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Evaluation of Patency After Vascular Anastomosis Using Quantitative Evaluation of Visualization Time in Indocyanine Green Video Angiography
Original Article
Evaluation of Patency After Vascular Anastomosis Using Quantitative Evaluation of Visualization Time in Indocyanine Green Video Angiography Shunsuke Nakagawa, Yasuo Murai, Fumihiro Matano, Eitaro Ishisaka, Akio Morita
BACKGROUND: In vascular reconstructive surgery, intraoperative confirmation of patency is performed by angiography, Doppler, or indocyanine videoangiography, but it is sometimes insufficient.
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OBJECTIVE: Using the FLOW 800 system (Carl Zeiss, Oberkochen, Germany), we confirmed patency in a quantitative relative evaluation of the timing of the luminance change of the regions of interest (ROIs) on the donor and recipient.
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METHODS: Thirty-seven patients (58 anastomoses) were divided into 2 groups: those with arteriosclerotic ischemic disease (CI group; n [ 23) and those with cerebral aneurysm (AN group; n [ 14). Four ROIs were set: the donor, proximal, and distal sides of the recipient middle cerebral artery (MCA) and cortical MCA (control MCA). The half-life for fluorescence intensity was calculated by using the FLOW 800 system. A delay map analysis was also performed.
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RESULTS: In the CI group, there were statistically significant differences (P < 0.05) between the donor vessel and control MCA, proximal MCA and MCA control, and distal MCA and control MCA. The investigation with the delay map showed red tones in 20/22 patients in the CI group and in 2/17 patients in the AN group.
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CONCLUSIONS: In the CI group, the transit time of the donor vessel was shown relatively early as red T. When
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Key words Cerebral blood flow - Fluorescent - Indocyanine green - Patency - Vascular reconstructive surgery -
Abbreviations and Acronyms COSS: Carotid Occlusion Surgery Study CT: Computed tomography DWI: Diffusion-weighted imaging ICA: Internal carotid artery ICG: Indocyanine green MCA: Middle cerebral artery MRA: Magnetic resonance angiography MRI: Magnetic resonance imaging
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good patency has been achieved, the FLOW 800 system can be used to confirm patency more reliably, especially in ischemic regions. The unique point of this research is that the patency of anastomotic vessels was evaluated as a quantitative value of its rendering time rather than as a change in fluorescence intensity.
INTRODUCTION
W
hen performing vascular reconstructive surgery, careful and detailed confirmation of the anastomotic vessel intraoperatively is one of the important points to prevent ischemic complications. In COSS (Carotid Occlusion Surgery Study),1 this confirmation was achieved using Doppler imaging or angiography. However, in COSS, ischemic complications occurred within the first 2 postoperative days. Based on these results, it is necessary to consider the insufficiency of the conventional confirmation method of patency. The most reliable method for confirming patency of the anastomotic region intraoperatively is cerebral angiography.2-4 In recent years, many studies have reported the use of indocyanine green (ICG) videoangiography (VAG) as a simpler method.5-13 However, Doppler imaging and ICG-VAG can be used only to confirm that blood is flowing in the donor vessel. For example, if blood flow in the anastomotic vessel is present only in the distal side or in the proximal side, the results of ICG-VAG or Doppler imaging of the donor vessel would mistakenly indicate good
RA: Radial artery ROI: Region of interest STA: Superficial temporal artery VAG: Videoangiography Department of Neurological Surgery, Nippon Medical School, Tokyo, Japan To whom correspondence should be addressed: Yasuo Murai, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2017). https://doi.org/10.1016/j.wneu.2017.11.072 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2017 Elsevier Inc. All rights reserved.
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patency. In addition, it is difficult to evaluate slow flow of the donor vessel caused by dissection, vasospasms, or kinking using ICG-VAG or Doppler. Thus, confirmation of the patency using ICG or Doppler is insufficient. In this study, we focused on differences in the transit time of ICG-VAG between the cortical middle cerebral artery (MCA) (control MCA), which had no relationship to the anastomosis, and the donor vessel (mainly, the superficial temporal artery [STA]), and the recipient proximal and distal MCA. To achieve a more reliable evaluation method for the patency of the anastomotic vessel, we investigated the feasibility of adding quantitative data regarding the direction and timing of blood flow from the donor vessel according to differences in transit times, not fluorescence intensity. METHODS Patient Population Patients who provided informed consent participated in the study. Between January 2012 and December 2016, 63 vascular reconstructive surgeries were performed at our institution. From these cases, 37 patients (38 surgeries [1 patient with a large MCA aneurysm was operated on twice] and 56 anastomoses) who underwent ICG-VAG using the FLOW 800 system (Carl Zeiss, Oberkochen, Germany) were included in this study (Table 1). Twenty-three cases of atherosclerotic internal carotid artery (ICA) to MCA occlusive disease and 14 cases of ICA to MCA aneurysm were included. Excluded cases were patients with moyamoya disease, revascularization of the posterior cranial fossa such as occipital artery to posterior inferior cerebellar artery bypass, subarachnoid hemorrhage, an iodine allergy, and ICG-VAG failure caused by microscope malfunction. The reason for malfunction was considered to be repeated shooting in a short period and the influence of electromagnetic waves of peripheral devices, but the cause was unknown. No patient had signs of an allergic reaction to the contrast medium. In 1 patient, appropriate ICG contrast images could not be obtained, although imaging was performed. The study patients included 17 men and 20 women aged 28e87 years (mean age, 61.58 years). In all aneurysm cases, 2 surgeons with experience performing more than 500 aneurysm surgeries and 1 intravascular surgeon examined the treatment strategy. This study also included cases in which vascular reconstructive surgery was necessary intraoperatively. In radial artery (RA) graft surgery, external carotid artery to RA to MCA bypass was performed in all patients. The RA was taken from the same side as the surgery. Patients were divided into 2 groups: 1) Arteriosclerotic cerebral ischemic group (CI group): patients who underwent STA-MCA anastomosis in the arteriosclerotic cerebral ischemic region (n ¼ 22 [13 men]; median age, 61.88 years; age range, 40e81 years). 2) Cerebral aneurysm group (AN group): patients who underwent RA graft bypass or STA-MCA anastomosis for a cerebral aneurysm (n ¼ 15 [4 men]; median age, 60.43 years; age range, 28e87 years). In the CI group, 9 patients underwent double bypass. In the AN group, 10 patients underwent RA graft bypass and STA-MCA
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anastomosis. Thirty-one anastomoses were performed in the CI group, and 25 anastomoses were performed in the AN group. In patients with STA-MCA anastomosis for arteriosclerotic ischemic lesions, the requirements of eligibility for bypass surgery were symptomatic lesions with modified Rankin Scale scores of 0e2, quantitative cerebral hemodynamic measurements using [123I]-iodoamphetamine single-photon emission computed tomography (CT) indicating a resting MCA blood flow volume, and impaired cerebral vascular reactivity.1,14 Reconstructive bypass surgeries were performed on symptomatic complex ICA and MCA aneurysms for which direct clipping or endovascular coiling was difficult. All patients underwent ICG-VAG after anastomosis. After completing anastomosis, analysis of the time from intravenous ICG was conducted using the FLOW 800 system. Some cases are poorly contrasted with ICG, or some cases may not be contrasted with ICG because of a thick aneurysm wall. In cases of cerebral aneurysm, we check the ICG-VAG findings before clipping is performed to see how the aneurysm will be contrasted with ICG. All patients underwent diffusion-weighted imaging (DWI) and magnetic resonance angiography (MRA) within the first 3 postoperative days to confirm ischemic findings and anastomotic vessel patency. FLOW 800 Analysis We used a Pentero microscope (Carl Zeiss) for FLOW 800 analysis. To detect luminance on the ICG-VAG images, fluorescence in the blood excited by near-infrared ray light in the microscope was detected and recorded as black and white moving images. During ICG-VAG, lights within the operating room were turned off, and the same visual field was imaged without changing the microscopic magnification or distance of the focus point. The imaging range was set as the entire range of the dura opening so that a large area throughout the frontal and temporal lobes could be observed. With the FLOW 800 system, square regions of interest (ROIs) of a prescribed size are set within the imaging range (Figures 1, 2B, and 3B), and changes in luminance over time within these ROIs are automatically recorded as semiquantitative values and shown in a graph.15 These data are also analyzed with an automatic algorithm.16 This strategy means that the delay time (T1/2max), which is defined as the halflife for fluorescence brightness to progress from 0 to the maximum fluorescence brightness in the ROI, is automatically calculated. In the present study, we compared the T1/2max time in ROIs set in the vessels of interest and investigated correlations between the T1/2max and delay map using the FLOW 800 system. ROIs were arbitrarily set postoperatively. The schematic setting of the ROI over the donor and recipient is shown in Figure 1. They were set in the STA donor vessel, proximal to the MCA recipient vessel anastomotic site (proximal side near the sylvian fissure) and distal to the MCA recipient vessel anastomotic site and the control MCA, which had no relationship to the anastomosed MCA (Figures 1, 2B, and 3B). In addition, these data are shown in a graph (Figures 2C and 3C). In regions with decreased cerebral blood flow in the CI group, the transit time (delay time [T1/2max]) was longer than in normal vessels, just as the mean transit time is prolonged on perfusion CT and perfusion magnetic resonance imaging (MRI) scans. Because
