Clinical Neurology and Neurosurgery 119 (2014) 70–74
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Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Target-controlled infusion technique with indocyanine green videoangiography for radial artery graft Yasuo Murai a,∗ , Takayuki Mizunari b , Kenta Koketsu b , Kojiro Tateyama a , Shiro Kobayashi b , Katsuya Umeoka b , Akira Teramoto a , Akio Morita a a b
Department of Neurosurgery, Nippon Medical School, Tokyo, Japan Department of Neurosurgery, Nippon Medical School Chiba Hokuso Hospital, Chiba, Japan
a r t i c l e
i n f o
Article history: Received 2 August 2013 Received in revised form 27 December 2013 Accepted 19 January 2014 Available online 31 January 2014 Keywords: Cerebral aneurysm Clip Indocyanine green Parent artery Radial artery
a b s t r a c t Object: To understand the relationship between the parent artery and its distal arteries, blood vessels running through the subarachnoid space need to be extensively dissected, which is time-consuming. We examined the efficacy of temporary clipping with the indocyanine green (ICG) technique (targetcontrolled infusion (TCI) technique), in which the parent artery is occluded using a temporary clip, and ICGV (videoangiography) is performed to clarify the relationship between the distal M4 and proximal M2. Methods: Thirteen radial artery grafts (RAGs) for internal carotid aneurysm underwent TCI to confirm the relationship between M2 and cortical M4. To monitor the perfusion pressure of the cortical middle cerebral artery, superficial temporal artery (STA) to M4 anastomosis was performed before RA-M2 anastomosis. We performed anastomosis of the recipient of STA- M4 that was distal and downstream of the M2 segment that is the recipient of RA-M2 anastomosis. To select the proper recipient M4 of the STA-M4 anastomosis, the ICGV image range was set sufficiently wide to accommodate the possibility that the distal artery was not the one anticipated. ICGV followed complete occlusion by temporary clipping of the recipient M2. Results: In 2 of the 13 cases, the relationship between the M2 and M4 could not be clarified. Conclusions: In cases with developed collateral circulation or small perfusion area of the occluded M2, it was difficult to ascertain the relationship by TCI. Nevertheless, TCI was useful in 11 of the 13 cases, suggesting that unnecessary dissection in the subarachnoid space may be reduced using this technique. © 2014 Elsevier B.V. All rights reserved.
1. Introduction The procedure for radial artery graft (RAG) [1–2] has been described in many reports [3–9], which strongly recommended [7–9] performing a superficial temporal artery (STA) to distal middle cerebral artery (M4 segment of MCA) anastomosis before performing the anastomosis of the radial artery (RA) to the M2 segment of the MCA. Our main therapeutic approach [1,4–6] for complex carotid aneurysms is one-stage cervical internal carotid artery ligation and RAG combined with STA–MCA anastomosis (Fig. 1). In our opinion [1,2,4–8], it is difficult to determine the best surgical strategy in the presence of high flow bypass, solely on the basis of preoperative angiographic findings or cerebral blood flow studies including single photon emission CT with short time temporary occlusion. Additionally, the preoperative occlusion test has the risk of ischemic complications [1,3,4,5]. Therefore, the decision about the surgical strategy was made after direct intraoperative determination of MCA pressure findings via the STA branch
∗ Corresponding author. Tel.: +81 3 3822 2131; fax: +81 3 5685 0986. E-mail address: [email protected] (Y. Murai). 0303-8467/$ – see front matter © 2014 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.clineuro.2014.01.015
[1,4,5,7]. When the investigators performed RAG, a superficial temporal artery (STA)–MCA bypass is used in all patients. The main purpose of the STA–MCA bypass is to monitor MCA pressure by the superficial temporal artery (also called double insurance bypass) [1,4,5,8,9]. This procedure is otherwise known as an assisted bypass [1,4,7,9], and its purpose [1,4,7,9] is to avoid ischemia during the temporary occlusion period in the M2–RA anastomosis. Other key purposes [1,4,7,9] of the technique were to allow the measurement of perfusion pressure on the brain surface after completion of RAG to monitor the patency of the anastomoses and to verify that blood flow through the graft was neither excessive or inadequate. Because the STA–MCA anastomosis is only one step [1,3–6] in the surgical procedure of high-flow bypass including RAG, the M4 segment on the brain surface, which is the M2 peripheral blood vessel, needs to be confirmed along with the continuation of M2 to M4. This requires extensive dissection of the sylvian fissure. The purpose of this study was to confirm the benefits of temporarily occluding the proximal recipient M2 and performing indocyanine green videoangiography (ICGVAG) [8–13] (targetcontrolled infusion (TCI) technique) to confirm the continuation of the distal/peripheral M4.
