth In only one case (5%) the difference between pre- and postoperative olfactory function was evident at testing
ACCEPTED MANUSCRIPT Abbreviations
“Sniffin´ Sticks” screening (SSS) magnetic resonance imaging (MRI)
AC C
EP
TE D
M AN U
SC
RI PT
Cerebrospinal fluid (CSF)
INI INTERNATIONAL NEUROSCIENCE INSTITUTE Präsident: Prof. Dr. med. Dr. h. c. mult. M. Samii
RI PT
ACCEPTED MANUSCRIPT
Please find enclosed our manuscript entitled:
SC
Hannover 05.2.2018
M AN U
Evaluation of the olfactory outcome after frontolateral approach for the treatment of suprasellar tumors
that we would like to submit to WORLD OF NEUROSURGERY for consideration of publication.
The authors have no personal financial or institutional interest in any of the
EP
Yours sincerely,
TE D
drugs, materials, or devices described in this article.
....................................
AC C
Mario Giordano MD
S1878-8750(18)30613-2
DOI:
10.1016/j.wneu.2018.03.131
Reference:
WNEU 7743
To appear in:
World Neurosurgery
Received Date: 5 February 2018 Revised Date:
18 March 2018
Accepted Date: 19 March 2018
Please cite this article as: Giordano M, Gerganov VM, Gallieni M, Samii A, Samii M, Title: Evaluation of the olfactory outcome after frontolateral approach for the treatment of suprasellar tumors, World Neurosurgery (2018), doi: 10.1016/j.wneu.2018.03.131. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
1
ACCEPTED MANUSCRIPT
Title: Evaluation of the olfactory outcome after frontolateral approach for the treatment of suprasellar tumors
•
Gerganov, Venelin M., MD 1
•
Gallieni, Massimo, MD 1
•
Samii, Amir, MD, PhD; Prof. 1,2
•
Samii, Madjid, MD, PhD; Prof. 1
International Neuroscience Institute; Department of neurosurgery, Rudolf Pichlmayr Str. 4,
Hannover 30625, Germany 2
SC
Giordano, Mario, MD 1
M AN U
1
•
RI PT
Authors:
Leibniz Institute for Neurobiology, Brenneckestrasse 6, Magdeburg 39118, Germany
TE D
Corresponding author:
Giordano, Mario, MD; International Neuroscience Institute- Hannover, Germany Address: International Neuroscience Institute- Hannover, Rudolf Pichlmayr Str. 4, Hannover 30625, Germany
EP
Phone: ++49 (511) 27092865 Fax: ++49 (511) 27092706
AC C
E-mail address: [email protected]
Key words: Olfactory nerve, frontolateral approach, suprasellar tumor Running head: Olfactory outcome after frontolateral approach No financial and/or material support The paper has not been presented (nor published) previously
2
ACCEPTED MANUSCRIPT
Introduction
In modern neurosurgery the preservation of patient´s neurological status and quality of life has
RI PT
become mandatory. Olfaction has received less attention in comparison to other fundamental senses such as vision and hearing. However, sense of smell has an important impact on patient´s everyday life: its deficit may lead to decreased appreciation of food, exposure to dangers (gas)
24
. Common pathological conditions, such as nasal, endocrine and
neurodegenerative disorders
10
, may lead to olfactory dysfunction that can be also iatrogenic
M AN U
normal population
SC
and difficulty in personal relationship leading to a higher depression rate in comparison with the
consequent to extensive transcranial 4,8,11,18,19,26 or transnasal 3 surgical approaches to the anterior skull base.
One of the most frequently used approaches to the anterior skull base and the supra-/ parasellar
TE D
area in the recent years is the frontolateral. The risk for olfactory nerve damage, related to the approach, however, has not been systematically evaluated. In the manuscript, we present the findings of our prospectively designed and performed study, assessing olfactory function
AC C
EP
outcome in patients undergoing frontolateral approach for the resection of suprasellar lesions.
