Intraoperative evaluation of local cerebral hemodynamic change by laser speckle contrast imaging for predicting postoperative cerebral hyperperfusion during STA-MCA bypass in adult patients with moyamoya disease

Abstract

Cerebral hyperperfusion (CHP) occurred frequently after direct superficial temporal artery–middle cerebral artery (STA-MCA) bypass surgery for moyamoya disease (MMD). We analyzed cortical microvascular density (CMD) and the change of cerebral blood flow (LΔCBF) using intraoperative laser speckle contrast imaging (LSCI) on 130 hemispheres of 95 consecutive adult patients with MMD. The demographic characteristics, cortical hemodynamic sources, bypass methods, intraoperative blood flow data, and relative CBF changes on single-photon emission computed tomography (SPECT) examination (SΔrCBF) were compared between the groups with and without CHP. The median values for CMD, LΔCBF, and SΔrCBF were significantly higher in the CHP group than in the non-CHP group (CMD 0.240 vs 0.206, P = 0.004; LΔCBF 2.285 vs 1.870, P < 0.001; SΔCBF 1.535 vs 1.260, P < 0.001). Multivariate analysis revealed that hemodynamic sources of recipient parasylvian cortical arteries from MCA (M-PSCAs), end-to-side (E-S) bypass method, CMD ≥ 0.217, and LΔCBF ≥ 1.985 were the risk factors for CHP. Intraoperative LSCI was useful for evaluating hemodynamics and predicting CHP in patients with MMD.

Keywords

Laser speckle contrast imaging moyamoya disease STA-MCA bypass cerebral hyperperfusion side-to-side bypass method

Introduction

Moyamoya disease (MMD) is a chronic cerebrovascular disease which characterized by progressive occlusion of the basal arteries of the circle of Willis in association with an abnormal vascular network at the base of the brain.^1
–3 Ischemic or hemorrhagic stroke resulting from MMD carries a high risk of morbidity and long-term disability worldwide. Direct revascularization has already proven to be effective for the treatment of adult MMD.^4
–7 However, postoperative complications, such as transient neurological deficits (TNDs) during the postoperative acute stage owing to developed cerebral hyperperfusion (CHP), are reasons for these patients’ inferior prognosis.^8
–13 To date, it is hard to accurately predict CHP before or during operation. Various methods (such as micro-Doppler ultrasonography, thermal diffusion probe, indocyanine green videography [ICG-VA], etc.) have been reported for intraoperative cerebral blood flow (CBF) monitoring.^14
–21 While ICG-VA is commonly used and can be applied to evaluate vascular patency and intravascular blood flow change during bypass, it fails to visualize microcirculatory flow and tissue perfusion.^19,22,23 The relationship between intraoperative microcirculation perfusion and postoperative CHP is unclear. Furthermore, CBF evaluation is usually performed during the first few days after surgery, when CHP may have already occurred, making it unsuitable for CHP prediction. If the onset of CHP could be predicted intraoperatively, early interventions for reducing CHP may result in fewer perioperative complications. Thus, it is aroused to develop a reliable method for intraoperative microcirculatory flow monitoring to predict postoperative CHP.

Laser speckle contrast imaging (LSCI) is a wide-field optical imaging scheme capable of quantitative imaging based on dynamic light scattering off moving particles.²⁴ Since Fercher and Briers firstly applied it to study retinal vasculature, LSCI was widely used to image vascular structure and associated hemodynamic changes.²⁵ Hecht and Kazmi et al. demonstrated that intraoperative LSCI was safe and effective in the process of neurosurgery.^24,26 LSCI represents a new modality that can set regions of interest (ROIs) for arbitrary shapes and sites, for these ROIs, direct parameters related to the local cerebral hemodynamics, such as cortical microvascular density (CMD) and CBF, can be calculated. In this study, we evaluated the hemodynamic changes around the anastomosis site before and after the superficial temporal artery-middle cerebral artery (STA-MCA) bypass in patients with MMD using LSCI and investigated whether the change could predict the incidence of CHP.