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Fig. 2. Preoperative lateral view of left internal carotid digital subtraction angiography showing a giant cavernous carotid aneurysm.
saphenous vein or the radial artery [2,7,13,14], simple proximal internal carotid artery occlusions [15], endovascular treatment, or a combination of these strategies [14]. We [4,5,8] have successfully used RAG, while treating a complex internal carotid artery aneurysm that we found difficult to clip. Low flow bypass using STA–MCA anastomosis and simple ligation for poor collateral patients are known risk factors for ischemic complications [2,7,8,14,15]. Therefore, RAG was performed in all the patients for the occlusion of the ICA. This approach was adopted along with the cerebral blood flow (CBF) study with the short-time balloon occlusion or the angiographical findings were not reliable enough to determine whether the ICA could be safely ligated without exposing the patient to the risk of short- or long-term cerebral ischemia or de novo formation of aneurysms, as this procedure is also associated with an approximately 3% risk of complications [2,7,8,14,15]. 2.2. Basic procedure for TCI
Fig. 1. Schematic drawing of the concept of external carotid artery–radial artery–middle cerebral artery (M2) anastomosis and superficial temporal artery to middle cerebral artery (M4) anastomosis for giant cavernous carotid aneurysms.
1.1. Materials From March 2007 to July 2013, we used this method for the following 13 patients: 9 cases with cavernous carotid aneurysm, 1 with petrous carotid aneurysm, 1 with paraclinoid aneurysms, and 2 with internal carotid artery anterior wall aneurysms. The patients were 3 men and 10 women, ranging in age from 62 to 74 years (mean, 68.2 years), with 2 ruptured aneurysms (World Federation of Neurological Societies (WFNS) scale grade II) and 11 unruptured large or giant complex carotid aneurysms. These cases were retrospectively examined. During this period, 411 cases received treatment for cerebral aneurysms at our institutions. TCI was used to determine the correct distal MCA for performing the STA–MCA anastomosis for complex internal carotid artery aneurysms. Informed consent was obtained from each patient or their families. This study was approved by the ethics committee of Nippon Medical School Hospital.
RAG involves opening the sylvian fissure and identifying the M2 segment that is suitable for RA–M2 anastomosis without perforating arteries or disturbing the arteriosclerotic changes. A rubber sheet was stretched under the M2 segment for preparation of the anastomosis, and the brain surface was carefully examined to include the M4–M5 segment and to identify blood vessels ≥1 mm in diameter for inclusion in the ICGVAG imaging range. Using a temporary clip, the recipient M2 was temporarily occluded, and ICGVAG (0.3 mg/kg) was performed to confirm that the recipient M4 segment was suitable for STA–MCA anastomosis [3,4,6,7,9]. 3. Results No ICG allergic reactions were observed in any of the cases, and ICG imaging was possible in all cases. In 2 of the 13 RAG cases, the M4 segment within the ICGVAG range on the brain surface covered the entire area and the relationship with the proximal M2 could not be ascertained. This may have occurred due to one or more of the following reasons: (1) temporary clipping occlusion was inadequate; (2) there was sufficient collateral circulation; or (3) the area of the occluded M2 segment was narrow and not within the range of the dural incision.
2. Methods
3.1. Representative cases
Aneurysmal surgical treatments in thirteen cases were performed using a Carl Zeiss Surgical Microscope OPMI Pentero INFRARED 800 (Carl Zeiss Co., Tokyo, Japan).
3.1.1. Case 1 In a 63-year-old female suffering double vision due to abducens nerve palsy, a giant aneurysm in the cavernous portion of the left internal carotid artery (ICA) (Fig. 2) was confirmed by cerebral angiography, which revealed a narrow posterior communicating artery (Pcom), hypoplasia of the right A1, and poor collateral circulation. RAG and ligation of the cervical internal carotid artery were performed.
2.1. Basic strategies of RAG Various treatment strategies adopted for complex carotid aneurysms include the following: revascularization using the
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Fig. 3. Left: Microscopic findings in the surgical field using the left trans-sylvian approach. Middle. ICGVAG image taken 9 s after ICG infusion. The M2 segment of the middle cerebral artery has been temporary clipped. Peripheral middle cerebral arteries on the temporal cortex were not enhanced (white arrow) and frontal cortex were enhanced (black arrow). Right An ICGVAG image was obtained 28 s after the ICG infusion showed the patency of the STA–MCA and ECA–RA–MCA anastomoses. The small white arrow indicates the superficial temporal artery, and the white arrowhead indicates the radial artery.
