Key-words:
Economical - intraoperative - neurosurgery - ultrasound
Introduction
Intraoperative imaging technology continues to evolve. Reliable intra-operative orientation
is the most important aspect of neurosurgery. Frame-based and frame-less neuronavigation,
intraoperative ultrasound (IOUS), intraoperative computed tomography (CT), and intraoperative
magnetic resonance imaging (iMRI) help the neurosurgeons to localize lesions and their
surrounding structures, aid in planning the neurosurgical approach and achieve safe
maximal resection. Intraoperative MRI and CT are generally accepted methods to achieve
this goal, but the enormous costs involved is the major obstacle in making them available
at majority of neurosurgical units worldwide, especially in developing countries.
IOUS is comparatively inexpensive, easy to use, and requires little intraoperative
equipment. Recent advances in technology have significantly improved the image quality
of IOUS.[[1]]
Intraoperative sonography has been used for many years and is an efficient imaging
adjunct. Image resolution, as well as the size and engineering of probes, have improved
considerably since 1978 when Reid first described the use of sonography for neurosurgical
guidance. Three-dimensional (3D) sonography with navigation software, which has been
introduced recently, solves the orientation problem experienced previously with 2D
sonography. The ability to show real-time anatomical details intraoperatively is valuable
and makes the surgical decision easy. Intraoperative sonography is a rapid and effective
way to localize the lesions and reduces the risk of injury to surrounding neural structures.[[2]]
The purpose of this study was to review the technical aspects and utility of intraoperative
sonography in various (n = 1250) neurosurgical procedures carried out at our tertiary
care center in a developing country.
Equipment and technique
All ultrasound imaging at our institution was performed using the ultrasound machine
of G E technology (no conflict of interest) [[Figure 12]]. Two scan probes with frequencies, MHz, and 7.5 MHz were used. Cerebral, cerebellar,
and brainstem lesions were imaged with a 5MHz transducer, whereas a 7.5-MHz transducer
is used for very superficial lesions and spinal lesions. Imaging was done with equal
clarity before opening the dura and directly on the brain surface. A sterile surgical
glove filled with jelly was used to cover the probe and better imaging, as shown in
[[Figure 12]]. Ultrasound is safe and it can be used frequently as necessary during the surgery
to assist the surgeon. As it provides immediate and accurate localization it usually
shortens the operative time. IOUS can easily differentiate solid or necrotic tumors
from cystic areas, in fact, better than either CT or magnetic resonance imaging. IOUS
provides imaging of normal structures adjacent to various lesions, the relationship
to these normal structures can be appreciated before, during, and after resection
of a lesion.
Image characteristics– normal structures. (Anatomically constant structures):[[1]]
-
Hyperechogenic (bright on iUS) structures include the falx, tentorium, choroid plexus,
and pineal gland
-
Isoechogenic (isointense on iUS) structures include the normal brain tissue
-
Hypoechogenic (dark on iUS) structures include the brainstem
-
Anechogenic (no signal) structures include the ventricles and basal cisterns [[Figure 10]].
Materials and Methods
A prospective study was carried out in our department of neurosurgery at Grant Medical
College and Sir J. J. Group of hospitals from January 2010 to May 2019. IOUS was during
various elective neurosurgical procedures done during this period as given in table
no below. A total of 1250 patients, 850 supratentorial lesions, 290 infratentorial
lesions, and 110 spinal lesions, were included in this study [[Table 1]]. IOUS was done in coronal and sagittal planes. Anatomically constant reference
points as mentioned above were used for the localization of lesion. Imaging characteristics
on IOUS were compared with CT or MRI images available.
Table 1: Site distribution
Of 850 supratentorial lesions, the most common tumor was astrocytoma followed by meningioma
and intraventricular tumors. IOUS was also used for significant number of vascular
lesions and orbital tumors [[Table 2]]. Among the 290 infratentorial lesions, the most common was medulloblastoma followed
by cerebellopontine angle meningioma and acoustic schwannoma [[Table 3]]. For spine surgeries (n = 110), it was most commonly used for intramedullary lesions
[[Table 4]].
Table 2: Supratentorial lesions
Table 3: Infratentorial lesions
Table 4: Spinal tumors
When the image morphology was compared with CT scan images, out of 320 hypodense lesions
on CT scan 300 were hypoechoic on IOUS. Eight hundred and forty lesions were hyperechoic
on IOUS out of 860 hyperdense lesions on CT scan. Furthermore, all lesions which were
isodense on CT scan were found to be isoechoic to the brain on IOUS [[Figure 11]].
Various lesions in which IOUS was used are shown below in images.
Discussion
All intracranial tumors, abscess, vascular lesions, and the congenital lesion can
be easily imaged using IOUS.
Tumors
High-grade gliomas
Large, high-grade gliomas are not difficult to locate during the surgery. IOUS imaging
helps define the borders of a lesion, provides a safe trajectory for excision of nonsurfacing
deep-seated tumor.
[[Figure 1]] shows a well-localized corpus callosal glioma with a cystic center. Ultrasound
has proven more accurate than CT scanning in differentiating cysts from necrosis since
necrotic material is more echogenic also showing the vascularity.
Figure 1: Intraoperative ultrasonography for high-grade glioma
Low-grade gliomas
Localizing a low-grade, infiltrating glioma can be difficult intraoperatively. Even
though there may be a sizable and obvious abnormality on CT scanning, the tumor appears
similar to surrounding normal brain parenchyma intraoperatively. [[Figure 3]] shows during IOUS imaging, the low-grade tumor was highly echoic to the surrounding
normal brain. However, still helps in both identification of the tumor and a much
better definition of its borders as compared to CT/MRI images.