Methods

Study design and inclusion criteria

We retrospectively analyzed the data from 95 adult patients (130 hemispheres) with MMD who underwent STA-MCA bypass with encephalo-duro-myo-synangiosis (EDMS) revascularization procedure performed by the same neurosurgeon (J.Z.) between September 2021 and September 2022. The earlier 45 hemispheres underwent the conventional E-S bypass method, while the later 85 hemispheres underwent the novel side-to-side (S-S) bypass method.²⁷ The diagnosis of MMD in all patients was established using digital subtraction angiography (DSA). All patients satisfied the diagnostic criteria set by the Research Committee on Spontaneous Occlusion of the Circle of Willis of the Ministry of Health, Labour and Welfare, Japan.^2,3 The inclusion criteria for this study, aligned with our surgical indications, comprised the following: 1) the presence of ischemic symptoms or history of hemorrhage; 2) single-photon emission computed tomography (SPECT) confirmed hemodynamic compromise; 3) modified Rankin Scale (mRS) score less than 2; 4) absence of major cerebral infarction; and 5) the patency of the anastomosis was confirmed by a postoperative magnetic resonance angiography (MRA) scan. All hemispheres that did not match these criteria were excluded from the study.

This study protocol was approved by the Zhongnan Hospital Ethics Committee (approval number: Kelun-2017005) and was performed in accordance with the Declaration of Helsinki revised in 1983. Written informed consent was obtained from all study participants.

Surgical procedures and patients’ management

The standard surgical procedure of the conventional E-S STA-MCA and the novel S-S STA-MCA anastomoses were almost the same as those already described in previous articles.^6,27 In all surgeries, under general anesthesia mainly using propofol and remifentanil, the STA-MCA (M4) anastomosis after frontotemporal craniotomy. To avoid postoperative compression of the brain surface by insertion of the temporal muscle, we drilled out the inner layer of the bone flap and created a wide bone window on the side of the EDMS flap. The patency was confirmed by ICG-VA intraoperatively. The intraoperative mean arterial pressure (MAP) (90–100 mmHg) and end-expiratory carbon dioxide (CO2) concentration (38–42 mmHg) were maintained at a constant level when the LSCIs were scanned twice before and after anastomosis. (Figure 1(a)). Post-surgery, all patients underwent a standardized intensive management strategy in the Neurosurgical Intensive Care Unit (NICU). We maintained body fluid balance, and the target systolic blood pressure was kept between 120 and 140 mmHg.²⁸ All patients received postoperative computerized tomography (CT) on postoperative day (POD) 1 to rule out procedure-related hemorrhage and we routinely administered 100 mg of aspirin per day from POD 1. Both SPECT and MRI, including diffusion-weighted images, T2-weighted images, and MRA were performed on POD 3 to evaluate the perfusion status of the brain, whether acute cerebral infarction presence and patency of the anastomosis.

Figure 1.

Illustration of data recording and calculation. (a) The intact parietal STA branch was the donor artery (white arrow). The MCA (M4) was the recipient artery (yellow arrow). Excellent S-S anastomosis (red circle). Software created a dynamic, two-dimensional, and color-coded map of CBF (flux image: red = high flow; blue = low flow). ROIs were set at 3 locations around the anastomotic site to record CBF and CMD. (b) Threshold processing of cerebral cortical microvascular and (c) the formulas for calculating LΔCBF and CMD.

Technical specifications and device setup of LSCI

A random interference phenomenon called laser speckle will appear when an irregular structure (e.g., blood cell) is illuminated by laser light. The integrated charge-coupled device (CCD) camera recorded the speckle signal, and the software created a dynamic, two-dimensional, and color-coded map of CBF (flux image: red = high flow; blue = low flow), which was consistent with the blood flow velocity in the tissue, commonly referred to as “flux”. Previous reports have demonstrated the feasibility, safety, and effectiveness of LSCI in neurosurgical procedures.^24,26,29