Material and methods
Eighteen consecutive non-randomized patients (7 females, 11 males) surgically treated at our Institute for suprasellar tumors were included in this prospective study. Lesions extending to the anterior skull base reaching directly the olfactory nerve were excluded. The mean age of the
3
ACCEPTED MANUSCRIPT
patients was 42 years (range 16-76 years). Exclusion criteria were: history of previous cranial surgery, radiotherapy or severe head trauma. Based on imaging and intraoperative findings every lesion was classified as cystic or solid. Maximal suprasellar (vertical) extension was calculated using the preoperative magnetic resonance imaging (MRI) scan on a plane perpendicular to the
RI PT
anterior skull base.
Olfactory function was evaluated at the admission and 14 days after the surgery using the standard 12-items “Sniffin´ Sticks” screening (SSS) test (Burghart Messtechnik, Wedel 14,15
. The test involves the presentation of 12 odorants in felt-tip pens. The pens
SC
Germany)
tampon is filled with different dissolved odorants. During the test, the pen cap is removed and
M AN U
presented to the patient for 3 seconds at a distance of 2 cm in front of the nostril. On a multiple choice task the identification of the odorants was done from a list of 4 for each pen. The interval between pens presentation was ca. 20 seconds. Both nostril were examined in all the subjects and the better nostril result was considered 14. The test result has a range from a minimum of 0 to a
TE D
maximum of 12. A difference between preoperative and postoperative value ≥ 3 was considered hyposmia. A patient with postoperative value of 0 was classified as anosmic. A subjective evaluation of the olfactory function was also performed before the administration of the
EP
postoperative SSS asking to the patient if a difference in smelling
AC C
The olfactory outcome was correlated to the following variables: tumor type, size, consistency and extent of vertical and lateral growth. Commercially available software (IBM SPSS Statistics for Mac, Version 23.0. Armonk, NY: IBM Corp) was used for data analysis. Descriptive statistic and t-test were performed with a significance ascribed in case of error probability of p<0.05.
Operative technique
4
ACCEPTED MANUSCRIPT
The frontolateral approach could be regarded as a modification of the frontotemporal approach, including only its frontal part or as a less invasive version of the unilateral subfrontal approach. The head of the patient is fixed with the Mayfield clamp, rotated slightly to the contralateral side and hyperextended so that the zygoma becomes be the highest point in the sagittal plane.
RI PT
Thus, due to gravity, less retraction of the frontal lobes is required. The skin incision is done behind the hairline, starting anterior to the tragus and reaching the midline. In bold patients, we prefer to place the incision at a skin crease in the forehead. Laterally a single burr hole is
SC
made at the key point and the craniotomy is performed with the craniotome. The size of the craniotomy is usually 25 to 35 mm in width and 20 to 25 mm in height; however, it extent is
M AN U
modified according to the size of the frontal sinus. The craniotomy should reach the supraorbital notch frontomedially preserving the supraorbital nerve. An attempt to avoid opening of the sinus is always made, unless it is very large. In case of opening, the mucosa is removed, the sinus is then treated with antiseptic solution and at the end isolated with
TE D
pericranial flap. The cranial base is flattened with a diamond drill in order to have a notobstructed basal view to the area of interest.
The dura is incised in a semicircular manner with an inferior base. The crucial step is the
EP
drainage of sufficient amount of CSF by creating a small opening of the Sylvain cistern. In
AC C
case of intrasellar extension of the tumor the tuberculum sellae is drilled off allowing to reach that portion. The application of angled endoscope may be useful in such cases. The frontal lobe has just to be held with a single self-retaining retractor. Importantly, the retractor should be placed along the olfactory nerve without crossing it to avoid pressure, exerting only moderate controlled traction of this nerve. In most cases there is no need of olfactory nerve dissection. If the nerve looks under tension, however, sharp dissection is performed, preserving its vascular supply. During tumor removal care is taken not to injure unintentionally the nerve or to cause its iatrogenic damage with the bipolar coagulation.
