Evaluation of Hemodynamic Change by Indocyanine Green-FLOW 800 Videoangiography Mapping: Prediction of Hyperperfusion Syndrome in Patients with Moyamoya Disease

Abstract

Objective: Hyperperfusion syndrome (HPS) after bypass surgery for moyamoya disease (MMD) mainly results from redistribution of blood flow, which leads to poor outcomes, while effective methods to predict HPS are still lacking. Indocyanine green (ICG) videoangiography can assess regional cerebral blood flow changes semiquantitatively with the application of FLOW 800 software. The purpose of this study was to investigate whether the intraoperative evaluation of local hemodynamic changes around anastomotic sites using FLOW 800 videoangiography mapping can predict the incidence of HPS and clinical outcomes.

Methods: Of the patients who were diagnosed with MMD in our hospital between August 2018 and December 2019, who underwent superficial temporal artery-middle cerebral artery bypass surgeries, we investigated 65 hemispheres (in 62 patients) in which intraoperative ICG analysis was performed using FLOW 800 (Zeiss Meditec, Oberkochen, Germany) to evaluate the local cerebral hemodynamics before and after anastomosis. Regions of interest were set at more than 2 points on the brain surface according to the location and situation of recipient arteries in the surgical area. Peak cerebral blood volume (CBV), regional cerebral blood flow (CBF), and time to peak (TTP) were calculated from the selected points. As the data were available intraoperatively, anastomoses were performed in a suitable area. According to the occurrence of HPS, patients were divided into the asymptomatic and symptomatic groups, from which hemodynamic parameters were compared. Furthermore, ROC analysis was performed to determine the diagnostic accuracy of change rates in CBV, CBF, and TTP (i.e., ΔCBV, ΔCBF, and ΔTTP) for predicting HPS.

Results: Data from the 62 patients were analyzed, and all patients were closely assessed during hospitalization after the procedures. The values of ΔCBV and ΔCBF were significantly higher in the symptomatic group (p < 0.01), while ΔTTP is slightly lower in the symptomatic group with no statistical differences (p = 0.72). Hemodynamic parameters including ΔCBV and ΔCBF, calculated by FLOW 800, had high sensitivity and specificity according to the ROC curve (ΔCBV: AUC = 0.743, 95% CI, 0.605-0.881, p = 0.002; ΔCBF: AUC = 0.852, 95% CI, 0.750-0.954, p < 0.01), which could be used as predictors for HPS.

Conclusions: Intraoperative ICG-FLOW 800 videoangiography mapping is a safe method which can reflect hemodynamic characteristics in the surgical area for MMD, the findings of which correlate with the occurrence of HPS. Parameters including ΔCBV and ΔCBF are proven to be efficient in the prediction of HPS.

Figure 1

ICG was performed after a craniotomy to identify alternative recipient arteries in the surgical area (a). Color mapping was available to locate the hypoperfusion area for anastomosis. Regions of interest were set at the artery branch and parameters, such as cerebral blood flow (CBF, slope), cerebral blood volume (CBV, peak), and time to peak (TTP, delay time), which could be calculated and compared to confirm local cerebral hemodynamics for surgical decision making. Postoperative ICG-FLOW 800 was performed again (b) to confirm the patency of the anastomosis and to compare blood flow changes in the previously selected area.

Figure 2

Subgroup analysis of the hemodynamic parameters (ΔCBF, ΔCBV, and ΔTTP) between the asymptomatic group (blue box) and the symptomatic group (red box). ΔTTP was slightly lower (-0.90% vs. 6.19%, p = 0.559) in the symptomatic group compared with the asymptomatic group, while ΔCBV (68.21% vs. 23.63%, p < 0.01) and ΔCBF (158.08% vs. 23.98%, p < 0.01) were significantly higher in the symptomatic group.

Figure 3

ROC analysis for each hemodynamic parameter correlated with clinical outcome. Results showed that diagnostic accuracy of ΔTTP was low (AUC = 0.597). As for ΔCBV, the AUC was 0.743 (95% CI, 0.605–0.881, p = 0.002), with the best threshold of 66.35 (sensitivity = 0.5, 1–specificity = 0.067, Yoden's index: 0.433). Similarly, the AUC was 0.852 for ΔCBF (95% CI, 0.750–0.954, p < 0.01), and the best threshold was 62.06 (sensitivity = 0.85, 1–specificity = 0.067, Yoden's index: 0.606).

Figure 4

DSA showed occlusion of R-ACA and stenosis of R-MCA with moyamoya vessel formation (a). MR scan revealed old infarction on right temporal-occipital lobe (b, c). ASL confirmed hypoperfusion in the right hemisphere (d). Recipient artery was selected from five optional vessels from ICG-FLOW 800 mapping (e, g). Anastomosis was performed in vessel 3 (blue box), and hemodynamic analysis showed an obvious increase of ΔCBF and ΔCBV (f, h). Three days after the procedure, the patients suffered from an epileptic seizure and were controlled by benzodiazepine. MR follow-up confirmed HPS with the evidence of increasing blood flow but not new infarction (i, j).