INTRODUCTION
The clinical significance of the anatomy of cerebral perforating arteries is well known [14]: despite their relatively small diameter of below 1 mm [3, 5], their pathology results in development of serious diseases such as lacunar stroke, intracerebral haemorrhage, vascular dementia, as well as leads to severe ischaemic complications after aneurysmal subarachnoid haemorrhage and neurovascular procedures [1, 2, 8, 9, 11]. Despite advances in neuroimaging techniques, assessment of presence and function of perforating arteries remains challenging.
The aim of the study was to assess suitability of standard contrast enhanced computed tomography (CT) for visualising deep cerebral perforators by comparing its results to microscopic and micro-computed tomography (micro-CT) studies of anatomical specimens.
MATERIALS AND METHODS
Preparation of the specimens
The specimens of basal ganglia and brainstem were prepared by obtaining an unfixed brain from the cadaver, filling the arteries with contrast medium (barium sulphate), and fixing in 10% buffered formalin solution, as precisely described previously [12]. In each case, the pontine branches of the basilar artery (from the vertebrobasilar junction to the superior cerebellar arteries) or the lenticulostriate arteries were counted and measured using a microsurgical microscope.
Scanning of the specimens and radiological analysis
Every specimen was scanned with both standard clinical CT scanner (Toshiba Asteion TSX-034A, voxel size 0.25 mm, 120 kV, 150 mA) and micro-CT scanner (Nikon Metris XT H 225 ST, voxel size 0.0034 mm, 225 kV, 4 million pixels detector). Images were processed in CT Pro 3D software (Metris XT 2.2, Nikon Metrology, Belmont, CA) and Mimics Innovation Suite 24.0 (Materialise, Belgium). The pontine branches or the lenticulostriate arteries were counted in each case. The quality of visualisation of the branching sites and the course of the arteries were also determined. The numbers of arteries visualised in standard and micro-CT were compared with the Wilcoxon signed rank sum test.
Ethical approval
All procedures performed in the study were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments. The study protocol was approved by The Ethics Committee of Medical University of Warsaw, Poland (Number 138/2020).
RESULTS
Six specimens of brainstem and 17 specimens of basal ganglia were prepared and scanned by both standard and micro-CT. The median (first–third quartile) number of the pontine branches of the basilar artery amounted to 8 (7–9) and 18 (17–21) in standard and micro-CT, respectively (p = 0.031). The median (first–third quartile) number of the lenticulostriate arteries amounted to 3 (3–4) and 7 (7–8) in standard and micro-CT, respectively (p < 0.0001). Numbers of arteries counted under microsurgical microscope and visualised in micro-CT were equal in all cases — every artery filled with contrast medium was visible in micro-CT. Diameters of the perforating arteries measured with the use of microsurgical microscope ranged from 0.11 to 0.76 mm and were equal to the diameters measured on micro-CT scans with an accuracy of arterial wall thickness. In standard CT vessels of diameter below 1–2 voxel sizes (0.25–0.5 mm) were either invisible or could not be measured reliably (Fig. 1). Moreover, perforating arteries tend to have parallel course (e.g. lenticulostriate arteries branching from M2 and distal M1 entering the hemisphere in the anterior perforated substance) and standard CT does not allow to differentiate them, because of distance between the arteries being smaller than the resolution. Therefore, counting and measuring perforating arteries in standard CT scans was significantly compromised. In contrast, micro-CT scans provided clear and precise geometry of branching points and course of studied arteries (Figs. 1, 2).
DISCUSSION
The main purpose of the study was to investigate suitability of standard CT for visualising perforating arteries of cerebral circulation. Our work clearly shows that this method is ineffective and unreliable. There are several quantitative and qualitative differences between standard CT scans on the one hand and microscopic and micro-CT studies on the other.
Quantitative differences between standard and micro-CT scans
The number of visualised pontine and perforating arteries was significantly higher, when counted using microscopic or micro-CT images, which was mainly due to better visualisation of smaller vessels. The resolution of standard CT significantly limited the ability to visualise the perforating arteries, because their diameters usually do not exceed 1–2 sizes of voxel.
Moreover, the number and the diameters of perforators in the micro-CT picture was the same as under the microsurgical microscope, suggesting that these techniques can be utilized interchangeably. This advantage is important especially when studying internal microvasculature as surrounding tissues can be left intact.
Qualitative differences between standard and micro-CT scans
As presented above, the standard CT could visualise only the presence of the biggest perforating arteries. What’s more interesting, the resolution was not high enough to study geometry of branching points or courses of the arteries. The micro-CT has visualised branching points and the courses of the perforating arteries far better than the standard CT. Moreover, standard CT scans could not precisely determine the number and branching points of parallel lenticulostriate arteries or pontine branches, making determination of the parent segment impossible. These properties are crucial to plan intracranial procedures, create reliable three-dimensional models, analyse supply areas, dynamics of blood flow and forces acting on arterial walls. Micro-CT allows studying all of the aforementioned aspects.
Noteworthy, angio-CT of the head usually visualises veins to some extent, which further reduces the quality of image. It is especially important in the case of the lenticulostriate arteries because they are located parallel to the deep middle cerebral vein.
The resolution of digital subtraction angiography and magnetic resonance imaging (even 7T [4]) usually do not reach values below 0.25 mm [6, 7]: therefore, one can anticipate the same problems with visualising the perforators as in the case of CT.
Clinical relevance of the study
Our study clearly shows that absence of a structure in imaging studies is not equivalent to non-existence in real life. This conclusion is critical, when studying cerebral vasculature, as the resolution is comparable to the diameters of some arteries (including variants of the circle of Willis with hypoplastic anterior cerebral artery or posterior communicating artery) [10]. Neurosurgeons and neuroradiologists should be aware of that fact when planning and performing intracranial interventions. Micro-CT is a useful tool in preclinical studies [13, 15].
Limitations of the study
The study was specimen-based; however, standard clinical CT scanner was used. Up to date, no micro-CT scanners are admitted to clinical use. It is only possible to study previously prepared anatomical specimens. The volume of the specimen is usually restricted due to technical features of scanners.
CONCLUSIONS
Computed tomography is inappropriate to study presence, course, and geometry of the perforating arteries of cerebral circulation. Micro-CT, in contrast, is a feasible and effective method that allows for precise determination of the number, branching points, and the course of the pontine and perforating arteries. These advantages may be used for several anatomical and haemodynamic studies; however, clinical application is restricted by technical features of micro-CT scanners.
Acknowledgements
The authors sincerely thank those who donated their bodies to science so that anatomical research could be performed. Results from such research can potentially increase mankind’s overall knowledge that can then improve patient care. Therefore, these donors and their families deserve our highest gratitude.
Funding
The study was founded by the National Science Centre, Poland (award number 2020/37/B/ST8/03430, Recipient: Jerzy Małachowski). The National Science Centre had no involvement in the study design, in the collection, analysis and interpretation of data, in the writing of the manuscript, in the decision to submit the manuscript for publication. Michał Tomaszewski is recipient of Foundation for Polish Science scholarship.