In our study, all LSCI measurements were performed using a laser speckle device (SIM BFI HR Pro, SIM Opto-Technology Co, Ltd, Wuhan, China, www.simopto.com) and purpose-designed data acquisition software (SIM BFI measurement software, Version V2.0, SIMBFI HR PRO, CN), the device was mounted on a mobile trolley connected by a rigid, flexible arm allowing re-adjustments to standardize height and to reduce motion artifacts, the lens was positioned approximately 250 mm above and perpendicular to the exposed frontotemporal lobe after craniotomy and durotomy according to the manufacturer’s recommendation, and radiates the laser to illuminate the investigated area. After the original images were acquired, regions of interest, which need to avoid thick blood vessels, were drawn manually as circles were set at more than 3 locations on the brain surface around the anastomotic site; Second, the CBF of the ROI regions automatically generated by the software before and after anastomosis, and then the change rate of CBF on LSCI (LΔCBF) was calculated using the formula (postanastomosis mean CBF/preanastomosis mean CBF). Last, LSCI images would be thresholded for cortical microvascular density (CMD) calculations, CMD is calculated as the ratio of the area of blood vessels after thresholding to the area of the ROI, as shown in Figure 1.

Measurement of relative cerebral blood flow with SPECT

The technetium-99m ethyl cysteinate dimer brain SPECT images were scanned under controlled blood pressure within 3 days before and after surgery in all patients. The anastomosis site and the exact vascular territory supplied by the graft were confirmed on postoperative axial MRA and SPECT. rCBF of manually defined regions of interest (ROIs) obtained from circles with a 1 cm diameter in the cortical areas at the anastomosis sites and ipsilateral cerebellum. The ipsilateral cerebellum hemisphere was referred as to the inner normal control, and we defined the rCBF in the ROI around the anastomosis site as the mean radioactive count in anastomotic ROIs/mean radioactive count in the ipsilateral cerebellar ROIs (Figure 5(d)). The diagnostic criteria for radiological CHP in the present study included as follows: 1) the rCBF at the vascular territory supplied by the graft was more than 150% increase; 2) visualization of STA-MCA bypass by MRA on POD 3; 3) the absence of any ischemic changes by diffusion-weighted imaging; and 4) the absence of other pathologies such as compression of the brain surface by the temporal muscle inserted for indirect pial synangiosis, ischemic attack and increases in CBF secondary to seizure.⁸ Alternatively, patients were considered to have symptomatic hyperperfusion if they exhibited TNDs, such as aphasia, limb numbness, decreased muscle strength, hemiparesis, seizure, dysarthria, severe headache, and facial palsy, etc. corresponding to the area where hyperperfusion occurred after surgery.³⁰ All image processing and parameter measurements were performed by two specialized radiologists who were blinded to the clinical condition of the patients, if the interpretations of the 2 observers conflicted, a discussion was held to reach a consensus.

Statistical analysis

All statistical calculations were performed with SPSS Statistics Desktop version 22.0 (IBM Corp.). Differences in the distribution of continuous variables were analyzed using the Shapiro-Wilk (SW) normality tests. Skewedly distributed continuous variables utilized the Mann-Whitney U-test, and the data were presented by medians and interquartile ranges (IQRs). Categorical variables were analyzed in contingency tables with the chi-square test and Fisher’s exact test. Receiver-operating characteristic (ROC) analysis was carried out to determine the optimal cutoffs of CMD and LΔCBF for predicting CHP. A multivariate logistic regression analysis was conducted to evaluate the association between multiple variables with postoperative CHP. Spearman’s rank correlation coefficient evaluated the association between parameters (i.e., CMD and LΔCBF) of LSCI and the onset or duration time of symptomatic CHP. Results with p < 0.05 were considered significant.

Results

Within a 12-month period, two cases of cerebral hemorrhage and four cerebral infarctions developed in all patients who underwent bypass surgery. Those events occurred immediately or within 3 days after the surgery, after the exclusion of these 6 hemispheres, 95 adult patients with MMD (130 hemispheres; mean [range] age 50.38 [19–73] years; 54 females [41.5%]) satisfied the clinical inclusion criteria. CHP was identified as occurring in 32 (24.6%) of the 130 hemispheres after revascularization, of these, TNDs occurred in 9 hemispheres (28.1%), and all the complications disappeared gradually without any residual symptoms. In univariate analysis, there were no statistical differences observed between the patients with and without CHP regarding age, sex, initial onset type, Suzuki stage, admission mRS score, surgical side, or baseline cerebral blood flow (bCBF) (all P > 0.05). However, the incidence of hypertension (56.3% vs 35.7%), M-PSCAs (59.3% vs 30.6%), and bypass method (E-S [68.8%] vs [23.5%]) showed accentuated significant differences between the two groups. Detailed descriptions of the enrolled patient groups were summarized in Table 1. The detailed characteristics and hemodynamic data of nine patients who suffered TNDs were described in Supplementary File 1.