5
ACCEPTED MANUSCRIPT
Results
All patients underwent tumor removal via the frontolateral approach: 16 on the right and 2 on the
RI PT
left side. The histological diagnosis was: craniopharyngioma in 9 (Figure 1 A,B), meningioma in 6, adenoma in 2 and chordoma in 1 case. Six tumors were classified as cystic and 12 as solid. The mean suprasellar extension was 15.26 mm (sd ± 4.45 mm). Preoperative and postoperative
SC
SSS test mean value were respectively 9.11 and 8.72 (not significant: p=0.274). In only one case (5%) the difference between pre- and postoperative SSS was ≥ 3 (reduction of 5 points). At the
M AN U
subjective evaluation, no patient stated a deficit in smelling.
The case with postoperative olfactory deficit was subjected to further analysis in an attempt to identify factors that could correlate to the outcome. It was a solid tumor and a clear difference of the suprasellar extension was found: the extension was 20 mm versus a mean value of 14.98 mm
EP
AC C
Discussion
TE D
of the cases with favorable olfactory outcome.
Various transcranial surgical routes have been proposed for the treatment of suprasellar region tumors such as pterional, bifrontal and frontolateral craniotomy
20,25
. This last approach has the
advantage, in comparison with the classic pterional, to be less traumatic for the temporal muscle avoiding the risk of postoperative facial asymmetry and masticatory dysfunction 30. It requires a shorter skin incision, related to lower risk of injury to the frontotemporal branch of the facial nerve
2,29
. Still, it provides sufficient exposure of the sellar and supra-/ parasellar regions
25
.
Bifrontal craniotomy has also been described in the past as an option to reach this area. This
6
ACCEPTED MANUSCRIPT
approach may lead to major complications due to the ligation of superior sagittal sinus such as venous infarction and bifrontal edema 21 or minor complications due to the opening of the frontal sinus. Therefore, during the last years its use in our institution has been very limited. A less invasive alternative is the basal interhemispheric approach which allows to reach the lesion from
RI PT
different angles. Drawbacks of this route are opening of the frontal sinus and the risk of venous complications.
Previous researches have addressed the problem of postoperative anosmia in anterior skull base
SC
surgery 8,18. The percentage of deficit using pterional craniotomy, mainly for aneurysm surgery, reaches up to 31.8% of the cases in the published literature 1,11,18,19,26. The studies on the bifrontal 12,13,18 7
M AN U
interhemispheric approach report even higher anosmia rate
. Due to this high number of
postoperative olfactory deficit using the above-mentioned approaches many methods have been proposed to preserve the nerve including its dissection 22, reinforcement with fibrin glue 9 or with gelfoam
18
. It is important to notice that previous studies are retrospective without any
TE D
preoperative olfactory testing and don´t use a systematic method for the evaluation of olfactory function. Actually, some of them are based on subjective judgment of the patient
7,18,28
or on
hyposmia.
EP
using a limited number of scents 6, with the risk to underestimate the number of patients having
AC C
The endoscopic endonasal approach has been increasingly utilized for the treatment of sellar and suprasellar lesions, such as pituitary adenomas, craniopharyngiomas and tuberculum sellae meningiomas. This route has the advantage to avoid craniotomy and brain manipulation, allowing - in selected cases- the complete removal of the lesion with minimal morbidity 3. On the other hand recent studies have shown a high rates of postoperative cerebrospinal fluid leak and anosmia 3 after endonasal approach compared to the transcranial route, which is probably due to the surgical trauma to the nasal structures, including the mucosa of nasal septum, medial side of the superior turbinate and the anterior wall of the sphenoid sinus 16-18,27. The goal of our paper
7
ACCEPTED MANUSCRIPT
is not to directly compare frontolateral and other approaches, but to prove if the frontolateral approach allows for olfactory preservation. Our experience using the minimal invasive frontolateral approach shows a high rate of postoperative preservation of the olfactory function. As explained above at surgery the nerve is not protected with any material.
RI PT
Nevertheless, the deficit rate is only 5% (1 patient) and is thus much lower than the rate reported in the literature using alternative approaches, despite the nerves' dissection or the application of nerve reinforcement techniques. Moreover, the single patient with hyposmia in our study group
SC
did not report any subjective worsening of the olfaction- the deficit was revealed only at the postoperative SSS test.