The cervical carotid artery was dissected, and the external carotid artery (ECA) was exposed to the bifurcation of the occipital artery. Following fronto-temporal craniotomy, a 24 F chest tube was inserted from the space between the 12th cranial nerve and the digastric muscle to the extracranial middle fossa under the temporal muscle [3,9]. The sylvian fissure was widely opened, exposing the M1 to the proximal M4 segment of the MCA. Based on the arteriosclerotic findings and the perforating branch, we selected the M2 segment believed to be appropriate for RA–M2 anastomosis. Thereafter, microscopic magnification and visual axis were configured so that the ICGVAG range would include the entire brain surface within the dural incision (Fig. 3, left). The M2 segment prepared for anastomosis was temporarily occluded using a Sugita No. 51 temporary clip followed by ICGVAG. The distal cortical MCA branch on the brain surface was identified without visualizing the temporal lobe (Fig. 3, middle). The STA (frontal branch) to M4 anastomosis on the temporal side of the MCA was performed (temporary occlusion time was 16 min). Next, the extracted RA was inserted into the chest tube passing from below the temporal muscle along the middle fossa through the space between the 12th cranial nerve and the digastric muscle. The RA–MCA anastomosis was performed (temporary occlusion duration, 38 min) and followed by the ECA–RA anastomosis. ICGVAG findings of the STA–MCA and ECA–RA–MCA anastomoses indicated patency in both bypasses (Fig. 3, right). Invasive blood pressure (BP) measurements using the STA parietal branch revealed an STA pressure of 110/64 mm Hg (systemic BP of 118/71 mm Hg). On occlusion of the proximal STA,
the systemic BP was 116/68 and the pressure in the cortical MCA was 92/57 mm Hg. When the cervical ICA was occluded using a bulldog clamp, the MCA pressure on the brain surface was 32/28 mm Hg, which increased to 76/48 mm Hg after opening the RAG. When the cortical MCA pressure from the RAG reached 80% of the normal flow from the ICA, it was deemed satisfactory. The patient recovered well with no postoperative neurological deterioration. Diffusion-weighted imaging (DWI) (Fig. 4, left) on postoperative day 2 revealed no new ischemic findings. Threedimensional computed tomographic (3D CT) angiography on day 8 identified the RAG and STA–MCA anastomosis (Fig. 4, right). 3.1.2. Case 2 A 67-year-old male presented with change in mental status caused by a left ICA anterior wall aneurysm (ICAW) (Fig. 5. upper left). Aneurysm trapping and RAG were performed. The surgical procedure was similar to that performed in case 1. The sylvian fissure was opened, and the microscopic magnification and visual axis were configured to visualize the range of the entire dural incision on the brain surface (Fig. 5, upper right). The M2 to RA–M2 anastomosis was temporarily occluded using a Sugita No. 51 temporary clip followed by ICGVAG. The entire cortical MCA on the brain surface within the opened dura was enhanced on ICGVAG (Fig. 5, lower left). Therefore, the distal cortical MCA branch on the brain surface was not identified. Subarachnoid hemorrhage (SAH) was irrigated on opening of the sylvian fissure to confirm the relationship between the distal cortical MCA and M2. Because the appropriate
Fig. 4. Left: Diffusion-weighted image on day 2 showing no abnormal ischemic findings on the surgical side. Right: Postoperative three-dimensional CT angiography demonstrating good patency of the STA–MCA (small arrow) anastomosis and ECA–RA–M2 bypass (large arrow).
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Fig. 5. Upper left: Preoperative oblique view of internal carotid artery three-dimensional angiography showing an internal carotid artery anterior wall aneurysm (white arrow). A posterior communicating artery and an anterior choroidal artery were branching from almost the same segment of the internal carotid artery. Upper right: Microscopic findings of the surgical field using the left trans-sylvian approach. Lower left: ICGVAG image taken 24 s after ICG infusion. The M2 segment of the middle cerebral artery has been temporary clipped. All cortical branches of the middle cerebral arteries were enhanced within the surgical field. Lower right: Postoperative three-dimensional CT angiography demonstrating good patency of the STA (small arrow)–MCA anastomosis and ECA–RA (large arrow)–M2 bypass.