Table 1.

Comparison of basic characteristics and hemodynamic data.

	Univariate analysis			Multivariate analysis
	CHP (n = 32)	Non-CHP (n = 98)	P Value	OR	95% CI	P Value
Age, yrs	51 (45.0–59.8)	51 (44.8–56.0)	0.482
Female sex	15 (46.9)	39 (39.8)	0.480
Hypertension	18 (56.3)	35 (35.7)	0.040			0.638
Onset manifestation			0.773
Ischemic	21 (65.6)	67 (68.4)
Hemorrhage	11 (34.4)	31 (31.6)
Suzuki stage			0.679
II	6 (18.7)	11 (11.2)
III	17 (59.4)	53 (54.1)
IV	6 (12.5)	25 (25.5)
V	3 (9.4)	9 (9.2)
Admission mRS score	1.5 (1–2)	2.0 (1–2)	0.323
M-PSCAs	19 (59.3)	30 (30.6)	0.004	4.221	1.260–14.137	0.020
Surgical side			0.938
Lt	20 (62.5)	62 (63.3)
Rt	12 (37.5)	36 (36.7)
Bypass method			<0.001
E-S	22 (68.8)	23 (23.5)		4.211	1.311–13.529	0.016
S-S	10 (31.2)	75 (76.5)
CMD	0.240 (0.220–0.250)	0.206 (0.191–0.253)	0.004	7.994	2.244–28.483	0.001
bCBF	219.10 (197.48–254.97)	209.36 (167.31–225.21)	0.199
LΔCBF	2.285 (2.015–2.418)	1.870 (1.800–1.970)	<0.001	7.821	2.109–29.005	0.002
SΔrCBF	1.535 (1.513–1.558)	1.260 (1.238–1.320)	<0.001

P < 0.050 were considered significant.

Values are shown as number (%) or median (interquartile ranges) unless indicated otherwise.

Relationships between parameters from LSCI or SPECT and postoperative CHP

From before to after the bypass surgery, CBF obtained from LSCI increased significantly in both the CHP and non-CHP group (Figure 2(a) to (d)). The parameters (LΔCBF, CMD) calculated by LSCI indicated significant differences between the patients with and without CHP (Figure 2(f) and (g)); CMD was significantly higher in patients with CHP than in those without CHP: median 0.240 (IQR 0.220–0.250) and median 0.206 (IQR 0.191–0.253), respectively (P = 0.004); LΔCBF was significantly higher in patients with CHP than in those without CHP: median 2.285 (IQR 2.015–2.418) and median 1.870 (IQR 1.800–1.970), respectively (P < 0.001). From the data on SPECT within 3 days before and after bypass surgery, rCBF augmented in both the CHP and non-CHP group (Figure 2(h)). Elevated SΔrCBF calculated by SPECT was observed in patients with CHP than in those without CHP: median 1.535 (IQR 1.513–1.558) and median 1.260 (IQR 1.238–1.320), respectively (P < 0.001), as summarized in Table 1.

Figure 2.

Illustration of results for intraoperative and perioperative blood perfusion using LSCI and SPECT. (a–d) Intraoperative blood flow analysis using LSCI. The enhanced red-colored image after anastomosis completion indicated an augmentation of cerebral cortical perfusion and the patency of vascular anastomosis after bypass procedures. (e) No statistical differences were observed between the patients with and without CHP in the bCBF. (f, g and h) The parameters (CMD, LΔCBF and SΔrCBF) calculated by LSCI or SPECT show a significant difference between the groups with and without CHP. In the group with CHP (compared with the group without CHP), CMD was significantly higher (median 0.240 vs 0.206, P = 0.004), LΔCBF was significantly higher (median 2.285 vs 1.870, P < 0.001), and SΔrCBF was significantly higher (median 1.535 vs 1.260, P < 0.001). Boxplots indicate the median value (horizontal line within box) and the 25th (lower limit of box) and 75th (upper limit of box) percentiles. The error bars indicate the maximum and minimum values. **P < 0.01; **** P < 0.0001.

