Quantitative Anatomic Study of the Minipterional Craniotomy in the Paraclinoid Region: Benefits of Extradural Anterior Clinoidectomy

Journal Pre-proof Quantitative anatomic study of the minipterional craniotomy in the paraclinoid region: benefits of the extradural anterior clinoidectomy Rafael Martínez-pérez, Thiago Albonette-felicio, Marcus Zachariah, Douglas Hardesty, MD, Ricardo L. Carrau, MD, Daniel M. Prevedello, MD PII:

S1878-8750(19)32960-2

DOI:

https://doi.org/10.1016/j.wneu.2019.11.120

Reference:

WNEU 13789

To appear in:

World Neurosurgery

Received Date: 25 October 2019 Revised Date:

20 November 2019

Accepted Date: 21 November 2019

Please cite this article as: Martínez-pérez R, Albonette-felicio T, Zachariah M, Hardesty D, Carrau RL, Prevedello DM, Quantitative anatomic study of the minipterional craniotomy in the paraclinoid region: benefits of the extradural anterior clinoidectomy, World Neurosurgery (2019), doi: https:// doi.org/10.1016/j.wneu.2019.11.120. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. 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. © 2019 Elsevier Inc. All rights reserved.

Quantitative anatomic study of the minipterional craniotomy in the paraclinoid region: benefits of the extradural anterior clinoidectomy

Rafael MARTÍNEZ-PÉREZ1, Thiago ALBONETTE-FELICIO1, Marcus ZACHARIAH1, Douglas HARDESTY MD1,2, Ricardo L. CARRAU MD1,2, Daniel M. PREVEDELLO MD1,2 1

Department of Neurological Surgery, The Ohio State University, Wexner Medical Center, Columbus, Ohio, United States, 2Department of Otolaryngology–Head and Neck Surgery, The Ohio State University, Wexner Medical Center Columbus, Ohio, United States, Corresponding and submitting Author’s name and current institution: Rafael Martinez-Perez, M.D., Ph.D., Department of Neurological Surgery, The Ohio State University, Wexner Medical Center, 410 W. 10th Ave., N-1049 Doan Hall, Columbus, OH 43210. Post publication Corresponding Author’s name and current institution: Daniel M. Prevedello, M.D., Department of Neurological Surgery, The Ohio State University, Wexner Medical Center, 410 W. 10th Ave., N-1049 Doan Hall, Columbus, OH 43210.

Keywords: Craniopharingioma; tuberculum sellae; meningioma; cerebral aneurysms; ophthalmic artery; carotid-ophthalmic; minimally invasive; key-hole Running head: Anterior clinoidectomy in Minipterional Approach Conflict of interest: This study was performed at ALT-VISION at The Ohio State University. This laboratory receives educational support from the following companies: Carl Zeiss Microscopy, Intuitive Surgical Corp., KLS Martin Corp., Karl Storz Endoscopy, Leica Microsystems, Medtronic Corp., Stryker Corp., and Vycor Medical. Daniel M. Prevedello is a consultant for Stryker Corporation and Medtronic Corp. Daniel Prevedello has equity on 3 rivers LLC, eLUM Technologies, LLC and Soliton LLC. Daniel Prevedello receives royalties from KLS-Martin and Mizuho. Ricardo L. Carrau is a consultant for Medtronic Corp.

Abbreviations: Anterior clinoid process (ACP) extradural anterior clinodectomy (eAC) Internal carotid artery (ICA) minipterional approach and extradural anterior clinoidectomy combination (MPT + eAC) Ophthalmic artery (OphA) posterior communicating artery (PComA) standard minipterional approach (MPT)

1 2 3

Manuscript

4

Abstract

5 6

Background: The extradural anterior clinoidectomy via minipterional craniotomy (MPT

7

+ eAC) has been recently introduced in the neurosurgical armamentarium to improve

8

access to anterior and middle fossa skull base structures via a minimally invasive

9

approach. However, the effect of extradural clinoidectomy on surgical exposure in the

10

minipterional approach

has not been evaluated. Moreover, the impact of eAC on

11

surgical maneuverability has not been established for either traditional pterional or

12

minipterional craniotomies.

13

Objective: We sought to illustrate the microsurgical anatomy of the MPT + eAC and to

14

evaluate the effect of eAC on surgical exposure and maneuverability.

15

Methods: Area of exposure, area of surgical freedom, and maneuverability score

16

provided by the MPT and MPT + eAC were compared in 5 cadaveric heads.

17

Results: In comparison to the MPT, the MPT + eAC enlarges the area of exposure

18

approximately 2-fold (93 vs 184 cm2, p<0.001). All targets considered in the

19

paraclinoid region, including the posterior communicating artery origin, prechiasmatic

20

region, and ophthalmic artery origin showed an increased in surgical freedom and

21

maneuverability after performing an eAC. Targets remote from the clinoid such as the

22

internal carotid bifurcation were not affected.

23

Conclusions: The MPT + eAC offers a larger area of exposure, surgical freedom and

24

maneuverability at the paraclinoid region in this minimally invasive approach.

