Abstract
Advances in imaging technology have provided new diagnostic
methods for assessment of cerebral vascular perfusion and
quantitative analysis of the microcirculation£¨Side
stream dark field imaging (SDF),Sidestream
dark field imaging (SDF)£© during cerebral
surgery. In this article, a range of imaging procedures are
described: Digital Subtraction Angiography (DSA) and
Three-Dimensional Computed Tomography Angiography (3D-CTA),
Indocyanine Green Video An¬giography (ICGVA), Orthogonal
Polarization Spectral (OPS) Imaging, Sidestream Dark-Field (SDF)
Imaging, Sidestream dark field (SDF),and Laser-Doppler Flowmetry (LDF). All these
measurements will foster development of precise evaluation tools
for microcirculation-re¬lated microvascular conditions, e. g.
stroke and hemorrhage, and support clinicians in their
thera¬peutic decision-making process.
Key words: angiography, cerebral surgery, intraoperative
imaging, microcirculation£¨Side
stream dark field imaging (SDF),Sidestream
dark field imaging (SDF)£©, macrocirculation
Cerebrovascular surgery is an operative treat-basic principles
of brain surgery, but main¬ment for brain vasculature diseases,
such as taining the integrity of cerebral microcircula¬aneurysms,
arteriovenous malformations, tion is also critical and more
challenging for cavernomas, and occlusive vascular diseases
function and survival of the tissue cells since like stroke.
Traditionally, neurosurgeons di-supply of oxygen and nutrients
to individual rectly inspect cerebral vessels with the aid of
cells and elimination of waste products from an operating
microscope during surgery. To cells occur in the
microcirculation£¨Side
stream dark field imaging (SDF),Sidestream
dark field imaging (SDF),Sidestream
dark field (SDF)£© (2). How¬minimize the morbidity and mortality
associ-ever, imaging techniques for assessing mi¬ated with the
surgical treatment, angiogra-crocirculation in clinical
medicine, especial¬phy has been introduced and used as a stan-ly
in brain surgery is very limited. In addidard method for
preoperative diagnosis and tion, there is a lack of agreement on
which postoperative evaluation of the vascular microcirculatory
parameters and analyzing anatomy. However, if postoperative
angiog-techniques can be used for evaluating the raphy reveals
an abnormal surgical result, microcirculation£¨Side
stream dark field imaging (SDF),Sidestream
dark field imaging (SDF),Sidestream
dark field (SDF)£©. This makes the microcircu¬another surgical procedure has to be per-latory study
more complex. The aim of this formed for correction or the
compromised article is to review techniques of intraopera¬vessel
has already caused an infarction. tive imaging at macro- and
microcirculation Therefore, intraoperative angiography has in
human brain surgery. been applied for evaluating vascular
anato¬my and perfusion in real-time (1).
Maintaining the integrity of tissue perfu¬sion through
macrovasculature is one of the
Digital Subtraction Angiography (DSA) and Three-Dimensional
Computed Tomography Angiography (3D-CTA)
DSA is considered as the ¡°gold standard¡± for detection of
cerebral aneurysms and moni¬toring surgical results
intraoperatively or postoperatively (3). However, since it¡¯s
inva¬sive, time-consuming and technical demand¬ing,
intraoperative DSA is not considered as a routine method for all
the cases and not available in all the centers. 3D-CTA as
anoth¬er diagnostic method in the detection of in¬tracranial
aneurysms is found to provide comparable information to DSA, but
less in¬vasive, less time consuming, cheaper and easier to
demonstrate the essential informa¬tion regarding the aneurysm
than DSA (4)(5).