Receiver operating characteristic curve analysis for postoperative CHP

ROC analysis yielded LΔCBF ≥ 1.985 and CMD ≥ 0.217 as the optimal cutoff values for CHP prediction, and the area under the curve (AUC) were 0.726 and 0.658, respectively (Figure 3). In general, LΔCBF (sensitivity 81.3%, NPV 92.8%, specificity 79.6%, PPV 55.3%) demonstrated superior accuracy compared to CMD. The sensitivity, specificity, PPV, and NPV of the corresponding LSCI parameters were described in Supplementary File 2.

Figure 3.

ROC curve analysis of LΔCBF and CMD for predicting postoperative CHP. The ROC curve revealed that the Youden index reached the maximum when the cutoff values for LΔCBF and CMD were set at 1.985 and 0.217 respectively. The area under the curve (AUC) were 0.726 and 0.658, respectively.

Multivariate logistic regression analysis for postoperative CHP

Included the variables with differences in univariate analysis into the logistic regression analysis model and performed quantitative assignment: the dependent variable was whether CHP occurred (CHP = 1, non-CHP = 0), the independent variable was hypertension (yes = 1, no = 0), M-PSCAs (yes = 1, no = 0), bypass method (E-S = 1, S-S = 0), CMD ≥ 0.217 (yes = 1, no = 0), and LΔCBF ≥ 1.985 (yes = 1, no = 0). The logistic regression analysis elucidated that hypertension was unrelated to the onset of postoperative CHP. M-PSCAs (OR, 4.221 [95% CI, 1.260–14.137]; P = 0.020), E-S bypass method (OR, 4.211 [95% CI, 1.311–13.529]; P = 0.016), CMD ≥ 0.217 (OR, 7.994 [95% CI, 2.244–28.483]; P = 0.001), and LΔCBF ≥1.985 (OR, 7.821 [95% CI, 2.109–29.005]; P = 0.002) were risk factors for CHP of patients with MMD underwent STA-MCA bypass, as shown in Table 1.

Relationships between parameters from LSCI and onset or duration time of TNDs

Spearman’s rank correlation coefficient was used to evaluate the association between parameters (LΔCBF and CMD) from LSCI and the onset time of TNDs. LΔCBF uncovered a strong correlation with the onset time of TNDs. The Spearman’s rank correlation coefficient for LΔCBF was −0.9747 (P = 0.0001). The larger the change in LΔCBF, the earlier the TNDs occurred. However, there was no significant correlation between CMD and the onset time of TNDs (P < 0.05). In addition, there was no significant correlation between LSCI parameters and the duration of TNDs in these 9 patients (all P < 0.05), as shown in Figure 4. The detailed data of nine patients who suffered TNDs are described in Supplementary File 1.

Figure 4.

Graphs of Spearman’s rank correlations between parameters from LSCI and onset or duration time of TNDs. LΔCBF showed a strong correlation with the onset time of TNDs (R = −0.9747, P = 0.0001), but no correlation with the duration of TNDs (P = 0.2249). CMD did not correlate with the onset time or duration of TNDs, P = 0.2366 and 0.3184, respectively.

Cerebral cortical perfusion of different bypass methods on LSCI and SPECT

With the advent of the novel side-to-side (S-S) bypass method, the authors are interested in the effects of the novel bypass method on cerebral hemodynamic change after anastomosis. Our study compared 45 patients using the end-to-side (E-S) bypass method and 85 using the side-to-side [S-S] bypass method. Data analysis indicated that LΔCBF was much higher in the E-S group than the S-S group: median 2.140 (IQR 1.865–2.415) and median 1.870 (IQR 1.800–1.990), respectively (P = 0.006), other hemodynamic parameters of LSCI (CMD and bCBF) were not significantly different between the E-S and S-S group. Interestingly, no significant difference was observed in SΔrCBF between the E-S group and S-S group: median 1.270 (IQR 1.220–1.530) and median 1.300 (IQR 1.260–1.405), respectively (P = 0.818), as summarized in Table 2.

Table 2.

Comparison of hemodynamic data of different anastomotic techniques.

