5 Decision Making in Cerebral Revascularization Surgery Using Intraoperative CBF Measurements

Introduction

Surgical cerebral revascularization can be performed through various extracranial-intracranial (EC-IC) bypass approaches, using a variety of different donor and recipient vessels, interposition grafts and anastomotic techniques. The specific choice of the type of bypass is dependent on several factors, incusing the ultimate goal of the operation, as well as the availability and suitability of particular donor and recipient vessels. The indications for EC-IC bypass fall into two broad categories:¹

1. Flow augmentation bypass for treatment of cerebral ischemia.

2. Flow replacement bypass for treatment of complex aneurysms or skull base tumors requiring parent vessel sacrifice.

Intraoperative blood flow measurements can provide a useful adjunct to optimizing decision making and outcomes during both flow augmentation and flow replacement bypass.

Intraoperative blood flow measurement

Intraoperative blood flow measurements can be easily and repeatedly performed using an ultrasonic flow probe (Charbel Micro-Flowprobe; Transonics Systems Inc., Ithaca, NY) that provides flow quantification in millimeters per minute, and is available in a variety of sizes to accommodate vessels ranging from 1 to 3 mm in width. The flow probe uses the principle of ultrasonic transit time to measure flow in vessels independent of the flow velocity profile, turbulence, or hematocrit.^2,³ The body of the probe consists of two ultrasonic transducers and a fixed acoustic reflector. Once the probe is placed around a vessel, a wave of ultrasound is alternately emitted from the two ultrasonic transducers, intersects the vessel, bounces off the acoustic reflector, is received by the other transducer, and converted into an electrical signal. The flow detection unit derives from these signals an accurate measure of the transit time, namely the time it has taken for the wave of ultrasound to travel from one transducer to the other. The transit time of the ultrasound is determined by the motion of blood flowing through the vessel, and the difference between the upstream and downstream transit time is used to derive the flow in millimeters per minute through the blood vessel. The accuracy of the device has been established with in vitro and in vivo studies.³

It is important when measuring intraoperative vessel flow to keep blood pressure and end-tidal carbon dioxide (CO₂) constant, as changes in these parameters will create alterations in blood flow; decrease in blood pressure and/or arterial (CO₂) will physiologically decrease the flow and vice versa. In addition, if burst suppression is used for brain protection during surgery, physiological reduction in blood flows will occur in response to the reduced metabolic demand induced by burst suppression. Therefore, flow measurements should be performed once a steady state of burst suppression has been achieved.

Bypass for flow augmentation

EC-IC bypass for cerebral ischemia remains controversial. Superficial temporal artery (STA)–middle cerebral artery (MCA) bypass is the mainstay of cerebral revascularization surgery in the setting of anterior circulation ischemia. The goal of the surgery is to augment flow to the ischemic hemisphere. The use of the procedure decreased markedly after the randomized EC-IC bypass study published in 1985 failed to demonstrate the efficacy of bypass over medical management for carotid occlusive disease.⁴ However, subsequent analysis of the EC-IC bypass trial methodology and results have identified shortcomings in the study design and implementation, and suggested that universal abandonment of cerebral revascularization for cerebral ischemia is likely not warranted.^5,⁶ One of the primary drawbacks of the trial was the lack of hemodynamic evaluation in the selection criteria for patients enrolled in the study. No objective physiological criteria were utilized to assess cerebral blood flow, and enrolled patients may have presented with ischemic events due to embolic phenomenon or small vessel disease, which would not be expected to respond to the flow augmentation provided by bypass surgery. Subsequent studies have demonstrated that careful evaluation of patients with occlusive cerebrovascular disease can identify a subgroup with severe compromise in cerebrovascular reserve capacity, who are at higher risk for stroke,⁷^–¹² and who may be reasonable candidates for surgical revascularization. Recently, the Japanese EC-IC Bypass Trial (JET) has reported favorable results for bypass in patients with internal carotid or MCA occlusive disease with hemodynamic compromise.¹³ In the United States, the role of STA-MCA bypass for recently symptomatic carotid occlusion is being re-evaluated by the Carotid Occlusion Surgery Study (COSS), which selects patients as candidates only if they demonstrate hemodynamic impairment on positron emission tomography (PET).¹⁴