Indocyanine Green Video Angiography (ICGVA)
ICGVA has been used in ophthalmology for many years but applied
in brain surgery re¬cently for intraoperative assessment of
cere¬bral vasculature in routine or emergency sur¬gery for
patients with intracranial aneurysms (6), cerebral arteriovenous
or dural fistulous malformations (7), moyamoya disease (8, 9)
and decompressive craniectomy for malig¬nant stroke (10). It was
performed with a laser-fluorescence imaging device that
con¬sisted of a NIR laser light source (0.16 W, =780 nm) and a
NIR-sensitive digital cam¬corder. The device was placed 30 to 40
cm from the area of interest and illuminated the area of
interest with the laser light source. The NIR laser light
emitted from the light source induced fluorescence of ICG, a NIR
fluorescent dye injected intravenously. The fluorescence signal
was recorded by the dig¬ital video camera with optical filtering
to block ambient and laser light for collection of only ICG-induced
fluorescence. Angiographic images could be reviewed on the
video screen in real time (25 images/s) and stored on the
digital video camera or trans¬ferred to a computer (6). ICGVA
provides high quality image with spatial resolution that allows
assessment of the arterial and venous vessels, including small
arteries (<0.5 mm in diameter), and the visible aneurysm sac at
real-time. It is a quick, reliable, cost-effective method and
clinically useful in aneurysm, dural fistula, and
revascularization surgery. It was report¬ed that results
obtained from intraoperative ICGVA in all the cases of aneurysms
surger¬ies corresponded to the postoperative angiographic
finding, but in some cases, the infor¬mation provided by
intraoperative ICGVA significantly changed the surgical
procedure (6). The major limitation of the method was that the
ICG angiographic views were re¬stricted to the angle of the
surgical approach. Vessels that were covered by blood clots or
aneurysm or brain tissue£¨Side
stream dark field imaging (SDF),Sidestream
dark field imaging (SDF),Sidestream
dark field (SDF)£© could not be ob¬served with this
technique (6).
In a recent study, Schnell and co-authors compared advantages
and drawbacks of ICGVA and intraoperative computed tomog¬raphy
angiography (iCTA) and intraoperative computed perfusion
tomography (iCTP) on visualizing brain vasculature during
aneurysm surgery (11). They found that ICG-VA was able to detect
blood flow and vascu¬lar patency in the vessels only located in
the visual field of microscope but not in the deeper areas of
surgical field. iCTA provided high quality image in 7/10
patients but could not detect small arteries. iCTP was also able
to detect global blood flow in some cases but not in others.
Therefore, ICGVA and iCTA/iCTP are complementary rather than
competing techniques and able to assess lo¬cal and regional
blood flow and cerebral perfusion in intracranial aneurysm
surgery (11).
Orthogonal Polarization Spectral (OPS) Imaging
OPS imaging is a noninvasive method for as¬sessing
microcirculation(Side
stream dark field imaging (SDF),Sidestream
dark field imaging (SDF)) on the surfaces of organs. It uses a handheld
device with a small optical probe. The tissue is illuminated
with linearly polarized light and only depo¬larized photons
scattered from the tissue contribute to the imaging (12). It
produces high contrast microvascular images that al¬low viewing
and quantifying microcirculato¬ry hemodynamic changes at
real-time and provides a convenient method for intravital
microscopy on the brain surface.
OPS has been used to assess cerebral mi¬crocirculatory changes
during brain surgeries of arteriovenous malformation (AVM) (13),
aneurysm (14)(15) and tumor removal (16). Parameters of
microcirculation£¨Side stream dark field
imaging (SDF),Sidestream dark field
imaging (SDF),Sidestream dark field (SDF)£©, including di¬ameters of blood vessels,
microvascular flow index (MFI), functional capillary index (FCD),
flow kinetics and arteriolar contractil¬ity could be evaluated
during the surgeries. For example, in AVM surgery, Pennings and
coauthors demonstrated that prior to AVM excision, cardiac
pulsation was absent in the arterioles and individual
erythrocytes were observed due to the slowing of blood flow.
However, increased flow velocity (to a level that individual
erythrocytes could not be traced), FCD and MFI were observed
after re¬section (13). In brain tumor surgeries, stop¬flow and
spurt-flow with irregularly shaped vessels and large mean vessel
diameters were observed in tumor microcirculation£¨Side
stream dark field imaging (SDF),Sidestream
dark field imaging (SDF),Sidestream
dark field (SDF)£© in comparison
to normal healthy cortex, which always expressed continuous flow
(16).
Although OPS imaging greatly con¬tributes to study the brain
microcirculation, there are still weaknesses by using OPS
im¬aging such as motion-induced image blur¬ring caused by
movement of the OPS device, the tissue and the blood flowing. In
addition, it is difficult to measure flow velocity in large
vessels, especially during continuous flow, due to blurring of
images (17, 18).
Sidestream Dark-Field (SDF) Imaging
SDF imaging is another noninvasive tech¬nique for continuous
observation of cerebral microcirculation on the brain surface
during brain surgery. It is a further development of OPS
techniques and consists of a handheld videomicroscope containing
a ring of strobo¬scopic light emitting diodes (18). Using SDF(Side
stream dark field imaging (SDF),Sidestream
dark field imaging (SDF)),
Perez-Barcena and coauthors reported direct visualization of
blood flow and vessel densi¬ty of cerebral microcirculation in
patients who underwent decompressive craniectomy after
infarction of cerebral artery and the non-stroke control
patients who underwent craniotomy for diseases other than stroke
(19). The cortical vessels in the control pa¬tients were
regularly shaped with continuous blood flow in all sizes of
vessels (from 10 to 100 µm in diameters) and the proportion of
the perfused vessels was near 100%. The cortical vessels in the
patients with stroke showed intermittent or no flow with smaller
proportion of perfused vessels (63.44%). The perfused vessels
density index was also high¬er in control group than in patients
with stroke (19).
