As the number of patients with unruptured cerebral aneurysms has increased, more attention has been given to the primary prevention of the aneurysm rupture⁴⁾. Endovascular intervention, one of the major treatment modalities, has begun to catch up with and surpass the surgery in the number of cases treated, based on the favorable outcomes and reduced morbidity/mortality^2,1220). In addition, recently, patients have shown a preference for endovascular intervention over surgery because of the cosmetic and psychological aspects. Scalpel surgeons are being asked to enhance their competitiveness and develop novel surgical devices and skills, such as minimally invasive keyhole surgery^8,1519), neuroendoscopic systems^7), indocyanine green (ICG) fluorescence angiography^5,18), intraoperative neurophysiological monitoring^16), and intraoperative cerebral angiography¹⁾.

Microscopic ICG fluorescence angiography is very helpful for detecting and readjusting unexpected arterial occlusion and incomplete clipping of cerebral aneurysms. However, the usefulness of ICG fluorescence angiography is limited when the microscopic view is poorly visualized or when ICG cannot absorb sufficient light to emit fluorescence. Therefore, these limitations can be overcome using the endoscopic systems that provide sufficient light illumination and excellent visualization of the operative fields. Thus, ICG fluorescence angiography would be very useful to supplement the shortcomings of microscopic ICG fluorescence. To date, there are 3 clinical reports regarding endoscopic ICG fluorescence angiography from Japan and Europe^5,1114). We independently developed an endoscopic camera system for ICG fluorescence angiography that can show the real-time simultaneous visible and fluorescent imaging. Using this system, we performed a preclinical study in swine.

ICG fluorescence began to appear on the cerebral cortex with endoscopy in approximately 25 seconds after ICG dye injection, it became peak in 1 minute, then it became pale in approximately 5 minutes. Visible color and ICG fluorescent endoscopic images of cortical vessels were simultaneously observed on the display monitor with a high resolution. In addition, real-time merging images of the fluorescent cortical vessels could be made and marked in a purple color. The real-time merging of the visible color and fluorescent images corresponded well (Fig. 4).

Since Raabe et al.¹⁷⁾ introduced microscopic ICG fluorescence angiography for cerebrovascular surgery in 2003, it has become a ubiquitous piece of equipment for aneurysm surgery as well as micro-anastomosis and surgery for arteriovenous fistulas and malformations. During aneurysm surgery, real-time identification of the blood flow in the vasculature within the operative field helps to improve surgical outcomes and reduce perioperative complications. This is because the repositioning and addition of clips can be promptly determined on the occlusion of parent arteries and perforators or incomplete clipping of the aneurysms. Intraoperative cerebral angiography is a good alternative¹¹⁾. However, it is invasive and has a limitation to visualize the small perforators around the aneurysms in spite of the superiority in the acquisition of 3-dimensional imaging around the clipped aneurysms. In addition, supplementary facilities for intraoperative cerebral angiography are needed, and a time lag between the identification of compromise of the normal arteries and the repositioning of clips can result in an irreversible ischemic complication. On the other hand, microscopic ICG angiography also has some shortcomings : vascular structures beyond the line of microscopic view are hard to visualize and ICG fluorescence is weakly detected for the deeply located structures because of the limited spatial resolution and light illumination of microscopy. When keyhole surgery is performed, such limitations in microscopic ICG angiography become more profound. To overcome the drawbacks of microscopic ICG angiography, we decided to develop endoscopic ICG fluorescence angiography.

In fact, endoscopic ICG angiography has been applied in other surgical fields before it was introduced in the field of neurosurgery, based on the property of ICG, which is circulated through the blood vessels, metabolized in the liver, and excreted via the bile duct into the intestines. Examples of the surgical applications of this technique include the detection of the sentinel lymph nodes of patients with gastric cancer^13), visualization of bleeding points in the gastrointestinal tract^9), assessment of tissue perfusion and bile tree in hepatopancreatobiliary surgery^22), and evaluation of free flap perfusion³⁾. Neuroendoscopy itself has been used mainly in skull base surgery via the transnasal approach and aneurysm surgery^7,1021). Meanwhile, the use of endoscopic ICG angiography in aneurysm surgery has recently been introduced^5,614). The authors consider endoscopic ICG angiography to be useful for confirming the occlusion of the aneurysms and the patency of blood flow in the parent arteries and perforators, which could not be visualized under the microscopy and its ICG angiography. Moreover, it is possible in the endoscopic ICG angiography to better magnify the areas of interest^5), obtain longer ICG fluorescence duration, and be more useful in the ruptured aneurysms^11), compared to the microscopic system. Light illumination from microscopy alone is reported to disturb the detection of ICG fluorescence with endoscopy⁵⁾.

The advantage of our endoscopic ICG angiography system is that ICG fluorescence and visible color imaging can be simultaneously visualized and merged in a real-time manner. Previous microscopic or endoscopic ICG angiography systems cannot help but to demonstrate the visible color or NIR fluorescence imaging one at a time such that surgeons may feel some difficulty in comparing the real structures with fluorescence images during the surgery. However, the size of our prototype camera is larger than the previous one, which is an improvement.

We have further plans to improve this endoscopic ICG angiography technique. First, an endoscope with smaller diameter and flexibility may be more useful because the operative space is very narrow without retracting brain tissue or drilling bony structures. As the diameter becomes smaller, imaging resolution and transmission of the light illumination and emitting fluorescence tend to be diminished. Such technical considerations should be made. Second, distinct from the endonasal approach, which is performed through the bony nasal cavity, endoscopy with ICG angiography during aneurysm surgery reaches and stays around the targeted vascular structures intradurally adjacent to the brain under microscopic inspection. Separate displays for microscopy and endoscopy may be detrimental and time-consuming because endoscopy can damage the adjacent cerebrovascular structures. A unified display system that can visualize both the microscopic and endoscopic imaging in one piece may be useful in terms of safety and convenience.

Our endoscopic ICG fluorescence angiographic system showed satisfactory imaging resolution in a swine study. Different from the previous systems, it was possible to simultaneously display visible color and ICG fluorescent images, and make a real-time merging images of them. Technical supplementation and approval for the clinical implication are expected to support the application of aneurysm surgery as well as surgery for other cerebrovascular diseases.