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VALUE OF RED TONES IN VASCULAR RECONSTRUCTION SURGERY
Table 1. List of Patients in this Study Case 1
Age (years)/Sex
Diagnosis
Group
Bypass Procedure
Occlusion Time (minutes)
60s/M
ICS
CI
STA-MCA single
18
2
60s/F
ICAN
AN
RAG &STA-MCA
17/25
3
50s/F
ICAN
AN
RAG &STA-MCA
19/28
4
70s/F
ICAN
AN
RAG &STA-MCA
19/37
5
60s/M
MCO
CI
STA-MCA double
20/18
6
60s/M
ICO
CI
STA-MCA double
16/19
7
70s/M
MCS
CI
STA-MCA single
20
8
70s/M
MCO
CI
STA-MCA double
20/18
9
50s/F
ICS
CI
STA-MCA single
18
10
60s/F
ICO
CI
STA-MCA single
18
11
70s/F
MCAN
AN
Clipping STA-MCA
27
12
70s/M
ICO
CI
STA-MCA double
19/18
13
60s/F
ICAN
AN
RAG &STA-MCA
21/26
14
60s/F
ICS
CI
STA-MCA double
21/18
15
40s/F
ICS
CI
STA-MCA double
20/25
16
60s/F
ICAN
AN
RAG &STA-MCA
17/46
17
40s/F
ICS
CI
STA-MCA double
24/2
18
80s/F
ICAN
AN
RAG &STA-MCA
18/35
19
50s/F
MCS
CI
STA-MCA single
27
20
60s/F
ICAN
AN
RAG &STA-MCA
19/18
21
40s/F
MCS
CI
STA-MCA single and clip
25
22
50s/M
MCS
CI
STA-MCA single
21
23
40s/M
MCO
CI
STA-MCA double
21/17
24
60s/F
MCS
CI
STA-MCA single
28
25
60s/M
MCAN
AN
STA-MCA double
22/18
26
70s/F
ICS
CI
STA-MCA single
25
27
50s/M
MCAN
AN
STA-MCA double
21/25
28
60s/M
ICO
CI
STA-MCA single
25
29
40s/M
ICO
CI
STA-MCA single
24
30
70s/F
ICO
CI
STA-MCA single
39
31
80s/M
ICO
CI
STA-MCA single
30
32
70s/M
ICO
CI
STA-MCA single
27
33
50s/F
ICAN
AN
RAG &STA-MCA
17/27
34
40s/F
ICAN
AN
RAG &STA-MCA
21/31
35
20s/M
ICAN
AN
RAG &STA-MCA
18/26
36(¼27)
50s/M
MCAN
AN
Trapping & RAG
32
37
50s/M
ICO
CI
STA-MCA single
21
38
70s/M
ICO
CI
STA-MCA single
23
M, male; ICS, internal carotid artery stenosis; CI, atherosclerotic cerebral ischemic; STA, superficial temporal artery; MCA, middle cerebral artery; F, female; ICAN, internal carotid artery aneurysm; AN, cerebral aneurysm; RAG, radial artery graft bypass; MCO, middle cerebral artery occlusion; ICO, internal carotid artery occlusion; MCS, middle cerebral artery stenosis; MCAN, middle cerebral artery aneurysm.
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(Figures 2D and 3D), vessels with short transit times (the part the anastomosed STA undergoes transit at a normal blood flow where ICG flows in earlier) are shown as red tones, whereas velocity, the transit time is relatively short. Thus, we hypothesized vessels with long transit times are shown as blue tones. that if the anastomosis had been appropriately performed and This delay map image was automatically detected, and the color patency had been maintained, the proximal and distal sides of the of the anastomotic area was extracted as a result of the recipient and the donor vessels would be filled in red color code. The color of the anastomosis is the part of tones, and the transit time of the cortical vessel with the pink square in Figure 2, upper right, Figure 4, and poor cerebral blood flow would be delayed. We also Video 1, which is the anastomotic portion. Figure 5A investigated whether the direction of blood flow could and 5B and Video 1 present a diagram showing the be confirmed by observing the transit time of the anastomotic area. vessels shown. We examined whether these transit Video available at WORLDNEUROSURGERY.org times were significantly shorter than those of the vessels with poor blood flow that had not undergone Statistical Analysis anastomosis. Data are shown as a mean standard error. Statistical analysis was performed using JMP 11.0.0 statistical software (SAS Institute, Cary, North Carolina, USA). We used the paired Student t test with Delay Map Image Bonferroni correction to evaluate the tests for each ROI in all Cerebral blood flow evaluation software was installed for the combinations between the AN group and CI group. A P value Pentero microscope (Carl Zeiss) for FLOW 800 analysis. By using <0.05 was considered statistically significant. these data, the average intensity change can be evaluated by The color tone by color code evaluation from the donor vessel to 2 methods of relative rendering time (delay map) and relative the recipient vessel near the anastomotic site was evaluated, and luminance change (intensity map). In this study, we use the the result was compared between the CI and AN groups. The delayed map. In the delay map of the FLOW 800 system,15 the significance level was set at P < 0.05 in the c2 test. That is, the entire range of ICG-VAG is set as the ROI and the average infrequency of those showing red color tones was compared betensity change over time is automatically measured. In this mode, tween the AN and CI groups. In addition, we compared the color the whole field of view is captured as the ROI, and the time until frequencies of red to orange and other color frequencies between the average luminance becomes half of the maximum, which is the AN and CI groups. equally divided into the earliest part in the order of red, yellow, green, and blue. On the delay map using the FLOW 800 system RESULTS
Figure 1. The locations of the regions of interest. White square regions of interest are shown on the cortical middle cerebral artery. Yellow square regions of interest are shown on the recipient proximal middle cerebral artery. Green square regions of interest are shown on the recipient distal middle cerebral artery. Blue square regions of interest are shown on the recipient donor superficial temporal artery. Pink square regions of interest are indicated on the color code area (Figure 5). The color code (Figure 5) of all cases is extracted from the pink square range. *Middle cerebral artery. **The recipient donor superficial temporal artery.
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In the CI group (Table 2), the results of T1/2max were as follows. There were statistically significant differences between the T1/ 2max of the control MCA and T1/2max of the recipient proximal MCA (P <0.001), recipient distal MCA, and donor STA (P < 0.001) (Table 2). There were statistically significant differences between the T1/2max of the donor vessel and T1/2max of the recipient proximal MCA (P ¼ 0.0003), and the T1/2max of the recipient distal MCA and donor (P ¼ 0.0023) (Table 2). There were no statistically significant differences between the T1/2max of the recipient distal MCA and T1/2max of the recipient proximal MCA (P ¼ 0.794) (Table 2). In all patients in the CI group, the T1/2max of the donor vessel was shorter than the T1/2max of the control MCA. In the AN group (Table 3), the results of T1/2max were as follows. There were statistically significant differences between the T1/2max (recipient MCA proximal) and T1/2max (donor STA) (P ¼ 0.0054), and the T1/2max (recipient MCA distal) and T1/2max (MCA control) (P ¼ 0.0047), respectively (Table 3). No statistically significant differences were observed in other combinations. In a comparison between the donor STA and control MCA, the P value was low in the CI group (P < 0.001) compared with that in the AN group (P ¼ 0.0608). This finding suggested that the donor STA was more clearly visualized earlier in the CI group. Delay Map Using the FLOW 800 System, Patency, and MRI Findings The color tone of the anastomotic area (pink square in Figure 1 and upper right in Figure 2) of all cases are shown in Figure 5. Regarding the evaluation of color codes, the frequency of red
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Figure 2. Intraoperative blood flow analysis imaging using the FLOW 800 system for arteriosclerotic cerebral internal carotid artery occlusion. (A) (Upper left) Intraoperative image of the surgical field after the superficial temporal artery (STA)-middle cerebral artery (MCA) single anastomosis for symptomatic atherosclerotic internal carotid artery occlusion. (B) (Lower left) Settings for the regions of interest were adjusted manually. (1): Red square: donor vessel (STA). (2): Green square: distal donor vessel (STA). (3) Blue square: recipient proximal MCA. (4) Pink square: recipient distal MCA. (5) Yellow square: cortical control MCA. (C) (Upper right) Delay map after STA-MCA anastomosis was performed in the arteriosclerotic
tones was statistically significant in the CI group (P ¼ 0.0155). In addition, the frequencies of red to orange were statistically significant in the CI group (P ¼ 0.0250). MRI, including MRA and DWI performed within 3 days postoperatively, did not show symptomatic ischemic complications in any patients. However, in 11 of 38 surgeries and 56 anastomoses, DWI scans indicated cortical ischemic lesions with a diameter of 3 mm or less as a result of minute coagulation of the bifurcation during recipient vessel anastomosis. MRA confirmed anastomotic vessel patency in all patients. DISCUSSION The results of this study suggest that by adding a quantitative assessment based on the rendering time (T1/2max) of the ROI on the target vessel using ICG-VAG, blood flow in the donor blood
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cerebral ischemic region. The donor STA and MCA around the anastomosis are shown in red (Red T). Small pink square on the distal end of STA indicate color code (Figure 5). The color code (Figure 5) of this case was extracted from the pink square range. (D) (Lower right) The calculations of indocyanine green fluorescence luminance. The point at which half of the maximum fluorescence luminance (T1/2max) is reached was calculated. Red graph: donor vessel (STA). Blue graph: recipient proximal MCA. Pink graph: recipient distal MCA. Yellow graph: cortical control MCA. The arteries from largest to smallest: STA>proximal MCA>proximal MCA>cortical control MCA of the measured value of T1/2max.