	E-S (n = 45)	S-S (n = 85)	P Value
CMD	0.220 (0.194–0.250)	0.210 (0.193–0.253)	0.870
bCBF	208.51 (178.67–227.74)	210.17 (167.06–230.58)	0.732
LΔCBF	2.140 (1.865–2.415)	1.870 (1.800–1.990)	0.006
SΔrCBF	1.270 (1.220–1.530)	1.300 (1.260–1.405)	0.818

P < 0.050 were considered significant.

Values are shown as median (interquartile ranges) unless indicated otherwise.

Representative case

A 44-year-old man experienced a recurrent transient ischemic attack of right-sided limb weakness for 2 months. DSA confirmed MMD (Figure 5(a)), and the preoperative SPECT depicted misery perfusion on both hemispheres, heavier on the left side. (Figure 5(d), upper panel). The novel S-S bypass method was performed, and the STA parietal branch was selected as the donor artery. Intraoperative FLOW 800 ICG-VA confirmed the patency of the anastomosis (Figure 5(b)). Intraoperative LSCI showed postanastomotic blood flow changes (LΔCBF) was 2.31 and microvascular density (CMD) was 0.241 (Figure 5(c)). Although postoperative blood pressure was maintained within the regular baseline range by continuous infusion of the antihypertensive agent, the patient still had a seizure postoperatively. We continued mild sedation until the patient’s seizure was under control at POD 6. Postoperative SPECT performed on POD 4 showed that the rCBF in the operated MCA territory was 154% of the preoperative value (Figure 5(d), lower panel). The patient was discharged at POD 9 without any residual symptoms and had recovered from his preoperative symptoms with an mRS score of 0 at the 3-month follow-up. Follow-up DSA demonstrated a good angiographic outcome (Matsushima grade A) (Figure 5(e)).

Figure 5.

Representative case. (a) Preoperative DSA showed terminal occlusion of the left internal carotid artery with abnormal smoke-like vessels. (b) Intraoperative FLOW 800 ICG-VA showed the patency of the anastomosis (yellow circle), preservation of the distal outflow of the donor STA. (c) LSCI showed the CBF of the anastomosis site had significantly improved and the postanastomic/preanastomic CBF value was 2.06 and microvascular density (CMD) was 0.25 (Predefined white circles indicate the ROIs that were placed to calculate CBF and CMD). (d) Preoperative SPECT indicated misery perfusion (upper panel). Local rCBF values were measured by manually defined ROI with a diameter of 1 cm, such as the anastomotic territory (white circles). Postoperative SPECT showed the rCBF of the anastomosis site had significantly improved (lower panel) and (e) The parietal STA branch was selected as the donor artery (upper panel; white arrow). Three-month follow-up DSA showed good angiographic outcome (lower panel).

Discussion

The study indicated that the parameters of LSCI (i.e., LΔCBF and CMD), M-PSCAs and E-S bypass method were correlated with postoperative CHP. Additionally, LΔCBF was found to be associated with the onset time of TNDs. Moreover, the LSCI demonstrated that the immediate CBF surge in the cerebral cortex after the E-S bypass method was significantly greater than that of the S-S bypass method.

Our study affirms that LSCI enables continuous and non-invasive imaging of CBF in patients who have undergone neurovascular surgery, offering high temporal resolution and sensitivity to even minor flow changes. In our study, standardized patient management and system configuration permitted robust assessment of CBF. With LSCI, surgeons can calculate direct hemodynamic parameters for an arbitrarily set ROI in real-time.

According to previous reports, various factors (such as hemodynamic sources of the PSCAs from MCA, preoperatively increased oxygen extraction fraction [OEF], prolonged recovery of increased CBV, RNF213 gene polymorphism, adult patient, preoperative CBV increase, microvascular transit time and type of onset, etc.) have been shown to be associated with CHP.^{8
–10,21,30} Our previous study emphasized that direct anastomoses of PSCAs with anterograde hemodynamic sources from the MCA was a risk factor of postoperative CHP, and the data analysis result of the present study was consistent with this view.³⁰ Currently, the reasons for the occurrence of CHP are still controversial. However, according to these studies, the excessively increased focal CBF was the generally accepted factor leading to CHP.