In patients with ischemia who are selected to undergo flow augmentation bypass surgery, intraoperative blood flow measurements can be helpful in decision making and predicting graft patency and success. The techniques and principles for flow measurement can be similarly applied to those undergoing STA-MCA bypass for anterior circulation ischemia, as to those undergoing bypass for posterior circulation ischemia, such as occipital artery–posterior inferior cerebellar artery (OA-PICA) or STA–superior cerebellar artery (STA-SCA) bypass.

Bypass Technique

Standard surgical technique is applied to performing the bypass.^15,¹⁶ Briefly, for STA-MCA bypass surgery, a linear incision is placed along the course of the STA branch, and the vessel is dissected for a distance of approximately 8 cm. The temporalis fascia and muscle are divided and a craniotomy is performed. A recipient cortical MCA vessel is freed of its arachnoid attachments in preparation for anastomosis. The STA vessel is cleared of its connective tissue distally, cut at an oblique angle, and fish-mouthed. An end-to-side anastomosis is performed to the recipient cortical MCA branch under temporary occlusion, utilizing interrupted or continuous 10-0 nylon sutures. The dural opening is covered with gelfoam, and the bone flap replaced, removing any portion of the flap that may lead to pressure on the STA. The muscle is loosely re-approximated and the skin closed. For OA-PICA bypass, the occipital artery is dissected from beneath the skin and muscle flap after creating a posterior hockey-shaped suboccipital incision; a lateral suboccipital craniotomy extending across midline is performed. An anastomosis is created between the OA and the tonsillomedullary loop of the PICA, running below the edge of the cerebellar tonsil. For the STA-SCA bypass, or its variant, the STA–posterior cerebral artery (PCA) bypass, the recipient vessel is exposed via a subtemporal approach, as it courses around the midbrain. Anastomosis is performed under temporary vessel occlusion along a perforator-free segment of the SCA or PCA.

Intraoperative blood flow measurement technique

Application of intraoperative flow measurements to flow augmentation bypass entails making flow measurements at two points during the surgery. The first flow measurement needed is the cut flow (Figure 5–1A). The cut flow refers to the maximal potential flow capacity of the in situ donor vessel (STA or OA) once it has been dissected and cut open. The flow in the intact STA or OA in situ is generally very low, less than 5 to 10 ml/min, because of the small caliber of the vessel and the high resistance of the distal scalp tissue bed. However, once the vessel is dissected free from its surrounding tissue, and its distal end is cut, the full carrying capacity of the vessel in the absence of downstream resistance can be determined. This constitutes the cut flow of the vessel. Prior to flow measurement, the vessel is wrapped in papaverine-soaked cottonoids following dissection to prevent any reductions in flow related to spasm induced by vessel manipulation.

Figure 5–1 Intraoperative flow measurement performed in flow augmentation bypass. A, Cut flow of donor vessel. B, Bypass flow following completion of anastomosis.

The second flow measurement of importance is the “bypass flow” (Figure 5–1B). Following the anastomosis, the flow in the STA or OA graft is re-measured, which constitutes the flow in the bypass. If the resistance in the cortical recipient bed is sufficiently low, as would be expected in patients with hemodynamic compromise due to cerebrovascular occlusive disease, the bypass flow would be expected to approximate the cut flow of the donor vessel. This can be quantified as a cut flow index (CFI):

Cut Flow Index = Bypass Flow (ml/min) / Cut Flow (ml/min)

This simple index provides insight into the success of the bypass operation, with a CFI of 1.0 indicating a highly successful bypass. It is important to maintain blood pressure, end-tidal CO₂, and anesthetic technique (such as burst suppression) stable during measurements to avoid spurious physiologic changes in the blood flow measurements.