However, SDF imaging(Side stream dark
field imaging (SDF),Sidestream dark
field imaging (SDF),Sidestream dark
field (SDF)) cannot directly measure the velocity of
erythrocytes since high erythrocyte velocity exceeds the capture
rate of the camera for tracing individual red blood cells. In
addition, pressure-induced mi¬crocirculatory alterations caused
by applica¬tion of the SDF probe onto the tissue surface might
lead to false interpretation of actual mi¬crocirculation
perfusion (18, 19). In the fu¬ture, new devices with more
advanced cam¬era technology may solve the problem for measuring
the velocity of erythrocytes.
Laser-Doppler Flowmetry (LDF) and Combined With
Photospectrometry
Laser Doppler flowmetry (LDF) was estab¬lished as a noninvasive
method for continu¬ous and real-time measurement of blood
flow in the microcirculation£¨Side
stream dark field imaging (SDF),Sidestream
dark field imaging (SDF),Sidestream
dark field (SDF)£©. It measures rel¬ative
microcirculatory flow based on the Doppler shift of the
illuminated laser light caused by the movement of red blood
cells (20). The light is able to penetrate into the depth of
tissue and measure microvascular blood flow throughout it, but
the depth de¬pends on optical feature, wavelength used and the
diameter of the beam (21). LDF has been used in the
intraoperative assessment of cortical blood flow during general
neuro¬surgical procedures (22) and surgeries for cerebral
arteriovenous malformations (23) and various cerebral tumours
(24). The major disadvantage is its high sensitivity to
motion¬produced disturbances.
Recently, a novel monitoring device (O2C, oxygen-to-see device)
based on com¬bined laser-Doppler flowmetry and
photo¬spectrometry has been introduced to moni¬tor cortical
microcirculation (Side stream dark field
imaging (SDF),Sidestream dark field
imaging (SDF)) during intracra¬nial surgery (25-27). The
device consists of a computer with built-in laser and light
emit¬ting diodes and a fiber optic measurement probe. It
transmits continuous wave laser light (830nm) and white light
(500-800nm) to tissue and collocate the scattered light from
tissue to the probe. The Doppler shift of the illuminated laser
light is displayed as blood flow velocity while the collected
white light is split into its spectral compo¬nents and converted
into an electrical signal. Oxygen saturation is determined by
compar¬ison with prerecorded deoxygenated and oxygenated
hemoglobin spectra, while the tissue hemoglobin values are
determined by the amount of light absorbed by the tissue. This
device is used only for measurements in the microcirculation
(<100 µm diameter) since light from bigger vessels (> 100 µm
di¬ameter) is completely absorbed (26, 27). Rel¬ative blood flow
is calculated based on the product of moving erythrocytes and
velocity of each erythrocyte.
This device£¨Side
stream dark field imaging (SDF),Sidestream
dark field imaging (SDF),Sidestream
dark field (SDF)£© is able to determine regional capillary-venous
cerebral blood flow, oxy¬gen saturation and hemoglobin amount
si¬multaneously in the cortical/cerebral tissue. It is easy to
set up and can be used continu¬ously during brain surgery.
Although the depth of measurement is dependent on the distant
between the illuminating and detect¬ing elements, the type of
probe used and op¬tical characteristics of the tissue, it has
been used for measuring cerebral microcirculation from 2 mm to 8
mm of depth. However, this device only provides relative values,
not quantitative measurement due to the feature of laser-Doppler
flowmetry. In addition, the measurement may be influenced by
neuro¬surgery, cortical temperature and blood film in the
cerebral cortex (26, 27).
In conclusion, advances in imaging tech¬nology provide new
diagnostic methods for assessment of cerebral vasculature
perfusion and quantitative analysis of the microcirculation£¨Side
stream dark field imaging (SDF),Sidestream
dark field imaging (SDF),Sidestream
dark field (SDF)£©
during cerebral surgery. The measure¬ments will be essential in
developing precise tools to evaluate microvascular conditions
that may affect the microcirculation, such as stroke or
hemorrhage and contribute to the further therapeutic
intervention.
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