vessel and in both directions from the anastomotic part to the recipient can be quantitatively drawn. In addition, by reflecting prolongation of the transit time in ischemic lesions, the detection of blood flow failure in the proximal part of the donor vessel may be possible by comparing the difference in the rendering time of another cerebral vascular vessel from the recipient. The delay map of the FLOW 800 system can easily detect these findings by focusing on the imaging timing. The unique point of this study is that the patency of anastomotic vessels using ICG-VAG and the FLOW 800 system was evaluated as a quantitative value of its rendering time rather than as a change in fluorescence intensity. Angiography, Doppler, and ICG-VAG are available as intraoperative patency evaluation methods of vascular reconstructive surgery. However, no previous study has evaluated patency more accurately by simultaneously measuring the blood flow timing in the donor and recipient in both directions, and vessels unrelated
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Figure 3. Intraoperative blood flow analysis in the case of double superficial temporal artery (STA) to middle cerebral artery (MCA) for a large MCA aneurysm using the FLOW 800 system. (A) (Upper left) Intraoperative image of the surgical field after the STA-MCA double anastomosis for a large MCA aneurysm. (B) (Lower left) Settings for the regions of interest were adjusted manually. (1) Red square: donor vessel (parietal branch of STA)e1. (2) Green square: recipient distal MCAe1. (3) Blue square: recipient proximal MCAe1. (4) Pink square: recipient proximal MCAe2. (5) Yellow square:
recipient distal MCAe2. (6) Sky blue square: donor vessel (frontal branch of STA)e2. (7) Brown square: cortical control MCA. (C) (Upper right) Delay map after STA-MCA double anastomosis. The both branch of the STA and recipient MCA is yellow (yellow T). Small pink square on the distal end of STA indicates color code (Figure 5). The color code (Figure 5) of this case was extracted from the pink square range. (D) (Lower right) Indocyanine green fluorescence luminance. The point at which half the maximum fluorescence luminance is reached was calculated.
to anastomosis. During angiography, in which the contrast medium is injected under pressure, it is impossible to accurately determine the timing of visualization. With Doppler, it is impossible to simultaneously evaluate multiple blood vessels. To assess the patency of intraoperative anastomotic vessels, the following must be observed: Blood flow of the donor STA is flowing forward Blood of the donor vessel flows earlier than the MCA of the brain Blood flows in both directions from the anastomotic part to the recipient vessel These 3 findings are observed over time. We believe that our method can be used to observe all of these features. Figure 4. Extraction of the color code from the delay map image. Extraction of the color of the anastomosis, as in this case in all patients, is summarized in Figure 5.
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If surgeons do not confirm blood flow in both directions of the donor vessel by the delay map and it is stained white with ICGVAG, the ICG-VAG image shows blood vessels with all blood
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Figure 5. List of postoperative magnetic resonance imaging findings and results of the delay map study. The color tone of the anastomotic area (pink square in Figure 1, upper right in Figure 2, and upper right in Figure 3) of all
flow irrespective of timing; thus, it is difficult to determine whether ICG flows in with blood flow from the donor. Especially during bypass procedures for atherosclerotic ischemic lesions (CI
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cases is also shown. (A) List of results for the cerebral infarction group. (Continues)
group), our results showed a significantly short T1/2max in the donor vessels and the recipient vessels in both directions compared with the control MCA unrelated to the anastomosis. In
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Figure 5. (Continued) B) List of results for the cerebral aneurysm group. AN, cerebral aneurysm; CI, cerebral infarction; ICAN, internal carotid artery aneurysm; ICO, internal carotid artery occlusion; ICS, internal carotid artery stenosis; LSA, lenticulostriate artery; MCAN, middle cerebral artery
addition, in all patients in the CI group, the T1/2max of the control MCA was larger than that of the proximal MCA and that of the distal MCA distal, which was reflected in the delay map, with the proximal and distal sides of the donor vessels and the recipient vessels being indicated in red tones (Figure 2D). The FLOW 800 system, which has a delay map system, originally enabled us to obtain the red tone sign easily. This red tone sign on the delay map of ICG-VAG should be able to be used as an easy indicator of good patency during bypass procedure for ischemic atherosclerotic procedures. Without red tones, we can obtain the information about the patency with the quantitative assessment of the FLOW 800 system using the temporary proximal occlusion of the recipient vessel, because it is reliable during vascular reconstructive surgery. Patency-related findings were consistent with the MRI findings obtained within 3 days postoperatively. Therefore, we successfully showed that the evaluation of the direction
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aneurysm; MCO, middle cerebral artery occlusion; MCS, middle cerebral artery stenosis; NP, no particular; PCA, posterior cerebral artery; RAG, radial artery graft bypass; STA, superficial temporal artery; SCI, small ischemic change <3 mm.
and the transit time of blood flow are useful for confirming the patency of the vascular anastomosis. In patients with cerebral aneurysms, the level of transit time differs by case, so further invention is necessary. Short Transit Time Effect Our results were obtained because the T1/2max of the donor vessel was relatively short (i.e., the short transit time effect). Decreased cerebral blood flow on [123I]-iodoamphetamine single-photon emission CT causes prolonged mean transit time4,17-21 on perfusion CT or perfusion MRI scans. Furthermore, when the balloon occlusion test is conducted with ICA occlusion in patients with poor collateral vessels, cortical vein and artery transit times on the side of the occlusion are known to be delayed.22 In patients with cerebral hypoperfusion, postanastomosis blood flow from the STA means that it shows a short transit time compared with the blood flow in
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VALUE OF RED TONES IN VASCULAR RECONSTRUCTION SURGERY
Table 2. Mean and Standard Error of Each Region of Interest (ROI) and Comparative Analysis of Regions of Interest in the Donor Vessel, Proximal Recipient Middle Cerebral Artery (MCA), Distal Recipient MCA, and Cortical Control MCA in the Arteriosclerotic Ischemic Disease Group Atherosclerotic Cerebral Ischemic Group
Mean
Standard Error
P Value 0.0003
Donor
34.298
2.220
MCA recipient proximal
34.61
2.679
MCA recipient distal
34.139
2.311
0.0023
Cortical MCA
36.419
2.308
<0.0001
MCA, middle cerebral artery.
the collateral vessels with decreased cerebral perfusion pressure. This finding of blood flow from the donor vessel showing an earlier filling than that from the cortical vessels is called the short transit time effect. In patients with cerebral hypoperfusion, the short transit time effect can be used to detect blood flow in both directions from the donor vessel at the anastomotic site. Using Doppler or ICG-VAG images monitored only according to fluorescence intensity, detection is impossible if the donor vessel is narrowed by kinking or vasospasm, causing delayed blood flow, or if there is blood flow in 1 direction only in the recipient vessel. However, with our method, we were able to solve these issues. In patients with cerebral aneurysms, there were no cerebral blood flow defects or prolonged transit time. For this reason, similar findings may be obtained by artificially prolonging the transit time by occluding the vessel with a temporary clip at the proximal MCA distal from the anastomotic site. In our case, red tones were confirmed in patients in whom ICG-VAG was performed with proximal occlusion of the recipient vessel. Importance in Confirming Patency In vascular reconstructive surgery, intraoperative confirmation of patency of the anastomosis is important. The COSS1 showed that angiography or Doppler can be used to confirm the patency. With Doppler, it is difficult to assess blood flow velocity4 and place the probe appropriately for monitoring both sides of the recipient vessel to detect the direction of blood flow. Doppler and ICG
imaging are unable to detect situations in which the anastomosis has failed and blood flow is flowing only peripherally or proximally from the anastomotic site. With ICGVAG alone, it is difficult to determine the direction of blood flow when the velocity of blood flow is fast. Thus, the evaluation of anastomotic vessel patency with ICG-VAG alone assesses only whether there is blood flow in the donor vessel. Studies regarding the evaluation of vascular anastomosis based on cerebral cortical luminance analysis using the FLOW 800 system have indicated problems related to quantitative evaluation.23 Therefore, we focused on T1/2max in the artery rather than evaluating the luminance itself. We also investigated whether the evaluation of the direction of blood flow in the recipient vessel could be used to accurately assess the patency of the anastomotic site. In particular, we confirmed that the quantitative analysis of the T1/2max in the donor vessel and the peripheral and proximal parts of the anastomotic site could be used to confirm peripheral and proximal blood flow in the donor anastomotic site. This finding indicates the possibility of achieving a stronger confirmation of the safety and efficacy of anastomosis using a combination of Doppler and ICG-VAG. The evaluation of cerebral cortical blood flow using ICG has several limitations. For instance, cerebral blood flow in deep areas of the cerebral parenchyma where light cannot enter cannot be evaluated. In addition, when cortical ICG-VAG luminance of the cerebral parenchyma is quantitatively evaluated, the
Table 3. Mean and Standard Error for Each Region of Interest (ROI) and Comparative Analysis of Regions of Interest in the Donor Vessel, Proximal Recipient Middle Cerebral Artery (MCA), Distal Recipient MCA, and Cortical Control MCA in the Cerebral Aneurysm Group Cerebral Aneurysm Group
Mean
Standard Error
P Value 0.0054
Donor
33.651
2.8597
MCA recipient proximal
32.636
2.9726
MCA recipient distal
37.376
3.3729
Cortical MCA
37.135
3.0693
0.0047
MCA, middle cerebral artery.