25 26 27 28 29 30 31 32 33 34 35 36 37 38 1

1 2

Introduction

3 4

Significant interest has been recently invested in the development of minimally

5

invasive techniques to approach anterolateral skull base regions, giving rise to

6

procedures such as the Minipterional Approach (MPT)1,2. The MPT has been shown to

7

achieve adequate exposure of the anterior and middle cranial fossae1,3–6. Compared to

8

the pterional and orbitozygomatic craniotomies, the MPT has been demonstrated to

9

offer better cosmetic results, improved patient comfort, and reduced operative times 7,8.

10 11

Nevertheless, several authors have questioned the applicability of the MPT in the

12

treatment of deep and complex lesions due to the small superficial exposure1,9,10 Despite

13

emerging literature reporting an extended use of minimally invasive approaches for

14

most simple anterior and middle fossa lesions (e.g., simple non-ruptured anterior

15

circulation aneurysms, small parasellar extradural lesions)2–4,8,10–13, only a few groups

16

have described the use of these techniques to approach the paraclinoid region7,11 .

17 18

The extradural anterior clinoidectomy (eAC) is a standard technique that enhances the

19

extradural corridor and provides a broad access to the entire parasellar region, while

20

reducing brain retraction14–18. For these reasons, the eAC has been proposed as an

21

additional step to improve the surgical exposure of the paraclinoid region when using a

22

MPT7,19. Few works have demonstrated the clinical safety and feasibility of performing

23

an eAC throughout a MPT craniotomy (MPT + eAC) to manage lesions around the

24

paraclinoid region from a minimally invasiveness perspective7,20. The impact of the

25

eAC in expanding the surgical corridor and improving the maneuverability around the

26

paraclinoid region has not been properly evaluated, and the current literature lacks a

27

qualitative and quantitative comparative analysis of the surgical anatomy that justify the

28

use of the MPT and its variants. Therefore, we aimed in the present study to

29

quantitatively

30

maneuverability of MPT + eAC versus that of MPT for approaching anatomic targets at

31

the paraclinoid region, as well as to illustrate step-by-step the surgical technique for for

32

MPT + eAC.

analyze

and

compare

the

exposure,

surgical

freedom,

and

33 34 2

1 2

Methods

3 4

Five embalmed human cadaveric heads (10 sides) were injected and prepared for

5

anatomical dissection. Informed consent and ethical approval were not deemed

6

necessary by the local ethics in view of the application of strict patient privacy

7

regulations operating in our center (cadavers were unidentified).

8 9

Prior to dissection, specimens underwent a high-resolution computed

10

tomography scan. The images were uploaded to the iNtellect Cranial Navigation System

11

(Stryker, Kalamazoo, Michigan). Based on surface recognition, cadavers were

12

registered with the BrainLab Curve (Feldkirchen, Germany) for the acquisition of

13

landmark points for the calculation of operative exposure. Surface matching refinement

14

based on bone surface were further performed during the dissection, ensuring a mean

15

deviation lower than 0.5 mm for all specimens.

16 17

The specimens were positioned to simulate the surgical position in the operating

18

room. The MPT craniotomy and eAC were performed combining macroscopic and

19

microscopic visualization with standard craniotomy and microsurgery instruments.

20 21

Technique

22 23

Minipterional Craniotomy (Figure 1): This procedure has been widely described

24

in previous reports1,2,7 and will be briefly explained here. An arcuate skin incision

25

starting at the level of the zygoma, one centimeter anterior to the tragus and directed

26

towards the mid pupillary line was performed. The scalp was retracted anteriorly and an

27

interfascial dissection as described by Yasargil et al. was performed before the

28

temporalis muscle dissection in order to protect the frontal branch of the facial nerve21.

29

The temporalis muscle was then dissected free and pulled downward to expose the

30

pterion and the squamous part of the temporal bone. A burr hole was placed below the

31

superior temporal line and superior to the zygomatic suture. The osteotomy proceeds

32

superiorly and posteriorly along the superior temporal line. Next, the osteotome was

33

directed anteriorly and inferiorly along the sphenoid bone to connect with the initial

3

1

burr hole. Once the craniotomy was performed, the sphenoid ridge was drilled until its

2

base was flattened and the superior orbital fissure was reached.

3

The initial anatomical measurements were performed through the MPT with the

4

clinoid still in place. The dura was opened in a semilunar fashion with the base of the

5

flap directed toward the base of the skull. The frontal and temporal operculum and the

6

Sylvian fissure anterior to the anterior sylvian point were exposed. Microsurgical

7

dissection of the sylvian fissure revealed the ipsilateral optico-carotid, chiasmatic, and

8

crural cisterns, as well as the internal carotid artery (ICA), middle cerebral artery,

9

anterior cerebral artery, anterior communicating artery, and posterior communicating

10

artery (PComA). All measurements were then performed for the MPT approach.