In the present study, the intraoperative LSCI analysis outlined that the change rate of CBF and cortical microvascular density correlated with CHP. LΔCBF had the highest correlation coefficient among the parameters calculated by LSCI; however, CMD should also be given attention due to its high sensitivity. Significantly, LΔCBF increased after anastomosis in almost all operated hemispheres, indicating enhanced cerebral cortical perfusion and the patency of vascular anastomosis following bypass procedures. A previous report indicated that 31% of CHP and 16.7% of TNDs occurred during bypass surgery.⁹ The incidence rates of CHP on SPECT (24.6%) and symptomatic hyperperfusion (6.9%) in the present study were significantly lower compared to the previous reports. The authors suggest this may be attributed to the novel side-to-side bypass method. The S-S bypass method may achieve self-regulation of incoming blood flow by shunting extra blood flow into the distal STA to reduce the incidence of CHP.²⁷ Within the current study, cortical microvascular density (CMD) was significantly higher in patients with CHP than those without CHP. We speculated that it may be related to the disease development of MMD. Typically, cerebral perfusion of MMD is insufficient due to the blood supply from stenotic MCA or extraintracranial vessels, and the brain uses several compensating mechanisms to adapt to chronic ischemia. Long-lasting cerebral ischemia may induce maximal dilatation of the arterioles and persistently promoted arteriole density, leading to postoperative hyperperfusion in response to a rapid recovery of cerebral perfusion pressure after bypass surgery. Furthermore, correlation analysis indicated that the larger the LΔCBF, the earlier the postoperative CHP occurred, suggesting that LSCI was significantly superior to SPECT in early screening for CHP.

Our data analysis demonstrated that CHP could be observed immediately during surgery by LSCI, and earlier CHP was highly likely to occur postoperatively in patients with LΔCBF ≥ 1.985, or CMD ≥ 0.217. For such patients, at least 24 hours of sedation in addition to strict control of blood pressure and maintained body fluid balance in the NICU are needed. In the present study, hypertension was not a risk factor for predicting CHP, and the authors suggested that this may be related to the postoperative blood pressure intensive management of our center. In all patients, SPECT was performed to assess cerebral hemodynamics on POD 3, and the target value of blood pressure was reset accordingly. We expect to reduce perioperative complications through these managements and intend to determine whether treatment outcomes are improved by screening patients at increased risk for postoperative CHP with LSCI and strengthening perioperative management in the future.

Two patients who developed postoperative cerebral hemorrhage and four patients with cerebral infarction were excluded from this study. The postoperative hemodynamics in these 6 patients remained unclear because they were not evaluated by SPECT. However, the results of LSCI indicated that local hemodynamic instability existed in these patients. The parameters (LΔCBF and CMD) of the two patients (both performed the E-S bypass method) who suffered cerebral hemorrhage greatly exceeded the optimal cutoff values for predicting CHP. The LΔCBF in three of the four patients with postoperative infractions were below the optimal cutoff values for predicting CHP, and the LΔCBF of another patient who performed the S-S bypass method was lower than before bypass surgery. We speculated the compensating vessels, such as the development of leptomeningeal and extraintracranial anastomoses, may be destroyed due to surgical invasion, and the donor STA provided less perfusion than damaged compensating vessels provided, which led to ischemic stroke. In addition, the authors conjectured the distal STA steal phenomenon may occur in this patient,²⁷ but SPECT performed 3 months postoperatively suggested that cortical perfusion at the anastomotic site was still slightly increased compared with preoperative. Although our current study demonstrated that the novel S-S STA-MCA bypass method might indeed alleviate relative complications of symptomatic CHP, the hyperperfusion or hypoperfusion may still occur postoperatively due to the complexity of moyamoya disease hemodynamics, so the criteria of patient and donor recipient artery selection should be strict to avoid inappropriate anastomosis which can cause infarction or hemorrhage.

