Arteriovenous malformations (AVMs) are intricate vascular anomalies where a tangled web of arteries and veins bypass the capillary system (1). This abnormal connection poses significant risks, including intracranial hemorrhage, seizures, and progressive neurological deficits (2). Surgical resection is often the treatment of choice for AVMs, necessitating precise intraoperative imaging to ensure complete removal while preserving critical vascular structures in unruptured Spetzler-Martin grade I and II patients (3). A fundamental principle of neurosurgical AVM treatment is to maintain perfusion by avoiding unnecessary vascular compromise. In the resection of intracerebral AVMs, this involves excluding uninvolved vessels and protecting nidal draining veins until arterial feeders are disconnected (1). Indocyanine green (ICG), a fluorescein-like dye, can be intravenously injected to help delineate vascular anatomy under direct visualization. ICG videoangiography (VA) is particularly useful as it allows the surgeon to directly and immediately assess the integrity of vessels under the intraoperative microscope (4, 5). ICG VA has become a valuable tool in neurosurgery, particularly for AVM management (6). ICG is a fluorescent dye that, when excited by near-infrared light, provides real-time visualization of blood flow (4, 5). This allows surgeons to delineate vascular structures clearly and verify complete resection of AVMs while protecting vital adjacent vessels (6). The technique was notably integrated into surgical microscopes by Raabe et al. in 2003, significantly enhancing intraoperative assessment during vascular neurosurgery (4). ICG VA is praised for its simplicity, rapid deployment, and real-time feedback. Despite the low toxicity profile (e.g., hypersensitivity reactions in iodine allergy) of ICG VA, modern intraoperative imaging methods strive to work without the application of contrast agents (7, 8). Hyperspectral imaging (HSI) is a novel imaging modality that captures a wide spectrum of light beyond the visible range (9). This technology provides detailed spectral information, enabling the differentiation of various tissue types based on their unique spectral signatures. Unlike ICG, HSI does not require the application of any contrast agents, making it a non-invasive alternative with minimal patient risk. HSI offers fast image acquisition and can be integrated into the surgical workflow without significantly prolonging operation times (10). Recent advancements have showcased HSI's potential in neurosurgery, particularly in tumor resection and tissue differentiation (9, 10). However, the present case illustrates the first use of intraoperative HSI in brain AVM surgery ability to demonstrate vascular structures and tissue characteristics, which is crucial for the accurate resection of AVMs.

In this case report, we detail our initial experience using Hyperspectral Imaging (HSI) and Indocyanine Green Videoangiography (ICG VA) together to visualize perfusion during brain AVM surgery. The combination of these advanced imaging techniques enhances the intraoperative assessment of vascular structures and tissue perfusion, offering a comprehensive approach to managing complex AVMs.

