Fig. 14.1
Imaging studies obtained in a patient with a cerebellar hemangioblastoma. (a) Axial contrast-enhanced MR image revealing a well enhanced tumor with a cyst in the left cerebellar hemisphere. (b) Digital subtraction angiogram (lateral view) depicting distinct angiographic staining at the late arterial phase. (c) Gray scale B-mode ultrasonography depicting a large mural nodule with a cyst. (d) Power Doppler ultrasonogram without contrast agent depicting flow signals in the tumor
As to the power Doppler US with contrast-enhancing agent, He et al. (2008) described that after intravenously administrating ultrasound contrast, the enhancement of tumors started from 9 to 20 s and the peak of the enhancement ranged from 20 to 120 s. The enhancement passed the peak and decreased from hyper-enhancement to hypo-enhancement from 80 to 120 s. The enhancement continued for 3–10 min allowed observation. The time, intensity, and distribution of the contrast enhancement on contrast-enhanced power Doppler US varied in the intracranial tumors with various pathological components. There was no enhancement in the area with cystic degeneration or necrosis of the tumor. The normal brain tissue was hypo-enhanced. The margin of the tumors was clearly identified on contrast-enhanced US images, which was ill-defined on conventional ultrasound. The edema border around the tumor was easily visualized as hypo-enhancement. The signal of power Doppler of the tumor was increased after intravenously administrating contrast-enhanced agent in all cases. The assessment of the extent of resection including the location, size, and margin of the tumors by intraoperative contrast-enhanced power Doppler US showed significant correlation with MRI. There were nine patients with suspected remaining tumor tissue who underwent second contrast-enhanced power Doppler US after the initial resection. Residual tumor tissue was not clearly identified on conventional ultrasound, which presented as an enhanced rim along the resection cavity suggested remained tumor tissue. Intraoperative biopsy was performed on suspected remained tumor tissue in the area that was minimally vascular on conventional color flow image and present as hypervascularity on contrast-enhanced US.
As to the combination with intraoperative power Doppler US and neuronavigation system, Rygh et al. (2006) used an intraoperative US-based neuronavigation system with a 4- to 8-MHz flat phased array probe with optimal focusing properties at 3–6 cm and with the capability of acquiring power Doppler US images. On the power Doppler US images, vessels were displayed as an overlay in shades of red over the tissue image according to the power of the Doppler signal. The ultrasound platform in SonoWand also has triplex imaging, but this cannot be imported and used for neuronavigation with 3D US. For tracking of the ultrasound probe, a tracking frame was attached. In addition, as to integration with the power Doppler US and neurophysiological monitoring, Nossek et al. (2011) reported the integration with motor evoked potential (MEP) monitoring and power Doppler US. They analyzed 55 patients undergoing resection of tumors located within or in proximity to the corticospinal tracts. Corticospinal tract tractography based on diffusion tensor imaging was co-registered to surgical navigation-derived images in 42 patients. Direct cortical-stimulated motor evoked potentials (dcMEPs) and subcortical-stimulated MEPs (scrtMEPs) were recorded intraoperatively to assess function and estimate the distance from the corticospinal tracts. Intraoperative US updated the navigation imaging and estimated resection proximity to the corticospinal tracts. Preoperative clinical motor function was compared with postoperative outcome at several time points and correlated with incidences of intraoperative dcMEP alarm and low scrtMEP values. The threshold level to elicit scrtMEPs was plotted against the distance to the corticospinal tracts based on diffusion tensor imaging tractography after brain shift compensation with intraoperative power Doppler US, generating a trend line that demonstrated a linear order between these variables, and a relationship for every 1 mm of brain tissue distance from the corticospinal tracts. Clinically, 71% of 55 patients had no postoperative deficits, and 9 of the remaining 16 improved to baseline function within 1 month. Seven patients had various degrees of permanent motor deficits. Subcortical stimulation was applied in 45 of the procedures. The status of 32 patients did not deteriorate postoperatively: 84% of them displayed minimum scrtMEP thresholds >7 mA. Six patients who experienced postoperative deterioration quickly recovered and displayed minimum scrtMEP thresholds >6.8 mA. Five of the seven patients who had late or no recovery had minimal scrtMEP thresholds <3 mA. An scrtMEP threshold of 3 mA was found to be the cutoff point below which irreversible disruption of corticospinal tract integrity may be anticipated. Moreover, as to the QOL changes after glioma surgery using power Doppler US, Jakola, A and Unsgård G et al. explored the relationship between QOL and traditional outcome parameters, and examined possible predictors of change in QOL (Jakola et al. 2011). They concluded that the surgical procedures may not significantly alter QOL in the average patient with glioma, but have a major undesirable effect on QOL. The active use of intraoperative US may be associated with a preservation of QOL. The EQ-5D seems like a good outcome measure with a strong correlation to traditional variables while offering a more detailed description of outcome.
As to the experimental study using an animal model, Monome Y and Furuhata H, et al. reported malignant glioma RT2 cells implanted stereotactically into the right caudate nucleus (Manome et al. 2009). They injected microbubble contrast-enhancing agent Levovist, and detected implanted glioma RT cells contrast-enhanced by Levovist.
Discussion
With skilful and technical advancement, 3D directions of feeding arteries can be detected. After removal of the tumor, no residual tumor is easily confirmed with power Doppler image. Only weak point is required for skillfulness and rapid fading of arterial image. It had better re-observe record of power Doppler US with contrast-enhancing agent in every one frame. Although subtraction method of power Doppler is also useful, B-mode image also provide background echo signals, and then power Doppler US without subtraction is enough to evaluate the tumor vasculature. The information obtained from contrast-enhanced power Doppler US is useful for surgical navigation since the appropriate approach route to access the tumor becomes quite apparent, and for an evaluation of peritumoral vessels, particularly for showing the vasculature of highly vascularized tumors such as hemangioblastomas.