The conventional E-S STA-MCA bypass method is popular, while it does not take into account the actual need for intracranial perfusion but instead perfuses all the blood flow of the STA into the recipient blood vessel.⁶ The current research using LSCI showed the immediately increased cerebral blood flow after the E-S bypass was significantly greater than the S-S bypass. However, postoperative SPECT data analysis pinpointed that there was not much difference in the changes of cortical cerebral perfusion between the two bypass methods, which was consistent with our previous findings. The difference in the increase of CBF between the two monitoring techniques may be due to the different evaluation periods, and the perfusion provided by the donor artery was confined around the anastomosis site in the early period. However, as the hemodynamics stabilized and the blood flow redistributed to the ischemic brain tissue, the CBF around the anastomosis site measured postoperatively by SPECT will be lower than that measured intraoperatively by LSCI. Meanwhile, the augmented CBF of the S-S bypass method is lower than the E-S bypass method in the acute phase due to the preserved distal outflow of the donor STA. The joint analysis of LSCI and SPECT indicated that the novel S-S bypass method may be safer perioperatively than the conventional E-S bypass method.

Limitations

One significant limitation of LSCI is the shallow penetration depth of the images, LSCI can only assess blood flow in superficial vascular territories exposed intraoperatively, thereby, monitoring methods such as SPECT are still required to detect delayed postoperative CHP. Second, LSCI cannot indicate the direction of blood flow and vessel stenosis. For the flow visualization within the vasculature, ICG angiography should remain the method of choice. Third, this single-center retrospective study included a limited number of patients, and the selection bias of the sample could be an issue.

Conclusions

Our study demonstrated that LSCI, as a non-invasive blood flow monitoring device, can provide intraoperative visualization and quantification of cortical blood flow for neurosurgeons performing extracranial-intracranial bypass surgery, and the two indicators obtained by LSCI analysis are high-risk factors for postoperative CHP in MMD patients, more attention should be paid to the postoperative management of such patients.

Supplemental Material

sj-pdf-1-jcb-10.1177_0271678X241226483 - Supplemental material for Intraoperative evaluation of local cerebral hemodynamic change by laser speckle contrast imaging for predicting postoperative cerebral hyperperfusion during STA-MCA bypass in adult patients with moyamoya disease

Supplemental material, sj-pdf-1-jcb-10.1177_0271678X241226483 for Intraoperative evaluation of local cerebral hemodynamic change by laser speckle contrast imaging for predicting postoperative cerebral hyperperfusion during STA-MCA bypass in adult patients with moyamoya disease by Tianshu Tao, Wenting Zhu, Jin Yu, Xiang Li, Wei Wei, Miao Hu, Mingrui Luo, Guiping Wan, Pengcheng Li, Jincao Chen and Jianjian Zhang in Journal of Cerebral Blood Flow & Metabolism

Supplemental Material

sj-xlsx-2-jcb-10.1177_0271678X241226483 - Supplemental material for Intraoperative evaluation of local cerebral hemodynamic change by laser speckle contrast imaging for predicting postoperative cerebral hyperperfusion during STA-MCA bypass in adult patients with moyamoya disease

Supplemental material, sj-xlsx-2-jcb-10.1177_0271678X241226483 for Intraoperative evaluation of local cerebral hemodynamic change by laser speckle contrast imaging for predicting postoperative cerebral hyperperfusion during STA-MCA bypass in adult patients with moyamoya disease by Tianshu Tao, Wenting Zhu, Jin Yu, Xiang Li, Wei Wei, Miao Hu, Mingrui Luo, Guiping Wan, Pengcheng Li, Jincao Chen and Jianjian Zhang in Journal of Cerebral Blood Flow & Metabolism

Footnotes

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Acknowledgements

The authors wish to thank Dr Changyin Wang for his help in conducting the SPECT experiments and professor Lixin Dong for her guidance on statistical methods

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Authors’ contributions

Conception and design: Jianjian Zhang, Jincao Chen, Pengcheng Li. Acquisition of data: Tianshu Tao, Mingrui Luo, Jin Yu, Miao Hu, Guiping Wan. Analysis and interpretation of data: Tianshu Tao, Wenting Zhu. Statistical analysis: Tianshu Tao, Wenting Zhu, Jin Yu. Drafting the article: Tianshu Tao. Critically revising the article: Jianjian Zhang, Xiang Li, Wei Wei. Reviewed submitted version of manuscript: Jianjian Zhang, Jincao Chen, Pengcheng Li. Approved the final version of the manuscript on behalf of all authors: Jianjian Zhang.

ORCID iD

Tianshu Tao

Supplementary material

Supplemental material for this article is available online.

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Supplementary Material

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