11 12

Extradural Anterior Clinoidectomy (eAC): After the initial measurements were

13

made via the MPT approach, the dural flap was closed with 3-0 silk sutures. The eAC

14

then continued in extradural fashion similarly to the conventional approach7. Further

15

drilling was carried on the lateral orbit and once the superior orbital fissure was

16

exposed, the meningo-orbital band was divided. The periosteal dural layer covering the

17

superior orbital fissure and the anterior part of the lateral wall of the cavernous sinus

18

was elevated to expose the lateral and inferior sides of the anterior clinoid process. The

19

3 osseous attachments of the anterior clinoid process were cut using the no-drill

20

technique using microrongeurs and the optic nerve sheath was opened22 (Figure 2). The

21

external dural ring was divided using microscissors and the clinoidal segment of the

22

ICA was exposed (Figure 3).

23 24 25

Measurements

26 27

Stereotactic measurements for each of the targets of interest consisted of the

28

Cartesian X, Y, and Z coordinates obtained with neuronavigation. All landmark

29

coordinates were grouped and processed using dedicated software (Microsoft Office

30

Excel 2013; Microsoft Corp., Redmond, Washington, USA) that calculated all the

31

measurements from a spreadsheet of 3D coordinates

32 33 34 4

1 2 3

Area of exposure

4 5

For each approach (MPT vs MPT + eAC), the area of exposure was determined

6

by the length and width of a pentagonal-shaped region defining the area of interest

7

within the paraclinoid region (Figure 4).

8 9

Six points of interest were selected to define this area, including 1) the bifurcation of the

10

ipsilateral ICA; 2) the anterior edge of the optic chiasma; 3) the origin of the posterior

11

communicating artery; 4) the most proximal exposed point of the ICA; 5) the most

12

anterior point of the exposed optic nerve. Points 1, 2, and 3 were fixed and permanently

13

marked to prevent errors in measurements. The selected area was representative of the

14

surgical anatomy of the paraclinoid region available within MPT approach.

15 16

Surgical Freedom

17 18

The surgical freedom was defined as the area of 4 extreme permissible working

19

positions of the proximal end of a 25-cm endoscopic dissector while its distal tip was

20

held fixed on a particular target of interest as described by Elhadi et al23. Accordingly,

21

the coordinates of the position of the proximal end of dissector were recorded with

22

stereotaxis. For this, the neuronavigation probe was held at the proximal end of the

23

instrument while the latter was moved in 4 different extreme positions in the horizontal

24

and vertical axes23 (ie, superior, inferior, medial, and lateral limits). At the same time,

25

the distal end of the instrument was held fixed to the surgical target of interest.

26 27

The 4 extreme positions of the instrument represented the limit of movement of

28

the surgical instrument inside the surgical corridor and assisted in the calculation of the

29

area of surgical freedom by the same method described previously for the area of

30

exposure.

31 32

Table 1 provides a list of the targets used to measure the surgical freedom.

33

Noteworthy, to minimize brain retraction, all targets were reached with the tip of the

5

1

dissector, precluding the introduction of measurement biases inherent to large shifts in

2

the position of the brain contents.

3 4 Evaluation of the surgical exposure and maneuverability

5 6 7

The visualization and manipulation achieved under microscopic visualization in

8

MPT was compared with those provided by MPT + eAC. All manipulations were

9

assessed by using straight surgical instruments. For accurate assessment, the visual

10

exposure degree of the important neurovascular structures as well as the surgical

11

maneuverability was scored based on the method of Ammirati and Bernardo24 (Table 2).

12

This scale quantifies, in a numerical scale, visual exposure and maneuverability of

13

certain neurovascular structures by evaluating from how many directions a structure can

14

be exposed and which maneuvers can be carried out at those targets. Table 1 displays a

15

list of the neurovascular targets used to determine the the surgical exposure and

16

maneuverability. The assessment of Ammirati and Bernado score24 was achieved by

17

consensus decision of two experienced neurosurgeons (R.M-P. and T.A-F.).

18 19 20 21

Statistical analysis

22 23

Differences in surgical exposure-maneuverability, surgical freedom and area of

24

exposure between the MPT and the MPT + eAC were analyzed using non parametric

25

tests (Mann-Whitney U test). The threshold for statistical significance was P < 0.05, and

26

all tests were calculated using R Studio version 1.0.136. (RStudio inc, Boston, MA,

27

USA).

28 29 30 31 32 33

Results

34 6

1

An example of the intradural view through the MPT and MPT + eAC is

2

displayed in figure 3). The eAC was able to be performed in all 10 sides from 5

3

cadavers. The ipsilateral ICA bifurcation could be exposed in all specimens. The

4

posterior communicating artery was patent in all but one side. The PcomA could be

5

visualized after performing the standard MPT, before performing the ACP removal, in

6

all 9 specimens in which it was present. The ophthalmic artery origin was visualized

7

only after performing the eAC in all sides. The mean length of exposure of the

8

ophthalmic artery after performing the eAC was 4.8 ± 1.8 mm, and the mean length of

9

exposure of the ICA proximal to the origin to the ophthalmic artery was 5 ± 0.8 mm.