ICG VA is a well-established fluorescent dye activated by near-infrared light (805 nm). Its fluorescence properties make it an invaluable tool for real-time angiography, allowing surgeons to visualize vascular anatomy and assess tissue perfusion dynamically. The utility of ICG VA in neurosurgery has been extensively documented, particularly for its role in the visualization of blood flow in small vessels and the assessment of vascular integrity during aneurysm surgery. Studies have demonstrated that ICG VA can accurately depict vascular flow and identify incomplete aneurysm occlusion or stenosis, which is crucial for ensuring optimal surgical outcomes (4, 5). In our case, the use of ICG VA allowed for the clear delineation of AVM feeding and draining vessels, facilitating a precise and safe resection. HSI represents a cutting-edge technology that captures a broad spectrum of light beyond the visible range, offering detailed spectral information about tissue properties (9). HSI does not require any contrast agents, making it a non-invasive and fast imaging modality. This technique provides several false-color images representing physiological parameters such as tissue oxygenation, tissue water content, and perfusion indices, enabling a thorough analysis of tissue viability and perfusion status (16, 17). For instance, HSI has been explored for its potential to enhance the visualization of brain tumors and assess cerebral perfusion (10, 18). Furthermore, in neurovascular field such as Moyamoya disease, HSI has been used to predict cerebral hyperperfusion syndrome post-bypass surgery, highlighting its ability to provide detailed perfusion maps and guide surgical decisions (18). In our case, HSI complemented ICG VA by offering a more comprehensive analysis of tissue perfusion and vascular integrity, thereby improving the accuracy of the AVM resection. For the present workflow we use the TIVITA® system produced by Diaspective Vision GmbH (Am Salzhaff-Pepelow, Germany). The exact technical characteristics of this imaging method have been previously published (19). This HSI system enables us to measure a spectrum of a range from 500 nm to 1,000 nm in wavelength. Besides parameters like oxygen saturation, perfusion, and content of hemoglobin, water, and fat, this contactless and contrast-agent-free imaging process shows detailed spectroscopy of several regions of interest with their absorbance spectra within a few seconds. The combination of HSI and ICG VA in this case provided a synergistic approach to intraoperative imaging. While ICG VA offered real-time visualization of blood flow and vascular structures, HSI provided detailed spectral data that allowed for the visualization of surrounding tissue characteristics (e.g., oxygenation, perfusion, water content) and identification of subtle perfusion anomalies. This dual-modality approach might enhance the precision and safety of the AVM surgery, ensuring a more complete resection with minimal risk of residual nidus. It might be worth mentioning at this point that, due to the rapid wash-out phase of ICG in the brain, the HSI images are likely not affected by artifacts. For example, in procedures involving the intestines, HSI typically needs to be performed before the administration of ICG (19, 20). However, the current workflow is limited by its ergonomics because the present HSI system is not integrated in the microscope and provides no real-time guidance in terms of hyperspectral video imaging. One of the potential future main advantages of more advanced and integrated HSI systems in the field of AVMs might be its ability to provide detailed spectral information of surrounding brain tissue before and after surgical excision of the AVM without the need for intravenous contrast agents, reducing the risk of adverse reactions and simplifying the imaging process. Additionally, HSI's fast acquisition time and non-contact nature make it a practical tool for intraoperative use in terms of potential low risk for surgical site infections and brain injury. Conversely, the real-time feedback and proven efficacy of ICG VA in visualizing vascular structures make it an indispensable tool in complex neurosurgical procedures. An important consideration and aspect in future HSI studies investigating AVM surgery is the change in perfusion of brain tissue surrounding the AVM following resection. This phenomenon, known as normal perfusion pressure breakthrough (NPPB) syndrome, can lead to hemorrhage and edema in the surrounding normal brain tissue due to the sudden restoration of normal perfusion pressures to previously hypoperfused areas (21). This occurs because the arteries supplying the AVM become dilated and lose their ability to autoregulate blood flow. Immediately following AVM removal, these arteries are unable to constrict adequately, resulting in hyperperfusion and potential damage to surrounding brain tissue. A study by Asgari et al. (22) demonstrated that intraoperative near-infrared spectroscopy (NIRS) with surface application on the cortex could detect hyperemia in the cortex adjacent to AVMs after resection. Their findings indicated significant increases in cortical oxygen saturation (StO₂) and blood volume (BV) post-resection, suggesting that these parameters are indicative of hyperemia and potential complications. As we observed similar findings with increased saturation of oxygen (see Figure 4E) of the surrounding brain regions after AVM resection with novel postoperative neurological symptoms, our parameters suggest that HSI as a contrast-agent free and contactless quick-to-use modality could play a crucial role in identifying patients at risk of NPPB by providing detailed maps of tissue perfusion and oxygenation, allowing for real-time monitoring and identification of those patients at risk for NPPB after AVM surgery. Using HSI, we observed a continuous increase of St0₂ in identical ipsilateral frontal brain regions next to the AVM resection site from beginning of intradural dissection to achievement of total AVM excision (see Supplementary Video). Despite the present case is the first to show HSI as an intraoperative imaging tool in AVM brain surgery and its potential use in the identification of those patients at risk for NPPB, the observed findings in HSI and the perioperative events reported is an isolated finding and needs to be evaluated using a larger set of AVM patients undergoing surgical excision. Furthermore, the present version of the institutional HSI system does not allow real-time analysis of brain perfusion at video-rate, which might provide more insight into the flow dynamics and changes of perfusion during the microsurgical steps of AVM resection. However, we introduced this dual intraoperative imaging approach (HSI & ICG VA) at the present institution and will further evaluate the use of HSI in neurovascular surgery as part of an ongoing prospective study.

We successfully demonstrated the first combined use of HSI and ICG VA for visualizing perfusion during brain AVM surgery. This dual-modality approach provided comprehensive intraoperative assessment, enhancing surgical precision and safety. Future integration of HSI into the surgical workflow holds potential for further improving outcomes in AVM resection by enabling detailed, contrast-agent-free perfusion mapping.