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injection speed, blood pressure, and heart rate variables, which are all difficult to regulate, may affect the results. To remove these difficulties related to quantitative evaluation, we focused on accurate patency evaluation of the anastomotic vessel rather than cerebral blood flow evaluation, and set ROIs only in visible cortical vessels. Studies of the quantitative evaluation method of patency of vascular anastomosis have been reported in the past 2 decades, and in this respect, our study is not new. These methods include investigations of visual light spectroscopy,24 flometry,25 and laser speckle imaging.26 These studies were intended to show the blood flow of donor blood vessels or cerebral blood flow. Therefore, we pointed out the usefulness of ICG-VAG from the viewpoint of prevention of complications of vascular anastomosis and timing of intensity not from the viewpoint of cerebral blood flow. This point differs from the conventional method. Various problems with the quantitative evaluation of luminance using the FLOW 800 system have been pointed out. The quantitative intensity evaluation of ICG is influenced by the plasma protein level.27,28 Therefore, it is affected by cholesterol and the amount of intraoperative infusion. Moreover, the difficulty of comparing the intensity between ROIs has been noted.10 This situation is because high-intensity blood vessels may affect the intensity evaluation of the surrounding tissues such as indirect illumination. It is optically called a point spread function.29,30 It is a function that represents the response to the point light source of the optical system. However, no previous study has served as a clinical example of ICG-VAG. According to Carl Zeiss, its software developers do not use a specific point spread function for corrections in its infrared 800 video. Furthermore, to reduce various influence, we decided to focus on differences in time until blood vessel depiction rather than intensity.
REFERENCES 1. Powers WJ, Clarke WR, Grubb RL Jr, Videen TO, Adams HP Jr, Derdeyn CP, et al. Extracranialintracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia: the Carotid Occlusion Surgery Study randomized trial. JAMA. 2011;306:1983-1992. 2. Bain MD, Moskowitz SI, Rasmussen PA, Hui FK. Targeted extracranial-intracranial bypass with intra-aneurysmal administration of indocyanine green: case report. Neurosurgery. 2010;67:527-531. 3. Gruber A, Dorfer C, Bavinski G, Standhardt H, Ferraz-Leite H, Knosp E. Super-selective indocyanine green angiography for selective revascularization in the management of peripheral cerebral aneurysms. AJNR Am J Neuroradiol. 2012;33: E36-E37. 4. Schichor C, Rachinger W, Morhard D, Zausinger S, Heigl TJ, Resier M, et al. Intraoperative computed tomography angiography with computed tomography perfusion imaging in vascular neurosurgery: feasibility of a new concept. J Neurosurg. 2010;112:722-728.
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Limitations We considered the following to be the limitations of the method of this study. First, because nonanastomotic regions of the recipient vessel must not be dissected, the range for setting ROIs with ICG is limited. While using ICG-VAG and the delay map, we could not change the visual axis, magnification, or focus of the microscope after the target vessel was in the ICG-VAG field. Therefore, it is not possible to change the direction or focus of the microscope to see the aneurysm from other orientations during ICG-VAG. Furthermore, in patients who have undergone vascular reconstructive surgery for cerebral aneurysms, cerebral blood flow is normal before aneurysm parent artery occlusion. Therefore, it is impossible to detect the short transit time effect and red tones. In patients who have undergone aneurysm surgery, the donor vessel being depicted without any delay in another normal cortical MCA is believed to confirm the patency of the anastomosis. In addition, this problem could be solved by ICG-VAG with temporary proximal occlusion of the recipient vessel. In the delay map image, color tone is based on the timing of the intensity visualization and quantitative evaluation, but there is a limit because it becomes the description of the color tone. However, we believe that this finding corresponds to the purpose of this research, which was to compare the fast part and the slow part of the visualization in 1 example shot. CONCLUSIONS In the CI group, the transit time of the donor was shown relatively early (i.e., red tones). Thus, a delay map image of the FLOW 800 system is useful to confirm patency in arteriosclerotic ischemic disease. However, physicians need another method of blood flow assessment such as temporary proximal occlusion in the AN group. When good patency has been achieved, the FLOW 800 system can be used to confirm the patency more reliably.
5. Czabanka M, Pe na-Tapia P, Schubert GA, Woitzik J, Vajkoczy P, Schmiedek P. Characterization of cortical microvascularization in adult moyamoya disease. Stroke. 2008;39:1703-1709. 6. Dashti R, Laasko A, Niemelä M, Porras M, Hernesniemi J. Microscope integrated nearinfrared indocyanine green video angiography during surgery of intracranial aneurysms: the Helsinki experience. Surg Neurol. 2009;71:543-550. 7. Esposito G, Durand A, van Doormaal TP, Regli L. Selective-targeted extra-intracranial bypass surgery in complex middle cerebral artery aneurysms: correctly identifying the recipient artery using indocyanine green video- angiography. Neurosurgery. 2012;71:274-285. 8. Florian F, Niklas T, Gunther F, Walter R, Roland G, Jörg-Christian T, et al. Enhanced analysis of intracerebral arteriovenous malformations by the intraoperative use of analytical indocyanine green video angiography: technical note. Acta Neurochir (Wien). 2011;153:2181-2187. 9. Hecht N, Woitzik J, Konig S, Horn P, Vajkoczy P. Laser speckle imaging allows real-time intraoperative blood flow assessment during
neurosurgical procedures. J Cereb Blood Flow Metab. 2013;33:1000-1007. 10. Kamp MA, Slotty P, Turowski B, Etminan N, Steiger HJ, Hänggi D, et al. Microscope-integrated quantitative analysis of intraoperative indocyanine green fluorescence angiography for- blood flow assessment: first experience in 30 patients. Neurosurgery. 2012;70:65-74. 11. Raabe A, Beck J, Gerlach R, Zimmermann M, Seifert V. Near-infrared indocyanine green video angiography: a new method for intraoperative assessment of vascular flow. Neurosurgery. 2003;52: 132-139. 12. Raabe A, Nakaji P, Beck J, Kim LJ, Hsu FP, Kamerman JD, et al. Prospective evaluation of surgical microscope-integrated intraoperative near-infrared indocyanine green videoangiography during aneurysm surgery. J Neurosurg. 2005;103: 982-989. 13. Woitzik J, Horn P, Vajkoczy P, Schmiedek P. Intraoperative control of extracranial-intracranial bypass patency by near-infrared indocyanine green videoangiography. J Neurosurg. 2005;102: 692-698.
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ORIGINAL ARTICLE SHUNSUKE NAKAGAWA ET AL.
14. Ogasawara K, Ogawa A. JET study (Japanese ECIC Bypass Trial). Nihon Rinsho. 2006;64(suppl 7): 524-527 [in Japanese]. 15. Fukuda K, Kataoka H, Nakajima N, Masuoka J, Satow T, Iihara K. Efficacy of FLOW 800 with indocyanine green videoangiography for the quantitative assessment of flow dynamics in cerebral arteriovenous malformation surgery. World Neurosurg. 2015;83:203-210. 16. Marcel A, Philip S, Bernd T, Nima E, HansJakob S, Daniel H, et al. Microscope-Integrated quantitative analysis of intraoperative indocyanine green fluorescence angiography for blood flow assessment: first experience in 30 patients. Oper Neurosurg. 2012;70:ons65-ons74. 17. Abud DG, Spelle L, Piotin M, Mounayer C, Vanzin JR, Moret J. Venous phase timing during balloon test occlusion as a criterion for permanent internal carotid artery sacrifice. AJNR Am J Neuroradiol. 2005;26:2602-2609. 18. Murayama K, Katada K, Nakane M, Toyama H, Anno H, Hayakawa M, et al. Whole-brain perfusion CT (computed tomography) performed with a prototype 256-detector row CT (computed tomography) system: initial experience. Radiology. 2009;250:202-211. 19. Siebert E, Bohner G, Dewey M, Masuhr F, Hoffmann KT, Mews J, et al. 320-slice CT (computed tomography) neuroimaging: initial clinical experience and image quality evaluation. Br J Radiol. 2009;82:561-570. 20. Singer OC, de Rochemont Rdu M, Foerch C, Stengel A, Lanfermann H, Sitzer M, et al. Relation between relative cerebral blood flow, relative
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VALUE OF RED TONES IN VASCULAR RECONSTRUCTION SURGERY
cerebral blood volume, and mean transit time in patients with acute ischemic stroke determined by perfusion-weighted MRI(magnetic resonance image). J Cereb Blood Flow Metab. 2003;23:605-611. 21. Van Rooij WJ, Sluzewski M, Slob MJ, Rinkel GJ. Predictive value of angiographic testing for tolerance to therapeutic occlusion of the carotid artery. AJNR Am J Neuroradiol. 2005;26:175-178. 22. Kaesemann P, Thomalla G, Cheng B, Treszl A, Fiehler J, Forkert ND. Impact of severe extracranial ICA stenosis on MRI (magnetic resonance image) perfusion and diffusion parameters in acute ischemic stroke. Front Neurol. 2014;5:254. 23. Prinz V, Hecht N, Kato N, Vajkoczy P. FLOW 800 allows visualization of hemodynamic changes after extracranial-to-intracranial bypass surgery but not assessment of quantitative perfusion or flow. Neurosurgery. 2014;10(suppl 2):231-239. 24. Hoshino T, Katayama Y, Sakatani K, Kano T, Murata Y. Intraoperative monitoring of cerebral blood oxygenation and hemodynamics during extracranial-intracranial bypass surgery by a newly developed visible light spectroscopy system. Surg Neurol. 2006;65:569-576. 25. Mucke T, Wolff KD, Wagenpfeil S, Holzle F, Scholz M. Reliability of near-infrared angiography and micro-Doppler sonography for evaluating microvascular anastomoses. Plast Reconstr Surg. 2010;126:1506-1514. 26. Nomura S, Inoue T, Ishihara H, Koizumi H, Suehiro E, Oka F, et al. Reliability of laser speckle flow imaging for intraoperative monitoring of cerebral blood flow during cerebrovascular surgery: comparison with cerebral blood flow
measurement by single photon emission computed tomography. World Neurosurg. 2014;82: e753-e757. 27. Wang Y, Wang C, Ding Y, Li J, Li M, Liang X, et al. Biomimetic HDL nanoparticle mediated tumor targeted delivery of indocyanine green for enhanced photodynamic therapy. Colloids Surf B Biointerfaces. 2016;148:533-540. 28. Halle BM, Poulsen TD, Pedersen HP. Indocyanine green plasma disappearance rate as dynamic liver function test in critically ill patients. Acta Anaesthesiol Scand. 2014;58:1214-1219. 29. Ghosh S, Preza C. Fluorescence microscopy point spread function model accounting for aberrations due to refractive index variability within a specimen. J Biomed Opt. 2015;20:75003. 30. Yoo H, Song I, Gweon DG. Measurement and restoration of the point spread function of fluorescence confocal microscopy. J Microsc. 2006;221: 172-176.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 13 August 2017; accepted 16 November 2017 Citation: World Neurosurg. (2017). https://doi.org/10.1016/j.wneu.2017.11.072 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2017 Elsevier Inc. All rights reserved.