10

The mean distance from the tip of the ACP to the origin of the PComA was 4.9 ± 1.4

11

mm (range 2 – 6.8 mm)

12 13

Area of exposure

14 15

The MPT + eAC provided a significantly greater exposure into the paraclinoid

16

region (184.1 ± 44 cm2) than the MPT approach alone (92.8 ± 24.2 cm2), p<0.001

17

(Table 3, Figure 4).

18 19

Surgical Freedom

20 21

Except for the ICA bifurcation, the mean area of surgical freedom provided by

22

MPT + eAC was superior to that of MPT at each of the targets (Table 4; Figure 5). In

23

the MPT, the ophthalmic artery was not exposed in any of the 10 sides, but it was

24

exposed in 100 % of cases after the eAC was performed.

25 26

Surgical exposure and Maneuverability

27 28

MPT + eAC was superior to MPT in terms of surgical exposure and

29

maneuverability, in all target points (OphA, PComA, PrechR), except at the ICA

30

bifurcation (Table 5)

31 32 33

Discussion

7

1 2

The evidence provided in this study establishes that the eAC affords an

3

improved surgical exposure and maneuverability when added to the MPT. Compared to

4

the standard MPT, the MPT + eAC approach affords a 2-fold increase in the area of

5

exposure of the paraclinoid region. Along with the benefits of decompressing the optic

6

nerve and exposing the ophthalmic artery, performing an eAC significantly increases

7

the maneuverability and surgical freedom along the posterior communicating segment

8

of the ICA and the prechiasmatic region.

9 10

These findings add a rationale to further discuss potential new indications of the

11

MPT. Chiarullo and Mura7 described the extradural minipterional approach to access

12

lesions located in the paraclinoid and parasellar area. The abovementioned technique

13

consisted in exploiting the extradural corridor of the MPT throughout a peeling of the

14

middle fossa and eAC. Beer-Furlan et al20 demonstrated the feasibility of using

15

endoscopic minipterional port to extradurally remove the ACP and decompress the optic

16

nerve. Hence, previous works are encouraging regarding reducing surgical invasiveness

17

to approach lesions located in the anterolateral skull base1,7,20,25. However, it is fair to

18

recognize that these techniques are not widely extended among the neurosurgical

19

community. A recent metanalysis demonstrated a clear tendency to use the supraorbital

20

craniotomy over the MPT to approach midline lesions and anterior communicating

21

aneurysms, while the MPT was reserved for middle cerebral aneurysms11. However, it

22

is difficult if not impossible to accomplish an eAC via supraorbital approach and the

23

visualization of the ipsilateral paraclinoid region may be hindered. Beyond the

24

applicability of eAC in the treatment of posterior communicating aneurysms and

25

aneurysms located in the paraclinoid region, the use of eAC via MPT is considered

26

anecdotical11.

27 28

Ophthalmic artery

29 30

Removal of the ACP through a minipterional craniotomy enhances the

31

extradural corridor and improves the surgical exposure and maneuverability deep at the

32

paraclinoid region. The increase in the surgical exposure allows to visualize the origin

33

of the ophthalmic artery. As such, this exposure is enough to comfortably access and

34

manage a cerebral aneurysm arising at this point from a lateral direction using a 8

1

pretemporal or a pure transylvian approach. As shown by others, the frontal lobe is not

2

widely exposed in the MPT craniotomy, and this hinders the frontal lobe retraction and

3

the approach to the ophthalmic artery aneurysms through a subfrontal trajectory1.

4

Nevertheless, this lack of exposure is not an issue per se for surgical freedom and

5

maneuverability. Additionally, the access to the origin of the ophthalmic artery would

6

still be warranted by combining the minipterional craniotomy with an eAC when using

7

a lateral corridor.

8 9

Conversely, the minipterional craniotomy is a minimally invasive technique

10

which provides enough surgical exposure and maneuverability to clip an OphA

11

aneurysm if the eAC is performed. Such technique provides a definitive solution for

12

these aneurysms with reduced risk of recanalization and rupture, in comparison to the

13

endovascular technique25-26.

14 15

Posterior Communicating Artery

16 17

Similarly, ACP removal is occasionally required in the management of certain

18

posterior communicating aneurysms, particularly in ruptured cases wherein proximal

19

control of the ICA before clipping is essential16,27. Cases in which the view of the

20

aneurysm is obstructed by the ACP is another potential indication to perform an ACP

21

removal. Previous studies have investigated the factors predicting the need of

22

performing an anterior clinoidectomy16,18,28. Among these factors the distance from the

23

tip of the ACP to the aneurysm has gained more acceptance16,18. Throughout a

24

meritorious statistical analysis of a large series of clipped PcomA aneurysms, Kamide et

25

al16 established the threshold of 4 mm to predict the requirements to perform an anterior

26

clinoidectomy. These preclinical considerations are key elements in the planification of

27

these type of aneurysms, as not all patients with a posterior communicating aneurysm

28

requires an eAC, and this is not a zero-risk procedure16. However, the power of these

29

studies is limited by several reasons, such as their retrospective nature, the potential

30

effect of observer bias (one-single-surgeon-experience), and the underrepresentation of

31

certain types of PcomA aneurysms (e.g. posteriorly directed PcomA aneurysms,

32

dissecting type).

