Carotid artery visualization during anterior skull base surgery:a novel protocol for neuronavigation

Brent M. McGrath • William J. Maloney •

Stefan Wolfsberger • Ron Hill • Emad Massoud •

Syed Ali Imran • David B. Clarke

Published online: 12 February 2010

� Springer Science+Business Media, LLC 2010

Abstract Detailed knowledge of the vascular anatomy

of the anterior skull base is critical to successful surgery

in this area. Whereas conventional neuronavigational

approaches combine MRI (± contrast) for tumor visuali-

zation and CT (± C) for bony and vascular anatomy, we

describe the Canadian and Austrian experiences using a

novel protocol integrating MR angiography (MRA) into

surgical neuronavigation to provide superior visualization

of the carotid arteries. The pre-operative imaging protocol

employs a T1-weighted, 3D fast spoiled gradient echo MRI

(± C) for soft tissue anatomy, a plain CT for bony anat-

omy, and a 3D time-of-flight MR angiography for carotid

anatomy. The series are imported into the Medtronic

StealthStation� TREON� Treatment Guidance System;

during intra-operative neuronavigation, each series (MRI,

CT, MRA) can be viewed individually, or layered and

viewed as a composite image. Our protocol has important

advantages. First, it provides detailed tissue, tumor, vas-

cular and bony anatomy. Second, a contrast CT is not

necessary; this is important, as numerous reports have

highlighted the nephrotoxic nature of radiographic contrast

material. Third, visualization of the carotid system is

superior than can be obtained from CT angiography. We

use this unique imaging protocol routinely for our endo-

scopic transsphenoidal surgeries to provide superior visu-

alization of the carotid arteries during anterior skull base

surgery.

Keywords Neuronavigation � Transsphenoidal surgery �Carotid artery � Skull base �Magnetic resonance angiography

Background

Guiot and Thibaut [1] repopularized transsphenoidal sur-

gery, a procedure whose widespread acceptance as a

modern neurosurgical approach was made possible by

Hardy’s refinements, including the introduction of micro-

surgical techniques and neuroimaging [2–4]. Transsphe-

noidal approaches to the skull base are now considered

safe, with acceptably low mortality rates [5–7]. Despite

low mortality rates, however, the morbidity associated with

transsphenoidal surgery remains significant; in a recent

B. M. McGrath � R. Hill � E. Massoud � D. B. Clarke (&)

Department of Surgery (Neurosurgery), Dalhousie University,

1796 Summer Street, Halifax, NS B3H 3A7, Canada

e-mail: d.clarke@dal.ca

W. J. Maloney

Department of Radiology and Diagnostic Imaging

(Neuroradiology), Dalhousie University, 1796 Summer Street,

Halifax, NS B3H 3A7, Canada

S. Wolfsberger

Department of Neurosurgery, Medical University of Vienna,

Vienna, Austria

E. Massoud � D. B. Clarke

Department of Surgery (Otolaryngology), Dalhousie University,

5820 University Avenue, Halifax, NS B3H 2Y9, Canada

S. A. Imran � D. B. Clarke

Department of Medicine (Endocrinology), Dalhousie University,

1276 South Park Street, Halifax, NS B3H 2Y9, Canada

E. Massoud � S. A. Imran � D. B. Clarke

Halifax Neuropituitary Program, Dalhousie University,

1796 Summer Street, Halifax, NS B3H 3A7, Canada

D. B. Clarke

Department of Anatomy & Neurobiology, Dalhousie University,

1796 Summer Street, Halifax, NS B3H 3A7, Canada

123

Pituitary (2010) 13:215–222

DOI 10.1007/s11102-010-0220-0

large review of more than five thousand cases, 26.8%

morbidity was reported which included neurovascular

complications in 6.9% of patients [6]. The importance of

avoiding carotid or basilar artery injury has been empha-

sized by several authors, and understanding the vascular

relationships in this era of endoscopic approaches is critical

[8–11].