M AN U
The improvement of olfactory outcome necessitates evaluation of the possible risk factors correlating to postoperative hypo-/anosmia. One previous study regarding aneurysm surgery showed that larger size and location (anterior cerebral and anterior communicating artery) of the aneurysm are risk factor for postoperative olfactory deficit after clipping via pterional approach . In our series we analyzed two possible tumor-related factors influencing the olfactory
TE D
19,23
outcome: suprasellar extension and consistency of the lesion. Interestingly, we observed that the mean suprasellar tumor extension in the case with postoperative deficit of the smell is higher
EP
than the other patients. Furthermore the patient with postoperative hyposmia had a large calcified
AC C
meningioma with significant bilateral extension and the surgical corridor crossed the midline. The small numbers do not allow statistical evaluation of the predictive value of these tumor characteristics. It has been reported in the literature that the postoperative olfactory deficit rate in patients harboring cerebral aneurysms is higher if treated if the midline is crossed using a contralateral approach 20. Three mechanism of olfactory nerve damage have been postulated 5: avulsion from the cribriform plate, injury during dissection and vascular damage due to pressure or tearing of the nerve (i.e. retractor). Our surgical concept, after exposing the tumor through frontolateral
8
ACCEPTED MANUSCRIPT
approach, is to perform sufficient enucleation and only after this step starting tumor dissection from the surrounding structures. We avoid going around the tumor before sufficient debulking, which even in cases of large tumors obviate the need of significant retraction.
RI PT
Conclusion
The frontolateral craniotomy is a minimal invasive route to treat suprasellar tumors and has a
SC
low approach-related morbidity. It allows tumor resection with very low risk for the olfactory
M AN U
function. A risk factor for postoperative olfactory deficit could be significant brain retraction
References
1.
Aydin IH, Kadioglu HH, Tuzun Y, Kayaoglu CR, Takci E, Ozturk M: Postoperative anosmia after anterior communicating artery aneurysms surgery by the pterional
2.
TE D
approach. Minim Invasive Neurosurg 39:71-73, 1996
Aydin IH, Takci E, Kadioglu HH, Kayaoglu CR, Tuzun Y: Pitfalls in the pterional approach to the parasellar area (review). Minim Invasive Neurosurg 38:146-152, 1995
3.
Bander ED, Singh H, Ogilvie CB, Cusic RC, Pisapia DJ, Tsiouris AJ, et al: Endoscopic
EP
endonasal versus transcranial approach to tuberculum sellae and planum sphenoidale meningiomas in a similar cohort of patients. J Neurosurg:1-9, 2017 Browne JD, Mims JW: Preservation of olfaction in anterior skull base surgery.
AC C
4.
Laryngoscope 110:1317-1322, 2000 5.
Cardali S, Romano A, Angileri FF, Conti A, La Torre D, de Divitiis O, et al: Microsurgical anatomic features of the olfactory nerve: relevance to olfaction preservation in the pterional approach. Neurosurgery 57:17-21; discussion 17-21, 2005
6.
Cho H, Jo KI, Yeon JY, Hong SC, Kim JS: Feasibility and Efficacy of Olfactory Protection Using Gelfoam and Fibrin Glue during Anterior Communicating Artery Aneurysm Surgery. J Korean Neurosurg Soc 58:107-111, 2015
7.
Curey S, Derrey S, Hannequin P, Hannequin D, Freger P, Muraine M, et al: Validation of the superior interhemispheric approach for tuberculum sellae meningioma: clinical article. J Neurosurg 117:1013-1021, 2012
9
ACCEPTED MANUSCRIPT 8.
Dare AO, Balos LL, Grand W: Olfaction preservation in anterior cranial base approaches: an anatomic study. Neurosurgery 48:1142-1145; discussion 1145-1146, 2001
9.