33

9

1

Although we acknowledge our results need further interpretation, it is suggested

2

that performing an eAC throughout a MPT may help in the management of some

3

PComA aneurysms as it significantly ameliorates the surgical maneuverability and the

4

range of motion around the origin of the PComA, regardless of the distance between

5

ACP and the origin of the posterior communicating artery. The ACP limits the anterior

6

and superior angulation of the microsurgical instruments, which hinders the placement

7

of a straight or a bayonette clip following a posterior direction. This feature explains

8

why clipping might be so challenging when approaching a posteriorly pointed PComA

9

aneurysm. Removal of the ACP, instead, enlarges the anterior space and permits a

10

straight-forward approach to the anterior margin of the aneurysm neck. This extra room

11

is particularly key in minimally invasive approaches in which the maneuvers are already

12

limited by the narrow craniotomy. Several authors have recently demonstrated that

13

posterior projection is a risk factor of intraoperative rupture and poor outcome for

14

microsurgical clipping of PComA aneurysms29,30. Systematically combining a MPT

15

with an eAC in this group of PComA aneurysms might reduce the incidence of

16

intraoperative rupture and achieve better satisfactory results. Moreover, when

17

performing an eAC, the aneurysm anatomy is also better visualized and minimal

18

Sylvian dissection is needed, which will reduce the risk of damaging the brain cortex

19

and the venous system.

20 21

Prechiasmatic region

22 23

MPT suitability to approach the prechiasmatic region has not been previously

24

proved. Across this work, we demonstrate that, if an eAC is performed, the transylvian

25

corridor is dramatically expanded and the prechiasmatic region can be approached with

26

minimal frontal retraction via minipterional craniotomy.

27 28

This approach might result in an excellent minimally invasive alternative for

29

tumors extending into the prechiasmatic area, when the endonasal route is discouraged

30

or when lateral tumor extension demands an open middle fossa approach to achieve

31

maximal resection.

32 33

Limitations

34 10

1

This study has some potential limitations. First, despite our results represent an

2

attempt to objectify the benefits of removing the eAC to increase the area of exposure in

3

deep structures, a broad anatomical knowledge and surgical skills remain the principal

4

factors for achieving maximal procedure success. Moreover, the origin and caliber of

5

the posterior communicating aneurysm is subjected to a great variability and the power

6

of this study might be limited given the small sample size31. Nonetheless, our sample

7

size was enough to demonstrate a significant improvement in the surgical freedom and

8

maneuverability within the paraclinoid region and at the origin of the PComA. Our

9

results were based on a cadaveric model, which lacks the same properties of live tissue

10

and cannot fully replicate the clinical environment. Finally, the eAC was performed in

11

this cadaver study after opening the dura and re-suturing it. Such particularity add a

12

potential limitation to our study, as this does not exactly replicate the clinical scenario,

13

in which the dura is ideally conserved. This drawback just hinders the performance of

14

the eAC in the cadaver, and presumably does not change the direction of our results.

15

Considering the abovementioned pitfalls, these preliminary results demand additional

16

clinical studies that corroborates these findings.

17 18 19

Conclusions

20 21

We have demonstrated eAC improves surgical exposure and maneuverability in

22

the MPT. eAC provides a 2-fold increase in the area of exposure of the paraclinoid

23

region. In comparison to the standard MPT approach, the eAC + MPT improves the

24

maneuverability and range of motion around the paraclinoid region, which carries some

25

clinical implications in the management of certain pathologies in the skull base. Targets

26

away from the clinoid as the internal carotid bifurcation were not affected by eAC.

27 28

Lesions arising at the prechiasmatic region (Craniopharyngiomas, tuberculum

29

sellae meningiomas), carotido-ophthalmic aneurysms, posteriorly pointed and complex

30

PComA aneurysms might be benefited from an MPT+eAC. The MPT offers a less

31

invasive alternative to the traditional pterional or orbitozygomatic approach, while the

32

eAC is a well stablished technique that overcomes some of the previous limitations of

33

the standard MPT.

34 11

1 2

Conflict of interest (see title page)

3 4 5

Figures

6 7

Figure 1. Stepwise dissection of the extradural anterior clinoidectomy through a

8

minipterional craniotomy (MPT + eAC) (right side). After the skin flap is reflected, a

9

classic interfascial dissection is performed (A). The temporalis muscle is dissected

10

subperiosteally and retracted caudally and posteriorly to expose the pterion (B). A

11

minipterional craniotomy is designed underneath the superior temporal line (C). The

12

dura covering the frontal and temporal operculum are exposed and the sphenoid ridge is

13

drilled until its base is flattened. The medial limit of the drilling is the emergence of the

14

MOB at the superior orbital fissure (D). The MOB is coagulated to avoid bleeding from