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Evaluation of Patency After Vascular Anastomosis Using Quantitative Evaluation of Visualization Time in Indocyanine Green Video Angiography Shunsuke Nakagawa, Yasuo Murai, Fumihiro Matano, Eitaro Ishisaka, Akio Morita
BACKGROUND: In vascular reconstructive surgery, intraoperative confirmation of patency is performed by angiography, Doppler, or indocyanine videoangiography, but it is sometimes insufficient.
-
OBJECTIVE: Using the FLOW 800 system (Carl Zeiss, Oberkochen, Germany), we confirmed patency in a quantitative relative evaluation of the timing of the luminance change of the regions of interest (ROIs) on the donor and recipient.
-
METHODS: Thirty-seven patients (58 anastomoses) were divided into 2 groups: those with arteriosclerotic ischemic disease (CI group; n [ 23) and those with cerebral aneurysm (AN group; n [ 14). Four ROIs were set: the donor, proximal, and distal sides of the recipient middle cerebral artery (MCA) and cortical MCA (control MCA). The half-life for fluorescence intensity was calculated by using the FLOW 800 system. A delay map analysis was also performed.
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RESULTS: In the CI group, there were statistically significant differences (P < 0.05) between the donor vessel and control MCA, proximal MCA and MCA control, and distal MCA and control MCA. The investigation with the delay map showed red tones in 20/22 patients in the CI group and in 2/17 patients in the AN group.
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CONCLUSIONS: In the CI group, the transit time of the donor vessel was shown relatively early as red T. When
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Key words Cerebral blood flow - Fluorescent - Indocyanine green - Patency - Vascular reconstructive surgery -
Abbreviations and Acronyms COSS: Carotid Occlusion Surgery Study CT: Computed tomography DWI: Diffusion-weighted imaging ICA: Internal carotid artery ICG: Indocyanine green MCA: Middle cerebral artery MRA: Magnetic resonance angiography MRI: Magnetic resonance imaging
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good patency has been achieved, the FLOW 800 system can be used to confirm patency more reliably, especially in ischemic regions. The unique point of this research is that the patency of anastomotic vessels was evaluated as a quantitative value of its rendering time rather than as a change in fluorescence intensity.
INTRODUCTION
W
hen performing vascular reconstructive surgery, careful and detailed confirmation of the anastomotic vessel intraoperatively is one of the important points to prevent ischemic complications. In COSS (Carotid Occlusion Surgery Study),1 this confirmation was achieved using Doppler imaging or angiography. However, in COSS, ischemic complications occurred within the first 2 postoperative days. Based on these results, it is necessary to consider the insufficiency of the conventional confirmation method of patency. The most reliable method for confirming patency of the anastomotic region intraoperatively is cerebral angiography.2-4 In recent years, many studies have reported the use of indocyanine green (ICG) videoangiography (VAG) as a simpler method.5-13 However, Doppler imaging and ICG-VAG can be used only to confirm that blood is flowing in the donor vessel. For example, if blood flow in the anastomotic vessel is present only in the distal side or in the proximal side, the results of ICG-VAG or Doppler imaging of the donor vessel would mistakenly indicate good
RA: Radial artery ROI: Region of interest STA: Superficial temporal artery VAG: Videoangiography Department of Neurological Surgery, Nippon Medical School, Tokyo, Japan To whom correspondence should be addressed: Yasuo Murai, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2017). https://doi.org/10.1016/j.wneu.2017.11.072 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2017 Elsevier Inc. All rights reserved.
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VALUE OF RED TONES IN VASCULAR RECONSTRUCTION SURGERY
patency. In addition, it is difficult to evaluate slow flow of the donor vessel caused by dissection, vasospasms, or kinking using ICG-VAG or Doppler. Thus, confirmation of the patency using ICG or Doppler is insufficient. In this study, we focused on differences in the transit time of ICG-VAG between the cortical middle cerebral artery (MCA) (control MCA), which had no relationship to the anastomosis, and the donor vessel (mainly, the superficial temporal artery [STA]), and the recipient proximal and distal MCA. To achieve a more reliable evaluation method for the patency of the anastomotic vessel, we investigated the feasibility of adding quantitative data regarding the direction and timing of blood flow from the donor vessel according to differences in transit times, not fluorescence intensity. METHODS Patient Population Patients who provided informed consent participated in the study. Between January 2012 and December 2016, 63 vascular reconstructive surgeries were performed at our institution. From these cases, 37 patients (38 surgeries [1 patient with a large MCA aneurysm was operated on twice] and 56 anastomoses) who underwent ICG-VAG using the FLOW 800 system (Carl Zeiss, Oberkochen, Germany) were included in this study (Table 1). Twenty-three cases of atherosclerotic internal carotid artery (ICA) to MCA occlusive disease and 14 cases of ICA to MCA aneurysm were included. Excluded cases were patients with moyamoya disease, revascularization of the posterior cranial fossa such as occipital artery to posterior inferior cerebellar artery bypass, subarachnoid hemorrhage, an iodine allergy, and ICG-VAG failure caused by microscope malfunction. The reason for malfunction was considered to be repeated shooting in a short period and the influence of electromagnetic waves of peripheral devices, but the cause was unknown. No patient had signs of an allergic reaction to the contrast medium. In 1 patient, appropriate ICG contrast images could not be obtained, although imaging was performed. The study patients included 17 men and 20 women aged 28e87 years (mean age, 61.58 years). In all aneurysm cases, 2 surgeons with experience performing more than 500 aneurysm surgeries and 1 intravascular surgeon examined the treatment strategy. This study also included cases in which vascular reconstructive surgery was necessary intraoperatively. In radial artery (RA) graft surgery, external carotid artery to RA to MCA bypass was performed in all patients. The RA was taken from the same side as the surgery. Patients were divided into 2 groups: 1) Arteriosclerotic cerebral ischemic group (CI group): patients who underwent STA-MCA anastomosis in the arteriosclerotic cerebral ischemic region (n ¼ 22 [13 men]; median age, 61.88 years; age range, 40e81 years). 2) Cerebral aneurysm group (AN group): patients who underwent RA graft bypass or STA-MCA anastomosis for a cerebral aneurysm (n ¼ 15 [4 men]; median age, 60.43 years; age range, 28e87 years). In the CI group, 9 patients underwent double bypass. In the AN group, 10 patients underwent RA graft bypass and STA-MCA
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anastomosis. Thirty-one anastomoses were performed in the CI group, and 25 anastomoses were performed in the AN group. In patients with STA-MCA anastomosis for arteriosclerotic ischemic lesions, the requirements of eligibility for bypass surgery were symptomatic lesions with modified Rankin Scale scores of 0e2, quantitative cerebral hemodynamic measurements using [123I]-iodoamphetamine single-photon emission computed tomography (CT) indicating a resting MCA blood flow volume, and impaired cerebral vascular reactivity.1,14 Reconstructive bypass surgeries were performed on symptomatic complex ICA and MCA aneurysms for which direct clipping or endovascular coiling was difficult. All patients underwent ICG-VAG after anastomosis. After completing anastomosis, analysis of the time from intravenous ICG was conducted using the FLOW 800 system. Some cases are poorly contrasted with ICG, or some cases may not be contrasted with ICG because of a thick aneurysm wall. In cases of cerebral aneurysm, we check the ICG-VAG findings before clipping is performed to see how the aneurysm will be contrasted with ICG. All patients underwent diffusion-weighted imaging (DWI) and magnetic resonance angiography (MRA) within the first 3 postoperative days to confirm ischemic findings and anastomotic vessel patency. FLOW 800 Analysis We used a Pentero microscope (Carl Zeiss) for FLOW 800 analysis. To detect luminance on the ICG-VAG images, fluorescence in the blood excited by near-infrared ray light in the microscope was detected and recorded as black and white moving images. During ICG-VAG, lights within the operating room were turned off, and the same visual field was imaged without changing the microscopic magnification or distance of the focus point. The imaging range was set as the entire range of the dura opening so that a large area throughout the frontal and temporal lobes could be observed. With the FLOW 800 system, square regions of interest (ROIs) of a prescribed size are set within the imaging range (Figures 1, 2B, and 3B), and changes in luminance over time within these ROIs are automatically recorded as semiquantitative values and shown in a graph.15 These data are also analyzed with an automatic algorithm.16 This strategy means that the delay time (T1/2max), which is defined as the halflife for fluorescence brightness to progress from 0 to the maximum fluorescence brightness in the ROI, is automatically calculated. In the present study, we compared the T1/2max time in ROIs set in the vessels of interest and investigated correlations between the T1/2max and delay map using the FLOW 800 system. ROIs were arbitrarily set postoperatively. The schematic setting of the ROI over the donor and recipient is shown in Figure 1. They were set in the STA donor vessel, proximal to the MCA recipient vessel anastomotic site (proximal side near the sylvian fissure) and distal to the MCA recipient vessel anastomotic site and the control MCA, which had no relationship to the anastomosed MCA (Figures 1, 2B, and 3B). In addition, these data are shown in a graph (Figures 2C and 3C). In regions with decreased cerebral blood flow in the CI group, the transit time (delay time [T1/2max]) was longer than in normal vessels, just as the mean transit time is prolonged on perfusion CT and perfusion magnetic resonance imaging (MRI) scans. Because
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ORIGINAL ARTICLE SHUNSUKE NAKAGAWA ET AL.