Dehdashti AR, de Tribolet N: Frontobasal interhemispheric trans-lamina terminalis approach for suprasellar lesions. Neurosurgery 56:418-424; discussion 418-424, 2005 Eibenstein A, Fioretti AB, Lena C, Rosati N, Ottaviano I, Fusetti M: Olfactory screening
RI PT
10.
test: experience in 102 Italian subjects. Acta Otorhinolaryngol Ital 25:18-22, 2005 11.
Eriksen KD, Boge-Rasmussen T, Kruse-Larsen C: Anosmia following operation for cerebral aneurysms in the anterior circulation. J Neurosurg 72:864-865, 1990
Fujiwara H, Yasui N, Nathal-Vera E, Suzuki A: Anosmia after anterior communicating
SC
12.
artery aneurysm surgery: comparison between the anterior interhemispheric and basal interhemispheric approaches. Neurosurgery 38:325-328, 1996
Ganna A, Dehdashti AR, Karabatsou K, Gentili F: Fronto-basal interhemispheric
M AN U
13.
approach for tuberculum sellae meningiomas; long-term visual outcome. Br J Neurosurg 23:422-430, 2009 14.
Hummel T, Konnerth CG, Rosenheim K, Kobal G: Screening of olfactory function with a four-minute odor identification test: reliability, normative data, and investigations in
15.
TE D
patients with olfactory loss. Ann Otol Rhinol Laryngol 110:976-981, 2001 Hummel T, Sekinger B, Wolf SR, Pauli E, Kobal G: 'Sniffin' sticks': olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chem Senses 22:39-52, 1997 Kim BY, Kang SG, Kim SW, Hong YK, Jeun SS, Kim SW, et al: Olfactory changes after
EP
16.
endoscopic endonasal transsphenoidal approach for skull base tumors. Laryngoscope
17.
AC C
124:2470-2475, 2014
Kim DH, Hong YK, Jeun SS, Park JS, Lim DJ, Kim SW, et al: Endoscopic Endonasal Transsphenoidal Approach From the Otolaryngologist Point of View. J Craniofac Surg, 2017
18.
Matano F, Murai Y, Mizunari T, Tateyama K, Kobayashi S, Adachi K, et al: Olfactory preservation during anterior interhemispheric approach for anterior skull base lesions: technical note. Neurosurg Rev 39:63-68; discussion 69, 2016
19.
Moman MR, Verweij BH, Buwalda J, Rinkel GJ: Anosmia after endovascular and open surgical treatment of intracranial aneurysms. J Neurosurg 110:482-486, 2009
10
ACCEPTED MANUSCRIPT 20.
Nakamura M, Roser F, Struck M, Vorkapic P, Samii M: Tuberculum sellae meningiomas: clinical outcome considering different surgical approaches. Neurosurgery 59:1019-1028; discussion 1028-1019, 2006
21.
Nakamura M, Struck M, Roser F, Vorkapic P, Samii M: Olfactory groove meningiomas: clinical outcome and recurrence rates after tumor removal through the frontolateral and
22.
RI PT
bifrontal approach. Neurosurgery 60:844-852; discussion 844-852, 2007 Nakayama H, Ishikawa T, Yamashita S, Fukui I, Mutoh T, Hikichi K, et al: [CSF leakage and anosmia in aneurysm clipping of anterior communicating artery by basal interhemispheric approach]. No Shinkei Geka 39:263-268, 2011
Park J, Lee SH, Kang DH, Kim JS: Olfactory dysfunction after ipsilateral and
SC
23.
contralateral pterional approaches for cerebral aneurysms. Neurosurgery 65:727-732; discussion 732, 2009
Philpott CM, Boak D: The impact of olfactory disorders in the United kingdom. Chem Senses 39:711-718, 2014
25.
M AN U
24.
Salma A, Alkandari A, Sammet S, Ammirati M: Lateral supraorbital approach vs pterional approach: an anatomic qualitative and quantitative evaluation. Neurosurgery 68:364-372; discussion 371-362, 2011
Suzuki J, Yoshimoto T, Mizoi K: Preservation of the olfactory tract in bifrontal
TE D
26.
craniotomy for anterior communicating artery aneurysms, and the functional prognosis. J Neurosurg 54:342-345, 1981 27.