15

the orbito-meningeal artery and divided. Sectioning the MOB and gentle retraction of

16

the temporal lobe following an interdural dissection provides exposure of the ACP and

17

the anterior third of the cavernous sinus (E). The superior wall of optic canal is removed

18

using a number 1 rotating Kerrison (F). Finally, the ACP is liberated from its

19

attachments and entirely removed, exposing the optic sheath, the triangular clinoidal

20

space and the superior wall of the cavernous sinus (G) (ACP = Anterior clinoidal

21

process; ICA = Internal Carotid Artert; MOB = Meningo-orbital band)

22 23

Figure 2. Extradural view of the minipterional approach combined with the extradural

24

anterior clinoidectomy. (CN IV = Fourth cranial nerve; ICA = Internal Carotid Artery;

25

OS = Optich Sheeth; V1 = Opthlamic branch of the trigeminal nerve).

26 27

Figure 3. Intradural view of the standard minipterional approach (A) and the

28

minipterional approach combined with the extradural anterior clinoidectomy (B). After

29

removing the anterior clinoid process and opening the distal dural ring, the ophthalmic

30

artery is exposed and the posterior communicating artery is possible to approach from a

31

wider angle. The area of exposure in the paraclinoid region between the standard

32

minipterional approach (C) and the minipterional approach combined with the

33

extradural anterior clinoidectomy (D) was calculated aided by the neuronavigation

34

system. Five points, three fixed (anterior border of the optic chiasma; internal carotid 12

1

bifurcation, and posterior communicating artery) and two mobile (proximal exposure of

2

the optic nerve and the internal carotid artery) defined the area of interest.

3 4

Figure 4. Computer-based 3D reconstruction of the minipterional approach illustrating

5

the method of measurement for the surgical freedom (pink area). The reconstruction

6

were obtained with the iNtellect Cranial Navigation System (Stryker, Kalamazoo, MI,

7

USA)

8 9

Figure 5. Boxplot comparing the surgical freedom of the minipterional approach and the

10

combined minipterional with the extradural clinoidectomy for each target of interest.

11

The lower and upper limits of the boxes represent the 25th and 75th percentiles,

12

respectively. The horizontal line represents the median, and bars, the range. (MPT =

13

Standard Minipterional Approach; MPT + eAC = Minipterional Approach and

14

Extradural Anterior Clinoidectomy combination; * significant difference for a p < 0.05,

15

Mann-Whitney U Test)

16 17 18 19 20 21

References

22 23 24 25

1.

Figueiredo EG, Deshmukh P, Nakaji P, et al. The minipterional craniotomy: technical description and anatomic assessment. Neurosurgery. 2007;61(5 Suppl 2):256-264; discussion 264-265. doi:10.1227/01.neu.0000303978.11752.45

26 27 28

2.

Figueiredo EG, Teixeira MJ, Spetzler RF, Preul MC. Clinical and surgical experience with the minipterional craniotomy. Neurosurgery. 2014;75(3):E324325. doi:10.1227/NEU.0000000000000456

29 30 31 32

3.

Caplan JM, Papadimitriou K, Yang W, et al. The minipterional craniotomy for anterior circulation aneurysms: initial experience with 72 patients. Neurosurgery. 2014;10 Suppl 2:200-206; discussion 206-207. doi:10.1227/NEU.0000000000000348

33 34 35

4.

Figueiredo EG, Welling LC, Preul MC, et al. Surgical experience of minipterional craniotomy with 102 ruptured and unruptured anterior circulation aneurysms. J Clin Neurosci. 2016;27:34-39. doi:10.1016/j.jocn.2015.07.032

36 37

5.

Kang H-J, Lee Y-S, Suh S-J, Lee J-H, Ryu K-Y, Kang D-G. Comparative Analysis of the Mini-pterional and Supraorbital Keyhole Craniotomies for Unruptured

13

Aneurysms with Numeric Measurements of Their Geometric Configurations. J Cerebrovasc Endovasc Neurosurg. 2013;15(1):5-12. doi:10.7461/jcen.2013.15.1.5

1 2 3 4 5 6 7

6.

Noiphithak R, Yanez-Siller JC, Revuelta Barbero JM, et al. Comparative Analysis of the Exposure and Surgical Freedom of the Endoscopic Extended Minipterional Craniotomy and the Transorbital Endoscopic Approach to the Anterior and Middle Cranial Fossae. Operative Neurosurgery. December 2018. doi:10.1093/ons/opy309

8 9 10 11

7.

Chiarullo M, Mura J, Rubino P, et al. Technical Description of Minimally Invasive Extradural Anterior Clinoidectomy and Optic Nerve Decompression. Study of Feasibility and Proof of Concept. World Neurosurgery. May 2019:S1878875019314731. doi:10.1016/j.wneu.2019.05.196

12 13 14 15

8.

Welling LC, Figueiredo EG, Wen HT, et al. Prospective randomized study comparing clinical, functional, and aesthetic results of minipterional and classic pterional craniotomies. J Neurosurg. 2015;122(5):1012-1019. doi:10.3171/2014.11.JNS146

16 17

9.