VALUE OF RED TONES IN VASCULAR RECONSTRUCTION SURGERY
Table 1. List of Patients in this Study Case 1
Age (years)/Sex
Diagnosis
Group
Bypass Procedure
Occlusion Time (minutes)
60s/M
ICS
CI
STA-MCA single
18
2
60s/F
ICAN
AN
RAG &STA-MCA
17/25
3
50s/F
ICAN
AN
RAG &STA-MCA
19/28
4
70s/F
ICAN
AN
RAG &STA-MCA
19/37
5
60s/M
MCO
CI
STA-MCA double
20/18
6
60s/M
ICO
CI
STA-MCA double
16/19
7
70s/M
MCS
CI
STA-MCA single
20
8
70s/M
MCO
CI
STA-MCA double
20/18
9
50s/F
ICS
CI
STA-MCA single
18
10
60s/F
ICO
CI
STA-MCA single
18
11
70s/F
MCAN
AN
Clipping STA-MCA
27
12
70s/M
ICO
CI
STA-MCA double
19/18
13
60s/F
ICAN
AN
RAG &STA-MCA
21/26
14
60s/F
ICS
CI
STA-MCA double
21/18
15
40s/F
ICS
CI
STA-MCA double
20/25
16
60s/F
ICAN
AN
RAG &STA-MCA
17/46
17
40s/F
ICS
CI
STA-MCA double
24/2
18
80s/F
ICAN
AN
RAG &STA-MCA
18/35
19
50s/F
MCS
CI
STA-MCA single
27
20
60s/F
ICAN
AN
RAG &STA-MCA
19/18
21
40s/F
MCS
CI
STA-MCA single and clip
25
22
50s/M
MCS
CI
STA-MCA single
21
23
40s/M
MCO
CI
STA-MCA double
21/17
24
60s/F
MCS
CI
STA-MCA single
28
25
60s/M
MCAN
AN
STA-MCA double
22/18
26
70s/F
ICS
CI
STA-MCA single
25
27
50s/M
MCAN
AN
STA-MCA double
21/25
28
60s/M
ICO
CI
STA-MCA single
25
29
40s/M
ICO
CI
STA-MCA single
24
30
70s/F
ICO
CI
STA-MCA single
39
31
80s/M
ICO
CI
STA-MCA single
30
32
70s/M
ICO
CI
STA-MCA single
27
33
50s/F
ICAN
AN
RAG &STA-MCA
17/27
34
40s/F
ICAN
AN
RAG &STA-MCA
21/31
35
20s/M
ICAN
AN
RAG &STA-MCA
18/26
36(¼27)
50s/M
MCAN
AN
Trapping & RAG
32
37
50s/M
ICO
CI
STA-MCA single
21
38
70s/M
ICO
CI
STA-MCA single
23
M, male; ICS, internal carotid artery stenosis; CI, atherosclerotic cerebral ischemic; STA, superficial temporal artery; MCA, middle cerebral artery; F, female; ICAN, internal carotid artery aneurysm; AN, cerebral aneurysm; RAG, radial artery graft bypass; MCO, middle cerebral artery occlusion; ICO, internal carotid artery occlusion; MCS, middle cerebral artery stenosis; MCAN, middle cerebral artery aneurysm.
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(Figures 2D and 3D), vessels with short transit times (the part the anastomosed STA undergoes transit at a normal blood flow where ICG flows in earlier) are shown as red tones, whereas velocity, the transit time is relatively short. Thus, we hypothesized vessels with long transit times are shown as blue tones. that if the anastomosis had been appropriately performed and This delay map image was automatically detected, and the color patency had been maintained, the proximal and distal sides of the of the anastomotic area was extracted as a result of the recipient and the donor vessels would be filled in red color code. The color of the anastomosis is the part of tones, and the transit time of the cortical vessel with the pink square in Figure 2, upper right, Figure 4, and poor cerebral blood flow would be delayed. We also Video 1, which is the anastomotic portion. Figure 5A investigated whether the direction of blood flow could and 5B and Video 1 present a diagram showing the be confirmed by observing the transit time of the anastomotic area. vessels shown. We examined whether these transit Video available at WORLDNEUROSURGERY.org times were significantly shorter than those of the vessels with poor blood flow that had not undergone Statistical Analysis anastomosis. Data are shown as a mean standard error. Statistical analysis was performed using JMP 11.0.0 statistical software (SAS Institute, Cary, North Carolina, USA). We used the paired Student t test with Delay Map Image Bonferroni correction to evaluate the tests for each ROI in all Cerebral blood flow evaluation software was installed for the combinations between the AN group and CI group. A P value Pentero microscope (Carl Zeiss) for FLOW 800 analysis. By using <0.05 was considered statistically significant. these data, the average intensity change can be evaluated by The color tone by color code evaluation from the donor vessel to 2 methods of relative rendering time (delay map) and relative the recipient vessel near the anastomotic site was evaluated, and luminance change (intensity map). In this study, we use the the result was compared between the CI and AN groups. The delayed map. In the delay map of the FLOW 800 system,15 the significance level was set at P < 0.05 in the c2 test. That is, the entire range of ICG-VAG is set as the ROI and the average infrequency of those showing red color tones was compared betensity change over time is automatically measured. In this mode, tween the AN and CI groups. In addition, we compared the color the whole field of view is captured as the ROI, and the time until frequencies of red to orange and other color frequencies between the average luminance becomes half of the maximum, which is the AN and CI groups. equally divided into the earliest part in the order of red, yellow, green, and blue. On the delay map using the FLOW 800 system RESULTS
Figure 1. The locations of the regions of interest. White square regions of interest are shown on the cortical middle cerebral artery. Yellow square regions of interest are shown on the recipient proximal middle cerebral artery. Green square regions of interest are shown on the recipient distal middle cerebral artery. Blue square regions of interest are shown on the recipient donor superficial temporal artery. Pink square regions of interest are indicated on the color code area (Figure 5). The color code (Figure 5) of all cases is extracted from the pink square range. *Middle cerebral artery. **The recipient donor superficial temporal artery.
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In the CI group (Table 2), the results of T1/2max were as follows. There were statistically significant differences between the T1/ 2max of the control MCA and T1/2max of the recipient proximal MCA (P <0.001), recipient distal MCA, and donor STA (P < 0.001) (Table 2). There were statistically significant differences between the T1/2max of the donor vessel and T1/2max of the recipient proximal MCA (P ¼ 0.0003), and the T1/2max of the recipient distal MCA and donor (P ¼ 0.0023) (Table 2). There were no statistically significant differences between the T1/2max of the recipient distal MCA and T1/2max of the recipient proximal MCA (P ¼ 0.794) (Table 2). In all patients in the CI group, the T1/2max of the donor vessel was shorter than the T1/2max of the control MCA. In the AN group (Table 3), the results of T1/2max were as follows. There were statistically significant differences between the T1/2max (recipient MCA proximal) and T1/2max (donor STA) (P ¼ 0.0054), and the T1/2max (recipient MCA distal) and T1/2max (MCA control) (P ¼ 0.0047), respectively (Table 3). No statistically significant differences were observed in other combinations. In a comparison between the donor STA and control MCA, the P value was low in the CI group (P < 0.001) compared with that in the AN group (P ¼ 0.0608). This finding suggested that the donor STA was more clearly visualized earlier in the CI group. Delay Map Using the FLOW 800 System, Patency, and MRI Findings The color tone of the anastomotic area (pink square in Figure 1 and upper right in Figure 2) of all cases are shown in Figure 5. Regarding the evaluation of color codes, the frequency of red
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ORIGINAL ARTICLE SHUNSUKE NAKAGAWA ET AL.