Interpretation of intraoperative blood flow measurements

The CFI serves as a useful indicator of bypass function and long-term success. In a series of 51 bypass operations performed for flow augmentation in 47 patients, CFI was found to be a significant predictor of bypass patency (p < 0.01).¹⁷ Using a CFI of 0.5 as a threshold, the bypass patency rate was 92% in cases when CFI > 0.5, compared with 50% in cases when the CFI < 0.5. Critical examination of the cases with poor CFI revealed that a logical interpretation of bypass function can be performed intraoperatively. A low CFI can be a result of varying forms of intrinsic or extrinsic errors, which can be classified as follows:

Type 1 error: Signifies that the hemodynamic status of the patient may not have been compromised to a significant degree, resulting in lack of demand on the graft. Although recognition of this type of error does not assist in altering the operative plan, information gained in this manner can help to modify the future indications for performing the procedure.

Type 2 error: Signifies a technical problem with the graft relating to the donor, the anastomosis, or the recipient vessel/bed. These fall into categories as below:

• Type 2A error is the result of donor vessel problems, such as atheromatous or calcific changes in the STA, or iatrogenic injury to the vessel during dissection.

• Type 2B error results from an anastomotic problem, such as thrombosis at the suture line.

• Type 2C error signifies a problem with graft outflow, either due to a poor recipient vessel or abnormal recipient vascular bed; this can result from a very diminutive cortical vessel that may not be able to carry the full flow of the donor, and become the limiting factor in the ultimate bypass flow; other factors such as diffuse atherosclerosis or vessel stenosis/occlusion proximal to the anastomosis may also limit the outflow from the bypass into the recipient bed (Figure 5–2).

Figure 5–2 Angiographic images following STA-MCA bypass to demonstrate a Type 2C error. A, Lateral view of carotid injection after STA-MCA bypass in a 59-year-old male with carotid occlusion. The CFI at time of surgery was only 0.27. The graft (arrow) is patent but filling only the temporal branches of the MCA distribution, secondary to a pre-existing proximal disease of the MCA that prohibits retrograde flow into the full MCA territory. B, In comparison, lateral view of carotid injection after STA-MCA bypass in a 48-year-old male with a carotid occlusion and CFI of 1.0 at the time of surgery. The bypass (arrow) fills the entire MCA distribution.

(From Amin-Hanjani S, Du X, Mlinarevich N, et al.: The cut flow index: an intraoperative predictor of the success of extracranial-intracranial bypass for occlusive cerebrovascular disease, Neurosurgery 2005;56:75–85, with permission.)

Recognition of these errors may direct intraoperative actions, such as reopening and revising an anastomosis for a Type 2B error, or considering a second bypass to a separate recipient using the anterior STA branch for a Type 2C error (as could have been performed for the case demonstrated in Figure 5–2).

Overall, intraoperative flow measurements allow immediate verification of bypass patency. Additionally, in flow augmentation bypass, the CFI provides a sensitive predictor of postoperative bypass patency. CFI > 0.5 predicts high rates of postoperative bypass patency, whereas a poor CFI can alert surgeons to potential difficulties with the donor vessel, anastomosis, or recipient vessel intraoperatively, allowing the opportunity to rectify the problem (Figure 5–3). Furthermore, a CFI closely approximating 1.0 provides physiologic confirmation of impaired cerebrovascular reserve in the recipient bed. Mere bypass patency can be judged intraoperatively with other techniques including intraoperative micro-Doppler, indocyanine green (ICG) angiography, or conventional angiography. However, given that bypasses with a low CFI are often patent at the time of surgery, the predictive value of CFI highlights the notion that mere anatomic patency may not be as useful in predicting a successful bypass procedure as the assessment of quantitative intraoperative bypass flow.