The present technical note reports on Canadian and

Austrian experiences using a novel imaging protocol that

provides excellent bony and high-quality carotid artery

visualization during anterior skull base surgery. This sur-

gical neuronavigation protocol uses a single contrast study,

integrating non-enhanced CT, contrast MRI and MR

angiography (MRA).

Imaging technique

MR data were acquired with a 1.5 Tesla (T) scanner (GE

HDx Signa). MRI images were obtained using sagittal T1,

coronal T1 and T2 as well as post-gadolinium coronal T1

weighted 3D fast spoiled gradient echo (FSGE) sequences

(TR = 11.21 ms, TE = 4.2 ms, slice thickness = 1.5 mm,

resolution = 256 9 256). During the same scanning

Fig. 1 Pre-operative studies,

Patient 1. a Coronal T1 MRI

with enhancement showing

sellar mass. b Anterior-posterior

MRA showing cerebral arterial

vasculature, including carotid-

basilar arteries. c Axial CT

(plain)

216 Pituitary (2010) 13:215–222

123

session, MRA images were obtained using a 3D vascular

time-of-flight (TOF) SPGR sequence (TR = 24 ms,

TE = 2.3 ms, slice thickness = 1.4 mm, resolution =

256 9 256). Non-enhanced CT data were acquired on a

Siemens Somatom Sensation 64 scanner in contiguous

1 mm thick axial slices. The same skin fiducial markers

were used for both CT and MRI/MRA scanning and served

to verify fusion of the three imaging data series.

Imaging data from all three paradigms were then

integrated and stored in the Medtronic StealthStation�

TREON� Treatment Guidance System for use during

surgery. Intra-operative multiplanar neuronavigation enables

each data series (i.e. MRI, MRA and/or CT) to be viewed

individually, or layered and viewed as a composite of any

combination of the three image series. MRI and CT

images are windowed to be viewed in the standard

radiological fashion, whereas MRA images are viewed in

heat scale so as to highlight the carotid-basilar arterial

system, and to differentiate it from surrounding soft tissue

and bone.

Illustrative cases

The following three cases include examples of the

acquired images and show intra-operative neuronavigation

images obtained by using our MRI/MRA/CT imaging

technique.

Fig. 2 Intra-operative neuronavigation, Patient 1. MRA/MRI fused

images showing carotid arteries (color) in relation to sellar mass (grayscale) in coronal (a) and sagittal (b) planes. MRA/CT fused images

showing carotid arteries (color) in relation to bony sellar anatomy

(gray scale) in similar coronal (c) and sagittal (d) planes. Crosshairsindicate the inferior border of the left cavernous sinus. (Color figure

online)

Pituitary (2010) 13:215–222 217

123

Patient 1

A 52-year-old man presented with a 3-month history of

headaches and decreased vision in his left eye, revealed by

Goldmann visual field-testing to be a left incomplete

temporal hemianopsia. Endocrine evaluation revealed

secondary hypothyroidism and hypogonadism. Pre-opera-

tive imaging by coronal MRI revealed a sellar mass

(2.5 cm 9 2.1 cm in maximal cross-sectional diameters)

extending superiorly and compressing the left aspect of the

optic chiasm. Clinical evaluation, neuroimaging and hor-

mone studies were consistent with the final diagnosis of a

non-functioning pituitary macroadenoma. See Figs. 1 and 2

for pre- and intra-operative images, respectively.

Patient 2

A 32-year-old woman presented with clinical features of

Cushing’s syndrome. Pre-operative coronal MRI revealed a

small, non-enhancing microadenoma and, incidentally, a

hypoplastic left vertebral artery. Clinical evaluation, neu-

roimaging and hormone studies were consistent with the

final diagnosis of Cushing’s disease. See Figs. 3 and 4 for

pre- and intra-operative images, respectively.