Figure 2. Intraoperative blood flow analysis imaging using the FLOW 800 system for arteriosclerotic cerebral internal carotid artery occlusion. (A) (Upper left) Intraoperative image of the surgical field after the superficial temporal artery (STA)-middle cerebral artery (MCA) single anastomosis for symptomatic atherosclerotic internal carotid artery occlusion. (B) (Lower left) Settings for the regions of interest were adjusted manually. (1): Red square: donor vessel (STA). (2): Green square: distal donor vessel (STA). (3) Blue square: recipient proximal MCA. (4) Pink square: recipient distal MCA. (5) Yellow square: cortical control MCA. (C) (Upper right) Delay map after STA-MCA anastomosis was performed in the arteriosclerotic
tones was statistically significant in the CI group (P ¼ 0.0155). In addition, the frequencies of red to orange were statistically significant in the CI group (P ¼ 0.0250). MRI, including MRA and DWI performed within 3 days postoperatively, did not show symptomatic ischemic complications in any patients. However, in 11 of 38 surgeries and 56 anastomoses, DWI scans indicated cortical ischemic lesions with a diameter of 3 mm or less as a result of minute coagulation of the bifurcation during recipient vessel anastomosis. MRA confirmed anastomotic vessel patency in all patients. DISCUSSION The results of this study suggest that by adding a quantitative assessment based on the rendering time (T1/2max) of the ROI on the target vessel using ICG-VAG, blood flow in the donor blood
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cerebral ischemic region. The donor STA and MCA around the anastomosis are shown in red (Red T). Small pink square on the distal end of STA indicate color code (Figure 5). The color code (Figure 5) of this case was extracted from the pink square range. (D) (Lower right) The calculations of indocyanine green fluorescence luminance. The point at which half of the maximum fluorescence luminance (T1/2max) is reached was calculated. Red graph: donor vessel (STA). Blue graph: recipient proximal MCA. Pink graph: recipient distal MCA. Yellow graph: cortical control MCA. The arteries from largest to smallest: STA>proximal MCA>proximal MCA>cortical control MCA of the measured value of T1/2max.
vessel and in both directions from the anastomotic part to the recipient can be quantitatively drawn. In addition, by reflecting prolongation of the transit time in ischemic lesions, the detection of blood flow failure in the proximal part of the donor vessel may be possible by comparing the difference in the rendering time of another cerebral vascular vessel from the recipient. The delay map of the FLOW 800 system can easily detect these findings by focusing on the imaging timing. The unique point of this study is that the patency of anastomotic vessels using ICG-VAG and the FLOW 800 system was evaluated as a quantitative value of its rendering time rather than as a change in fluorescence intensity. Angiography, Doppler, and ICG-VAG are available as intraoperative patency evaluation methods of vascular reconstructive surgery. However, no previous study has evaluated patency more accurately by simultaneously measuring the blood flow timing in the donor and recipient in both directions, and vessels unrelated
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Figure 3. Intraoperative blood flow analysis in the case of double superficial temporal artery (STA) to middle cerebral artery (MCA) for a large MCA aneurysm using the FLOW 800 system. (A) (Upper left) Intraoperative image of the surgical field after the STA-MCA double anastomosis for a large MCA aneurysm. (B) (Lower left) Settings for the regions of interest were adjusted manually. (1) Red square: donor vessel (parietal branch of STA)e1. (2) Green square: recipient distal MCAe1. (3) Blue square: recipient proximal MCAe1. (4) Pink square: recipient proximal MCAe2. (5) Yellow square:
recipient distal MCAe2. (6) Sky blue square: donor vessel (frontal branch of STA)e2. (7) Brown square: cortical control MCA. (C) (Upper right) Delay map after STA-MCA double anastomosis. The both branch of the STA and recipient MCA is yellow (yellow T). Small pink square on the distal end of STA indicates color code (Figure 5). The color code (Figure 5) of this case was extracted from the pink square range. (D) (Lower right) Indocyanine green fluorescence luminance. The point at which half the maximum fluorescence luminance is reached was calculated.
to anastomosis. During angiography, in which the contrast medium is injected under pressure, it is impossible to accurately determine the timing of visualization. With Doppler, it is impossible to simultaneously evaluate multiple blood vessels. To assess the patency of intraoperative anastomotic vessels, the following must be observed: Blood flow of the donor STA is flowing forward Blood of the donor vessel flows earlier than the MCA of the brain Blood flows in both directions from the anastomotic part to the recipient vessel These 3 findings are observed over time. We believe that our method can be used to observe all of these features. Figure 4. Extraction of the color code from the delay map image. Extraction of the color of the anastomosis, as in this case in all patients, is summarized in Figure 5.
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If surgeons do not confirm blood flow in both directions of the donor vessel by the delay map and it is stained white with ICGVAG, the ICG-VAG image shows blood vessels with all blood
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Figure 5. List of postoperative magnetic resonance imaging findings and results of the delay map study. The color tone of the anastomotic area (pink square in Figure 1, upper right in Figure 2, and upper right in Figure 3) of all
flow irrespective of timing; thus, it is difficult to determine whether ICG flows in with blood flow from the donor. Especially during bypass procedures for atherosclerotic ischemic lesions (CI
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cases is also shown. (A) List of results for the cerebral infarction group. (Continues)
group), our results showed a significantly short T1/2max in the donor vessels and the recipient vessels in both directions compared with the control MCA unrelated to the anastomosis. In
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Figure 5. (Continued) B) List of results for the cerebral aneurysm group. AN, cerebral aneurysm; CI, cerebral infarction; ICAN, internal carotid artery aneurysm; ICO, internal carotid artery occlusion; ICS, internal carotid artery stenosis; LSA, lenticulostriate artery; MCAN, middle cerebral artery
addition, in all patients in the CI group, the T1/2max of the control MCA was larger than that of the proximal MCA and that of the distal MCA distal, which was reflected in the delay map, with the proximal and distal sides of the donor vessels and the recipient vessels being indicated in red tones (Figure 2D). The FLOW 800 system, which has a delay map system, originally enabled us to obtain the red tone sign easily. This red tone sign on the delay map of ICG-VAG should be able to be used as an easy indicator of good patency during bypass procedure for ischemic atherosclerotic procedures. Without red tones, we can obtain the information about the patency with the quantitative assessment of the FLOW 800 system using the temporary proximal occlusion of the recipient vessel, because it is reliable during vascular reconstructive surgery. Patency-related findings were consistent with the MRI findings obtained within 3 days postoperatively. Therefore, we successfully showed that the evaluation of the direction
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aneurysm; MCO, middle cerebral artery occlusion; MCS, middle cerebral artery stenosis; NP, no particular; PCA, posterior cerebral artery; RAG, radial artery graft bypass; STA, superficial temporal artery; SCI, small ischemic change <3 mm.
and the transit time of blood flow are useful for confirming the patency of the vascular anastomosis. In patients with cerebral aneurysms, the level of transit time differs by case, so further invention is necessary. Short Transit Time Effect Our results were obtained because the T1/2max of the donor vessel was relatively short (i.e., the short transit time effect). Decreased cerebral blood flow on [123I]-iodoamphetamine single-photon emission CT causes prolonged mean transit time4,17-21 on perfusion CT or perfusion MRI scans. Furthermore, when the balloon occlusion test is conducted with ICA occlusion in patients with poor collateral vessels, cortical vein and artery transit times on the side of the occlusion are known to be delayed.22 In patients with cerebral hypoperfusion, postanastomosis blood flow from the STA means that it shows a short transit time compared with the blood flow in
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Table 2. Mean and Standard Error of Each Region of Interest (ROI) and Comparative Analysis of Regions of Interest in the Donor Vessel, Proximal Recipient Middle Cerebral Artery (MCA), Distal Recipient MCA, and Cortical Control MCA in the Arteriosclerotic Ischemic Disease Group Atherosclerotic Cerebral Ischemic Group
Mean
Standard Error
P Value 0.0003
Donor
34.298
2.220
MCA recipient proximal
34.61
2.679
MCA recipient distal
34.139
2.311
0.0023
Cortical MCA
36.419
2.308
<0.0001
MCA, middle cerebral artery.