Davies JM, Lawton MT. Advances in open microsurgery for cerebral aneurysms. Neurosurgery. 2014;74 Suppl 1:S7-16. doi:10.1227/NEU.0000000000000193

18 19 20 21

10. Yagmurlu K, Safavi-Abbasi S, Belykh E, et al. Quantitative anatomical analysis and clinical experience with mini-pterional and mini-orbitozygomatic approaches for intracranial aneurysm surgery. J Neurosurg. 2017;127(3):646-659. doi:10.3171/2016.6.JNS16306

22 23 24

11. Rychen J, Croci D, Roethlisberger M, et al. Keyhole approaches for surgical treatment of intracranial aneurysms: a short review. Neurol Res. 2019;41(1):68-76. doi:10.1080/01616412.2018.1531202

25 26 27

12. Tra H, Huynh T, Nguyen B. Minipterional and Supraorbital Keyhole Craniotomies for Ruptured Anterior Circulation Aneurysms: Experience at Single Center. World Neurosurgery. 2018;109:36-39. doi:10.1016/j.wneu.2017.09.058

28 29 30

13. Wicks RT, Zhao X, Hardesty DA, Liebelt BD, Nakaji P. Mini-pterional approach for clip ligation of ethmoidal dural arteriovenous fistula. Neurosurg Focus. 2019;46(Suppl_2):V9. doi:10.3171/2019.2.FocusVid.18660

31 32 33

14. Dolenc VV. A combined transorbital-transclinoid and transsylvian approach to carotid-ophthalmic aneurysms without retraction of the brain. Acta Neurochir Suppl. 1999;72:89-97.

34 35 36 37

15. Giammattei L, Starnoni D, Levivier M, Messerer M, Daniel RT. Surgery for Clinoidal Meningiomas: Case Series and Meta-Analysis of Outcomes and Complications. World Neurosurg. 2019;129:e700-e717. doi:10.1016/j.wneu.2019.05.253

38 39 40 41

16. Kamide T, Burkhardt J-K, Tabani H, Safaee MM, Lawton MT. Preoperative Prediction of the Necessity for Anterior Clinoidectomy During Microsurgical Clipping of Ruptured Posterior Communicating Artery Aneurysms. World Neurosurg. 2018;109:e493-e501. doi:10.1016/j.wneu.2017.10.007 14

1 2 3

17. van Loveren HR, Keller JT, el-Kalliny M, Scodary DJ, Tew JM. The Dolenc technique for cavernous sinus exploration (cadaveric prosection). Technical note. J Neurosurg. 1991;74(5):837-844. doi:10.3171/jns.1991.74.5.0837

4 5 6 7

18. Yang Y, Wang H, Shao Y, Wei Z, Zhu S, Wang J. Extradural anterior clinoidectomy as an alternative approach for optic nerve decompression: anatomic study and clinical experience. Neurosurgery. 2006;59(4 Suppl 2):ONS253-262; discussion ONS262. doi:10.1227/01.NEU.0000236122.28434.13

8 9 10

19. Martinez-Perez R, Mura JM. The Extradural Minipterional Approach: “Think Small, Play Wider.” World Neurosurgery. 2019;125:534-535. doi:10.1016/j.wneu.2018.10.240

11 12 13

20. Beer-Furlan A, Evins AI, Rigante L, et al. Endoscopic extradural anterior clinoidectomy and optic nerve decompression through a pterional port. J Clin Neurosci. 2014;21(5):836-840. doi:10.1016/j.jocn.2013.10.006

14 15 16 17

21. Yaşargil 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. 1987;67(3):463-466. doi:10.3171/jns.1987.67.3.0463

18 19 20 21

22. Iwasaki K, Toda H, Hashikata H, Goto M, Fukuda H. Extradural Anterior Clinoidectomy and Optic Canal Unroofing for Paraclinoid and Basilar Aneurysms: Usefulness of a No-Drill Instrumental Method. Acta Neurochir Suppl. 2018;129:39-42. doi:10.1007/978-3-319-73739-3_6

22 23 24 25

23. Elhadi AM, Hardesty DA, Zaidi HA, et al. Evaluation of surgical freedom for microscopic and endoscopic transsphenoidal approaches to the sella. Neurosurgery. 2015;11 Suppl 2:69-78; discussion 78-79. doi:10.1227/NEU.0000000000000601

26 27 28

24. Ammirati M, Bernardo A. Analytical evaluation of complex anterior approaches to the cranial base: an anatomic study. Neurosurgery. 1998;43(6):1398-1407; discussion 1407-1408. doi:10.1097/00006123-199812000-00081

29 30 31 32

25. Martinez-Perez R, Hernandez-Alvarez V, Maturana R, Mura JM. How I do it: The extradural minipteriona pretemporal approach for the treatment of spheno-petroclival meningiomas. Acta Neurochir (Wien). September 2019:[Epub ahead of print]. doi:10.10077s00701-019-04064-3