Metastatic tumors
Localizing a small, solitary, and subcortical metastatic lesion can be difficult and
frustrating. With IOUS, lesions of virtually any size and location can be quickly
localized and the safest trajectory of excision can be planned. [[Figure 1]] demonstrates the preoperative CT and IOUS images of a small, left-sided, and subcortical
metastasis. With this precise localization, an overlying sulcus was separated and
the tumor was removed through a 10-mm incision at the base of the sulcus. Extent of
tumor excision and residual part can also be confirmed with ultrasound imaging.
[[Figure 2]] is an example of a cystic metastasis and the ultrasound image clearly demonstrates
the solid and cystic portions of the tumor. This helps the operating surgeon while
taking a biopsy of the solid portion of the tumor as well as in resection.
Figure 2: Intraoperative ultrasound in cystic glioma
Figure 3: Intraoperative ultrasound in low-grade glioma
Other tumors
IOUS is useful in surgery for meningiomas which are located deep on the falx, at the
base of the skull, intraventricular, or a convexity meningioma to plan the dural opening.
Small posterior fossa tumors such as hemangioblastomas, dermoid, ependymomas, and
medulloblastomas can be easily visualized with ultrasound and their relationship to
the fourth ventricle can defined [[Figure 5]].
[[Figure 4]] demonstrates the ultrasound image of the colloid cyst with vascular channels around
it preoperatively. Postoperative IOUS shows the complete excision of the colloid cyst.
Figure 4: Intraoperative ultrasound for colloid cyst
Figure 5: Intraoperative ultrasound in intraventricular lesions
Spinal tumors
IOUS is very useful during the surgery for spinal lesions for confirming the level
and localizing the lesion. We have used IOUS very effectively for intradural extramedullary
lesions such as neurofibromas as well as intramedullary lesions such as ependymomas,
astrocytomas [[Figure 9]].
Infectious lesions
Abscesses of varying sizes and consistency can be visualized well with ultrasound.
Depending on the stage of development of the abscess, the center may be of low, medium,
or high echogenicity. Accurate intraoperative localization allows safe excision and
immediate assessment of the residual abscess cavity as shown in [[Figure 6]] in a tubercular abscess in the cerebellum as well as in the frontal lobe.
Figure 6: Intraoperative ultrasound in tubercular abscess
Vascular lesions
A variety of vascular lesions such as arteriovenous malformations (AVM), cavernoma
can be visualized well with IOUS. Doppler mode of IOUS provides accurate imaging of
arterial feeders and venous drainage on table. This mode is very helpful in AVM surgery
as it shows real-time vascular flow. In tumor surgery, locating the main arteries
and veins relative to a tumor, patency of the venous sinuses, demonstration of vascularity
of the tumor, aid in safe resection. [[Figure 7]].
Figure 7: Intraoperative ultrasound in arteriovenous malformation surgery
Hematomas
Intracerebral hematoma, acute of subacute, are seen as hyperechogenic lesion.
Structural abnorrnalities
Virtually any variation of the ventricular system, including the fourth ventricle,
can be imaged with ultrasound. This can be helpful when there are multiple septae
within the ventricles during shunting procedures [[Figure 8]].
Figure 8: Use of intraoperative ultrasound in inserting Ventriculo peritoneal shunt
Figure 9: Intraoperative ultrasound in spinal tumors
Figure 10: Reference points for intraoperative ultrasound
Figure 11: Comparative study of intraoperative ultrasound and computed tomography brain morphology
Figure 12: Ultrasound machine used intraoperatively in our department with two probes covered
in sterile glove
Postoperative complications
After dural closure and immediately before reposition of the bone flap, a final check
with ultrasound allows the identification of an early intracerebral hematoma or hydrocephalus.[[1]],[[3]]
Disadvantages
In spite of the continued progress, IOUS does not deliver the same image quality as
iMRI or good quality CT. Its use has a learning curve and is user dependant. Unlike
neuronavigation, it is more difficult to point a site and rapidly identify it on the
ultrasound screen. Intraoperative bleeding and metal instruments can interfere with
image quality. As it does not penetrate the adult bone, it could not be used to plan
a craniotomy.
Current and future developments in intraoperative ultrasound[[1]]
Three dimensional ultrasound. intraoperative 3D ultrasound enhances the quality of
neuronavigation by allowing repeated intraoperative volumetric updates that can be
fused with preoperatively MRI images.
Contrast
Ultrasound imaging with ultrasound contrast agents is an emerging technique for evaluating
brain tumors. Contrast-enhanced ultrasound is helpful in the surgery for intracerebral
vascular lesions.
Transendoscopic ultrasonography
Significant reductions in the size of ultrasound probes have facilitated the use of
IOUS in endoscopic surgery.
Therapeutic applications
Magnetic resonance-guided focused ultrasound is a promising interventional method
in the thermal coagulative treatment of tumors, vascular malformation, functional
disorders, even for targeted drug delivery, and gene therapy.
Functional imaging
Ultrasound was able to detect the increase in regional cerebral blood flow in the
motor cortex compared to baseline during peripheral stimulation in experimental studies
on dogs. This allowed the identification of the motor strip intraoperatively using
a transdural color Doppler examination.
Conclusions
High-resolution real-time IOUS is a convenient and user-friendly method for identifying,
localizing, and characterizing the pathological focus during an operation. Such information
is very important and can enhance surgical results. The advantages include reduced
exploration and surgical time and presumably, decreased cost. It is a safe, noninvasive
technique and economical tool for neurosurgeon which is easily available. With the
advent of newer technologies, the paradigm of IOUS use is ever increasing in the field
of neurosurgery.