the collateral vessels with decreased cerebral perfusion pressure. This finding of blood flow from the donor vessel showing an earlier filling than that from the cortical vessels is called the short transit time effect. In patients with cerebral hypoperfusion, the short transit time effect can be used to detect blood flow in both directions from the donor vessel at the anastomotic site. Using Doppler or ICG-VAG images monitored only according to fluorescence intensity, detection is impossible if the donor vessel is narrowed by kinking or vasospasm, causing delayed blood flow, or if there is blood flow in 1 direction only in the recipient vessel. However, with our method, we were able to solve these issues. In patients with cerebral aneurysms, there were no cerebral blood flow defects or prolonged transit time. For this reason, similar findings may be obtained by artificially prolonging the transit time by occluding the vessel with a temporary clip at the proximal MCA distal from the anastomotic site. In our case, red tones were confirmed in patients in whom ICG-VAG was performed with proximal occlusion of the recipient vessel. Importance in Confirming Patency In vascular reconstructive surgery, intraoperative confirmation of patency of the anastomosis is important. The COSS1 showed that angiography or Doppler can be used to confirm the patency. With Doppler, it is difficult to assess blood flow velocity4 and place the probe appropriately for monitoring both sides of the recipient vessel to detect the direction of blood flow. Doppler and ICG
imaging are unable to detect situations in which the anastomosis has failed and blood flow is flowing only peripherally or proximally from the anastomotic site. With ICGVAG alone, it is difficult to determine the direction of blood flow when the velocity of blood flow is fast. Thus, the evaluation of anastomotic vessel patency with ICG-VAG alone assesses only whether there is blood flow in the donor vessel. Studies regarding the evaluation of vascular anastomosis based on cerebral cortical luminance analysis using the FLOW 800 system have indicated problems related to quantitative evaluation.23 Therefore, we focused on T1/2max in the artery rather than evaluating the luminance itself. We also investigated whether the evaluation of the direction of blood flow in the recipient vessel could be used to accurately assess the patency of the anastomotic site. In particular, we confirmed that the quantitative analysis of the T1/2max in the donor vessel and the peripheral and proximal parts of the anastomotic site could be used to confirm peripheral and proximal blood flow in the donor anastomotic site. This finding indicates the possibility of achieving a stronger confirmation of the safety and efficacy of anastomosis using a combination of Doppler and ICG-VAG. The evaluation of cerebral cortical blood flow using ICG has several limitations. For instance, cerebral blood flow in deep areas of the cerebral parenchyma where light cannot enter cannot be evaluated. In addition, when cortical ICG-VAG luminance of the cerebral parenchyma is quantitatively evaluated, the
Table 3. Mean and Standard Error for Each Region of Interest (ROI) and Comparative Analysis of Regions of Interest in the Donor Vessel, Proximal Recipient Middle Cerebral Artery (MCA), Distal Recipient MCA, and Cortical Control MCA in the Cerebral Aneurysm Group Cerebral Aneurysm Group
Mean
Standard Error
P Value 0.0054
Donor
33.651
2.8597
MCA recipient proximal
32.636
2.9726
MCA recipient distal
37.376
3.3729
Cortical MCA
37.135
3.0693
0.0047
MCA, middle cerebral artery.
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injection speed, blood pressure, and heart rate variables, which are all difficult to regulate, may affect the results. To remove these difficulties related to quantitative evaluation, we focused on accurate patency evaluation of the anastomotic vessel rather than cerebral blood flow evaluation, and set ROIs only in visible cortical vessels. Studies of the quantitative evaluation method of patency of vascular anastomosis have been reported in the past 2 decades, and in this respect, our study is not new. These methods include investigations of visual light spectroscopy,24 flometry,25 and laser speckle imaging.26 These studies were intended to show the blood flow of donor blood vessels or cerebral blood flow. Therefore, we pointed out the usefulness of ICG-VAG from the viewpoint of prevention of complications of vascular anastomosis and timing of intensity not from the viewpoint of cerebral blood flow. This point differs from the conventional method. Various problems with the quantitative evaluation of luminance using the FLOW 800 system have been pointed out. The quantitative intensity evaluation of ICG is influenced by the plasma protein level.27,28 Therefore, it is affected by cholesterol and the amount of intraoperative infusion. Moreover, the difficulty of comparing the intensity between ROIs has been noted.10 This situation is because high-intensity blood vessels may affect the intensity evaluation of the surrounding tissues such as indirect illumination. It is optically called a point spread function.29,30 It is a function that represents the response to the point light source of the optical system. However, no previous study has served as a clinical example of ICG-VAG. According to Carl Zeiss, its software developers do not use a specific point spread function for corrections in its infrared 800 video. Furthermore, to reduce various influence, we decided to focus on differences in time until blood vessel depiction rather than intensity.
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Limitations We considered the following to be the limitations of the method of this study. First, because nonanastomotic regions of the recipient vessel must not be dissected, the range for setting ROIs with ICG is limited. While using ICG-VAG and the delay map, we could not change the visual axis, magnification, or focus of the microscope after the target vessel was in the ICG-VAG field. Therefore, it is not possible to change the direction or focus of the microscope to see the aneurysm from other orientations during ICG-VAG. Furthermore, in patients who have undergone vascular reconstructive surgery for cerebral aneurysms, cerebral blood flow is normal before aneurysm parent artery occlusion. Therefore, it is impossible to detect the short transit time effect and red tones. In patients who have undergone aneurysm surgery, the donor vessel being depicted without any delay in another normal cortical MCA is believed to confirm the patency of the anastomosis. In addition, this problem could be solved by ICG-VAG with temporary proximal occlusion of the recipient vessel. In the delay map image, color tone is based on the timing of the intensity visualization and quantitative evaluation, but there is a limit because it becomes the description of the color tone. However, we believe that this finding corresponds to the purpose of this research, which was to compare the fast part and the slow part of the visualization in 1 example shot. CONCLUSIONS In the CI group, the transit time of the donor was shown relatively early (i.e., red tones). Thus, a delay map image of the FLOW 800 system is useful to confirm patency in arteriosclerotic ischemic disease. However, physicians need another method of blood flow assessment such as temporary proximal occlusion in the AN group. When good patency has been achieved, the FLOW 800 system can be used to confirm the patency more reliably.
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neurosurgical procedures. J Cereb Blood Flow Metab. 2013;33:1000-1007. 10. Kamp MA, Slotty P, Turowski B, Etminan N, Steiger HJ, Hänggi D, et al. Microscope-integrated quantitative analysis of intraoperative indocyanine green fluorescence angiography for- blood flow assessment: first experience in 30 patients. Neurosurgery. 2012;70:65-74. 11. Raabe A, Beck J, Gerlach R, Zimmermann M, Seifert V. Near-infrared indocyanine green video angiography: a new method for intraoperative assessment of vascular flow. Neurosurgery. 2003;52: 132-139. 12. Raabe A, Nakaji P, Beck J, Kim LJ, Hsu FP, Kamerman JD, et al. Prospective evaluation of surgical microscope-integrated intraoperative near-infrared indocyanine green videoangiography during aneurysm surgery. J Neurosurg. 2005;103: 982-989. 13. Woitzik J, Horn P, Vajkoczy P, Schmiedek P. Intraoperative control of extracranial-intracranial bypass patency by near-infrared indocyanine green videoangiography. J Neurosurg. 2005;102: 692-698.
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cerebral blood volume, and mean transit time in patients with acute ischemic stroke determined by perfusion-weighted MRI(magnetic resonance image). J Cereb Blood Flow Metab. 2003;23:605-611. 21. Van Rooij WJ, Sluzewski M, Slob MJ, Rinkel GJ. Predictive value of angiographic testing for tolerance to therapeutic occlusion of the carotid artery. AJNR Am J Neuroradiol. 2005;26:175-178. 22. Kaesemann P, Thomalla G, Cheng B, Treszl A, Fiehler J, Forkert ND. Impact of severe extracranial ICA stenosis on MRI (magnetic resonance image) perfusion and diffusion parameters in acute ischemic stroke. Front Neurol. 2014;5:254. 23. Prinz V, Hecht N, Kato N, Vajkoczy P. FLOW 800 allows visualization of hemodynamic changes after extracranial-to-intracranial bypass surgery but not assessment of quantitative perfusion or flow. Neurosurgery. 2014;10(suppl 2):231-239. 24. Hoshino T, Katayama Y, Sakatani K, Kano T, Murata Y. Intraoperative monitoring of cerebral blood oxygenation and hemodynamics during extracranial-intracranial bypass surgery by a newly developed visible light spectroscopy system. Surg Neurol. 2006;65:569-576. 25. Mucke T, Wolff KD, Wagenpfeil S, Holzle F, Scholz M. Reliability of near-infrared angiography and micro-Doppler sonography for evaluating microvascular anastomoses. Plast Reconstr Surg. 2010;126:1506-1514. 26. Nomura S, Inoue T, Ishihara H, Koizumi H, Suehiro E, Oka F, et al. Reliability of laser speckle flow imaging for intraoperative monitoring of cerebral blood flow during cerebrovascular surgery: comparison with cerebral blood flow
measurement by single photon emission computed tomography. World Neurosurg. 2014;82: e753-e757. 27. Wang Y, Wang C, Ding Y, Li J, Li M, Liang X, et al. Biomimetic HDL nanoparticle mediated tumor targeted delivery of indocyanine green for enhanced photodynamic therapy. Colloids Surf B Biointerfaces. 2016;148:533-540. 28. Halle BM, Poulsen TD, Pedersen HP. Indocyanine green plasma disappearance rate as dynamic liver function test in critically ill patients. Acta Anaesthesiol Scand. 2014;58:1214-1219. 29. Ghosh S, Preza C. Fluorescence microscopy point spread function model accounting for aberrations due to refractive index variability within a specimen. J Biomed Opt. 2015;20:75003. 30. Yoo H, Song I, Gweon DG. Measurement and restoration of the point spread function of fluorescence confocal microscopy. J Microsc. 2006;221: 172-176.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 13 August 2017; accepted 16 November 2017 Citation: World Neurosurg. (2017). https://doi.org/10.1016/j.wneu.2017.11.072 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2017 Elsevier Inc. All rights reserved.
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