33 34 35 36 37

26. Molyneux AJ, Kerr RSC, Yu L-M, et al. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet. 2005;366(9488):809-817. doi:10.1016/S0140-6736(05)67214-5

38 39 40 41

27. Otani N, Wada K, Toyooka T, Takeuchi S, Tomiyama A, Mori K. Surgical Strategies for Ruptured Complex Aneurysms Using Skull Base Technique and Revascularization Surgeries. Asian J Neurosurg. 2018;13(4):1165-1170. doi:10.4103/ajns.AJNS_176_18

15

1 2 3 4

28. Ochiai C, Wakai S, Inou S, Nagai M. Preoperative angiographical prediction of the necessity to removal of the anterior clinoid process in internal carotid-posterior communicating artery aneurysm surgery. Acta Neurochir (Wien). 1989;99(34):117-121. doi:10.1007/bf01402319

5 6 7 8

29. Fukuda H, Hayashi K, Yoshino K, et al. Impact of Aneurysm Projection on Intraoperative Complications During Surgical Clipping of Ruptured Posterior Communicating Artery Aneurysms. Neurosurgery. 2016;78(3):381-390; discussion 390. doi:10.1227/NEU.0000000000001131

9 10 11

30. Matsukawa H, Fujii M, Akaike G, et al. Morphological and clinical risk factors for posterior communicating artery aneurysm rupture. J Neurosurg. 2014;120(1):104110. doi:10.3171/2013.9.JNS13921

12 13 14

31. Gibo H, Lenkey C, Rhoton AL. Microsurgical anatomy of the supraclinoid portion of the internal carotid artery. J Neurosurg. 1981;55(4):560-574. doi:10.3171/jns.1981.55.4.0560

15 16 17 18 19 20

16

Table 1. Neurovascular targets used to measure the surgical freedom and manipulability along the paraclinoid region.

-

Origin of the ipsilateral ophthalmic artery

-

Bifurcation of the ipsilateral internal carotid artery

-

Origin of the ipsilateral posterior communicating artery

-

Prechiasmatic area measured at the anterior edge of the optic chiasma

Table 2. Surgical exposure and maneuverability according to the Ammirati & Bernardo´s scale1. Score 0 1 2 3

No exposure Limited exposure; surgical maneuvers are not possible Multiangled exposure; surgical maneuvers are difficult Multiangled exposure; surgical maneuvers are facilitated

Table 3. Area of Exposure of the Paraclinoid region provided by standard Minipterional Craniotomy and Combination of the minipterional approach with the extradural anterior clinoidectomy. Area of Exposure ± SD (cm2) MPT MPT + eAC 92.8 ± 24.2 184.1 ± 44

p Value < .001

Table 4. Surgical Freedom for Each Surgical Target Provided by standard Minipterional Craniotomy and Combination of the minipterional approach with the extradural anterior clinoidectomy.

Target of interest Ophthalmic Artery Internal Carotid Bifurcation Posterior Communicating Artery Prechiasmatic Area

Mean surgical freedom ± SD (cm2) p Value MPT MPT + eAC < .001 0 17.7 ± 3.9 0.9 13.9 ± 4.6 14.8 ± 5.8 0.002 13.2 ± 2.8 18.9 ± 3.8 0.004 6.2 ± 2 12.3 ± 2.4

MPT = Minipterional Approach; MPT + eAC = Combination of the minipterional approach with the extradural anterior clinoidectomy; SD = Standard Deviation. * P Value according to the Mann-Withney U Test

Table 5. Surgical exposure and maneuverability for Each Surgical Target Provided by standard Minipterional Craniotomy and Combination of the minipterional approach with the extradural anterior clinoidectomy. Target of interest Ophthalmic artery Internal carotid bifurcation Posterior communicating artery Prechiasmatic region

Mean Ammirati&Bernardo score ± SD MPT MPT + eAC 2.6 ± 0.5 0±0 2.9 ± 0.3 2.9 ± 0.3 2.2 ± 0.8 2.9 ± 0.5 2.6 ± 0.6 1.2 ± 0.6

P value < 0.001 > .9 .022 0.001

MPT = Minipterional Approach; MPT + eAC = Combination of the minipterional approach with the extradural anterior clinoidectomy; SD = Standard Deviation. * P Value according to the Mann-Withney U Test

Authors contribution section: 1. 2. 3. 4. 5. 6.

Conception and design of the study: Martinez-Perez Acquisition of data: Albonette-Felicio Interpretation of data: Zachariah, Carrau, Prevedello Drafting the article: Martinez-Perez, Albonette-Felicio, Zachariah Critically reviewed the manuscript: Prevedello, Carrau, Hardesty Final approval of the last version: Martinez-Perez, Albonette-Felicio, Hardesty, Zachariah, Carrau, Prevedello

Abbreviations: Anterior clinoid process (ACP) extradural anterior clinodectomy (eAC) Internal carotid artery (ICA) minipterional approach and extradural anterior clinoidectomy combination (MPT + eAC) Ophthalmic artery (OphA) posterior communicating artery (PComA) standard minipterional approach (MPT)