As for CNS hemangioblastomas, Glasker S and Shah M, et al. indicate that power Doppler flow sonography is a reliable and useful tool to localize hemangioblastomas intraoperatively (Gläsker et al. 2011). On grayscale imaging B-mode, many hemangioblastomas were only visible if cystic. However, with the use of power Doppler US, all lesions were able to be localized intraoperatively. The distinct sonographic visualization of hemangioblastomas compared with other tumors in the posterior fossa is due to their vascular and cystic nature. To localize cerebellar hemangioblastomas, power Doppler US surpasses MRI navigation since there is no brain shift. Furthermore, US- guided puncture of large posterior fossa cysts was useful for rapid release of pressure in cases where cerebellar tissue herniated after dural opening. In surgery for intra-medullary hemangioblastomas, power Doppler US is the only possibility of navigation. This is specifically important in patients with VHL disease who frequently undergo multiple surgeries. Such minimal approaches do not allow extensive searching of a tumor that is not directly visible after dural opening. Despite the fact that Avila and coauthors (Avila et al. 1993) used an older power Doppler technique with inferior resolution compared with the current technique, the authors feel that power Doppler US is helpful for surgery of hemangioblastomas and facilitates the localization of the tumors. The use of power Doppler has advantages and disadvantages compared with other methods of neuronavigation. The advantages include the possibility of real-time imaging, fast availability, non brain shift, and the possibility to visualize vascular structures. It is the only well-established navigation method in the surgery of intra-axial tumors. The disadvantages include limitations in its resolution. More than all other navigation methods, the usefulness of USs depends on the experience of the surgeon. The image planes may be unfamiliar for inexperienced surgeons. The imaging artifacts are different from other imaging methods. In addition, based on their findings, Kanno H and co-authors suggested that data on vascularity obtained using DSA correlated with those obtained using power Doppler US, but that the US contrast- enhancing effect obtained using Levovist were different from that revealed on MR or CT images (Kanno et al. 2005). In vitro studies, animal experiments, and clinical studies have revealed that a US contrast agent Levovist, did not have toxicity or side effects. Furthermore, Levovist improves the signal intensity and the signal- to-nose ratio for several minutes. Nevertheless, there have been few studies on intraoperative power Doppler US for intracranial lesions, in which both non-enhanced and contrast-enhanced images have been examined. In addition, it is not clear what kinds of intracranial tumors might display the enhancing effect. Otsuki H and co-authors demonstrated that intraoperative harmonic subtraction images of intracranial lesions obtained using a US contrast agent were almost equal to MR angiograms and DSAs (Otsuki et al. 2001). Previously, we examined the US contrast-enhancing effect on the tumor parenchyma and assessed the relationship between vascularization seen on DSAs and the contrast enhancement of intracranial tumors seen on power Doppler USs. Our results revealed that most meningiomas, metastatic tumors, and, particularly, hemangioblastomas reflected strong signals on contrast-enhanced power Doppler US images, while some gliomas and malignant lymphomas displayed weak signals despite their contrast enhancement on CT and MR images. Bogdahn U and co-authors found that for all Grade IV gliomas contrast-enhanced transcranial color-coded US revealed not only color Doppler flow signals within the tumor parenchyma, but also atypical arterial and venous spectra (Bogdahn et al. 1994). The mechanism of US contrast enhancement has not yet been fully elucidated, but depends on the microbubble concentration in the blood pool in the tumor parenchyma, which is considered to be related to tumor vascularity and not to the destruction of the blood–brain barrier. On the other hand, contrast enhancement on CT or MR images is considered to be related to destruction of the blood–brain barrier rather than to tumor vascularity. Various abdominal tumors, such as liver cell carcinoma, liver hemangioma, metastatic liver carcinoma, gallbladder carcinoma, pancreatic carcinoma, and, in particular, liver cell carcinoma and metastatic liver carcinoma, display a high level of US contrast enhancement. In addition, these findings indicate that the US contrast-enhancing effect in abdominal tumors depends on vascular enrichment. It is demonstrated that hemangioblastomas, meningiomas, metastatic brain tumors, and some high-grade gliomas also show high-grade contrast enhancement during power Doppler US when a contrast agent is used, and that the angiographic grade was correlated with this level of contrast enhancement. In particular, hemangioblastomas, even if small, demonstrate the US contrast-enhancement effect, which is useful to determine the orientation of a tumor during an operation. Thus, the use of power Doppler US with a contrast-enhancing agent has several advantages to facilitate tumor removal. The correct approach route to access the deep-seated tumor becomes immediately apparent because feeding arteries, draining veins, and tumor vasculature are clearly shown in color images. In addition, the extent of resection in parenchymal brain tumors is easily evaluated, particularly in tumors that have abundant vessels, and finally total removal of the tumor is confirmed with the disappearance of power Doppler signals in the tumor vasculature. Although we used the US contrast agent as a single bolus injection, other enhancement protocols such as repeated bolus injections or continuous infusion should be tried. In addition, other imaging modes such as pulse inversion and 3D US may be practical when performing power Doppler US with the contrast agent. Although a neuronavigation system based on data obtained from MR or CT images makes errors because of brain shift, US provides true real-time imaging without any brain shift. A neuronavigation system that could be revised by data obtained using power Doppler US with contrast enhancement would provide more superior information during surgery.
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