Wang S, Chen Y, Li J, Wei L, Wang R: Olfactory function and quality of life following
2015
Wermer MJ, Donswijk M, Greebe P, Verweij BH, Rinkel GJ: Anosmia after aneurysmal
AC C
28.
EP
microscopic endonasal transsphenoidal pituitary surgery. Medicine (Baltimore) 94:e465,
subarachnoid hemorrhage. Neurosurgery 61:918-922; discussion 922-913, 2007 29.
Yasargil MG, Reichman MV, Kubik S: Preservation of the frontotemporal branch of the facial nerve using the interfascial temporalis flap for pterional craniotomy. Technical article. J Neurosurg 67:463-466, 1987
30.
Yasuda CL, Costa AL, Franca M, Jr., Pereira FR, Tedeschi H, de Oliveira E, et al: Postcraniotomy temporalis muscle atrophy: a clinical, magnetic resonance imaging volumetry and electromyographic investigation. J Orofac Pain 24:391-397, 2010
11
SC
RI PT
ACCEPTED MANUSCRIPT
M AN U
Legends
Figure 1. A: image showing the performed right frontolateral craniotomy before the dura incision. The size of bone flap is ca. 30x25 mm and the cranial base is flattened with a
TE D
diamond drill in order to have a not-obstructed basal view to the area of interest. B: The dura is incised in a semicircular shape and the drainage of CSF is obtained by creating a small
AC C
EP
opening of the Sylvain cistern.
ACCEPTED MANUSCRIPT Table 1: Patient´s population including characteristics of the lesion and the values of preoperative and postoperative “Sniffin´ Sticks” screening (SSS) test.
16,4 24,6 15,1 9,7 11,9 14 17,1 12,3 15 16 19,5 13,5 20 10,3 14,6 7 22,7 15
SSS Preoperative
SSS Postoperative
10 2 10 8 10 9 11 9 12 12 9 7 12 9 10 8 5 11
10 4 10 7 10 9 10 10 11 12 9 6 7 10 10 8 3 11
RI PT
Solid Cystic Cystic Solid Solid Solid Solid Cystic Solid Cystic Cystic Solid Solid Solid Solid Solid Solid Cystic
Suprasellar tumor extension (mm)
SC
Meningioma Craniopharyngioma Craniopharyngioma Pituitary Adenoma Chordoma Meningioma Meningioma Craniopharyngioma Craniopharyngioma Craniopharyngioma Craniopharyngioma Craniopharyngioma Meningioma Meningioma Craniopharyngioma Meningioma Pituitary Adenoma Craniopharyngioma
TE D
63 43 16 27 48 35 37 44 23 66 19 19 50 49 56 29 76 55
Consistency
EP
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
Histology
M AN U
AGE
AC C
Case
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
ACCEPTED MANUSCRIPT Highlights • •
AC C
EP
TE D
M AN U
SC
RI PT
•
We present the findings of our prospective study assessing olfactory function outcome in patients undergoing frontolateral approach The olfactory outcome was correlated to the following variables: tumor type, size, consistency and extent of vertical and lateral growth In only one case (5%) the difference between pre- and postoperative olfactory function was evident at testing
ACCEPTED MANUSCRIPT Abbreviations
“Sniffin´ Sticks” screening (SSS) magnetic resonance imaging (MRI)
AC C
EP
TE D
M AN U
SC
RI PT
Cerebrospinal fluid (CSF)
INI INTERNATIONAL NEUROSCIENCE INSTITUTE Präsident: Prof. Dr. med. Dr. h. c. mult. M. Samii
RI PT
ACCEPTED MANUSCRIPT
Please find enclosed our manuscript entitled:
SC
Hannover 05.2.2018
M AN U
Evaluation of the olfactory outcome after frontolateral approach for the treatment of suprasellar tumors
that we would like to submit to WORLD OF NEUROSURGERY for consideration of publication.
The authors have no personal financial or institutional interest in any of the
EP
Yours sincerely,
TE D
drugs, materials, or devices described in this article.
....................................
AC C
Mario Giordano MD