Patient 3

A 31-year-old women admitted to hospital due to rapid

visual deterioration. Pre-operative MRI revealed a large

Fig. 3 Pre-operative studies,

Patient 2. a Pre-operative

coronal T1 MRI with

enhancement showing sellar

mass. b Pre-operative anterior-

posterior MRA showing

cerebral arterial vasculature.

c Pre-operative axial CT (plain)

218 Pituitary (2010) 13:215–222

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sellar tumor with suprasellar extension compressing the

optic chiasm and parasellar extension encasing the left

intracavernous carotid artery (Grade IV according to Knosp

[12]). Clinical and biochemical evaluations confirmed the

diagnosis of acromegaly secondary to a pituitary growth

hormone producing tumor, a macroadenoma. See Figs. 5

and 6 for pre- and intra-operative images, respectively.

Discussion

Vascular complications associated with transsphenoidal

pituitary surgery include venous injury involving the cav-

ernous sinus and carotid arterial injury that may necessitate

carotid sacrifice, with or without stroke. Fundamental to

avoiding such carotid injuries is the surgeon’s ability to

understand in detail the course of the carotid arteries as

they approach, and then course through, the cranial base.

Also critical is recognizing that the course of the carotids,

and therefore their anatomic relationships with surrounding

structures, can vary significantly from one patient to

another [13, 14].

Advances in modern neuronavigation and imaging

techniques, including CT and MRI (both with, and without

contrast enhancement) have enabled better pre-operative

assessment of surgical anatomy. However carotid visuali-

zation by CT angiography provides suboptimal vessel—

bone contrast and, similarly, Gd-enhanced MRI provides

Fig. 4 Intra-operative neuronavigation, Patient 2. MRA/MRI fused

images showing carotid-basilar arteries (color) in relation to sellar

mass (gray scale) in coronal (a) and sagittal (b) planes. MRA/CT

fused images showing carotid-basilar arteries (color) in relation to

bony sellar anatomy (gray scale) in similar coronal (c) and sagittal (d)

planes. Crosshairs indicate the inferior border of the sellar mass.

(Color figure online)

Pituitary (2010) 13:215–222 219

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poor carotid artery—cavernous sinus distinction. Further-

more, the use of contrast agents in both scans carries

additional cost and potential risk. The use of iodinated

agents and gadolinium have been reported in numerous

studies to cause subsequent renal dysfunction [15, 16], and

to be the third most common cause of renal failure among

hospitalized patients [15, 17]. While there is some recent

evidence [18] to suggest that the nephrotoxic effects of

contrast agents may not be as pervasive as once thought,

employing an imaging method that provides excellent

visualization of the neuro-vasculature while minimizing

the patient’s exposure to potentially toxic substances is a

worthy endeavor.

Utilization of this protocol has several important

advantages. First, it provides the detailed tissue, tumor,

vascular and bony anatomy that is a prerequisite for an

optimal neuronavigational tool. Second, a contrast CT or

catheter-based angiographic approach is not necessary; this

is an important advantage in light of the risks outlined

above. Moreover, catheter angiography carries the added

risk of inducing severe neurologic injury [19]. MRA, like

all MR imaging modalities, has no known adverse effects

and is done as part of the routine pre-operative MR scan.

Third, visualization of the carotid system is superior than

can be obtained from CT angiography; the surgeon is

provided with high quality vascular images having high

spatial resolution. The only foreseeable drawback of uti-

lizing MRA in place of contrast CT is that it requires longer

scan times in the MR imager. At many institutions,

including our own, MR time is at a premium. That said, the

additional scan time is small (less than 6 min) and the

associated cost would likely be offset by reductions in CT

scanning time, the use of contrast agents, incidence of

contrast-induced nephropathies, and vascular injury at the

time of surgery.

In response to the suboptimal neuronavigational visu-

alization of the carotid arteries as they course through the

skull base, we have developed and have now used this

imaging protocol in almost 400 patients; it is now used for

all of our anterior skull base surgeries.

Fig. 5 Pre-operative studies, Patient 3. a Coronal T1 MRI with enhancement showing sellar mass with supra- and left para-sellar extension.

b Sagittal MRA showing cerebral arterial vasculature. Note the elongated left carotid siphon. c Axial CT (plain)

220 Pituitary (2010) 13:215–222

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Acknowledgments The authors would like to thank Carla Roberts

for her assistance in the preparation of this manuscript.

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