distal cortical MCA branch could not be identified, the temporal M4 on the brain surface was selected for anastomosis to avoid complications related to excessive dissection of the sylvian fissure. Once all anastomoses had been completed, invasive blood pressure (BP) measurements using the STA parietal branch revealed an STA pressure of 92/54 mm Hg (systemic BP of 110/64 mm Hg). On occlusion of the proximal STA, the systemic BP was 108/68 mm Hg and the pressure in the cortical MCA was 84/48 mm Hg. When the cervical ICA was occluded using a bulldog clamp, the MCA pressure on the brain surface was 43/32 mm Hg, which increased to 64/38 mm Hg after opening the RAG. Invasive BP measurements were continued following occlusion of the proximal STA with a Sugita temporary clip no. 51. The ICAW was trapped using Yasargil aneurysm clips FT747T and FT750T (Aesculap, San Francisco, CA, USA). ICGVAG imaging revealed retrograde blood flow from the RAG and Pcom circulation. Immediately before suturing the dura and adherence of fibrin glue to the outside of the dura, direct measurement of arterial BP was continued for 96 min, during which time the MCA–BP on the surface of the brain increased to 79/60 mm Hg. DWI on postoperative day 4 revealed no new ischemic findings. 3D CT angiography on day 9 identified the RAG and STA–MCA anastomosis (Fig. 5. lower right). At 7 weeks after surgery, diffuse muscular weakness was the only symptom that required treatment, and the patient was transferred for rehabilitation. 4. Discussion Because there are few anatomical markers for the distal MCA, identifying the M2–M3 bifurcation is more difficult than identifying the circle of Willis [16,17]. We used TCI and a combination
of temporary clipping and ICGVAG to confirm the continuity of arteries. This study indicated that TCI may help reduce surgical time and avoid brain damage by reducing the size of the opening in the subarachnoid space. Although the 13 cases treated in our study represent a limited group, intraoperative findings, postoperative DWI–MRI, and postoperative magnetic resonance angiography revealed no complications associated with TCI. In the 2 cases that underwent RAG, a connection could not be confirmed between M2 (occluded by temporary clipping) and M4 within the range of the dural incision. 4.1. The significance of STA–MCA anastomosis in RAG Temporary occlusion requires more time with a RA–M2 anastomosis than with a STA–MCA anastomosis because of the deep surgical field and long suture line [1,9]. To avoid ischemia during the anastomosis and for the purpose of post-bypass monitoring, several reports [1,3,7,9] have recommended STA–MCA anastomosis. With respect to the recipient artery for the STA–MCA anastomosis, previous reports [1,3,7,9] have recommended performing the STA–M4 bypass as the “assisted bypass”, and we have used this method as well. We [7,9] believe that the following are the 3 main objectives of this method: (1) to maintain blood flow of the peripheral MCA when performing the RA–MCA anastomosis; (2) to monitor the adequacy of blood flow after completion of RAG; and (3) to supplement blood flow when the RA lumen is restricted. The STA–MCA bypass was first termed “assisted bypass” by Kamiyama et al. [1], who used it to maintain blood flow in the peripheral MCA when performing a RA–MCA anastomosis. Experience [7–9] gained from over 98 cases of RAG has led us to
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believe that the most important point during the STA–MCA bypass is to monitor the adequacy of blood flow after completion of all bypasses. Data obtained from invasive BP measurements of the MCA using the STA–MCA anastomosis are quantitative and can only confirm lack of blood flow from the RA intraoperatively. When the frontal branches of the STA are used for anastomosis, invasive BP measurements are performed on the parietal branch of the STAs. When the bifurcation of the frontal branch and parietal branch is located proximally, this method cannot be used. Therefore, to take post-RAG measurements in such cases, direct puncture or measurements using the small branch of the anastomosed STA is required. When the M1–M2 bifurcation is shallow or when the surgical field is wide in the M2 segment and prolonged occlusion time is not needed to perform the RA–M2 anastomosis, we select the M4 segment that is not the distal M2 segment used for the RA–M2 anastomosis to monitor the adequacy of blood flow post-RAG. This is because we believe that perfusion pressure is more accurate. In cases where both RA–M2 and STA–M4 anastomoses are performed on the same continuous artery and the anastomosis fails, the RA–M2 bypass flows only peripherally to M4 and perfusion pressure from the STA–MCA anastomosis does not reflect perfusion pressure in other M2 segments. Therefore, when the M1–M2 bifurcation is deep or when arteriosclerotic changes are present in the M2 segment and prolonged occlusion time is needed to perform the RA–M2 anastomosis, both RA–M2 and STA–M4 anastomoses should be performed on the same continuous artery, allowing for the appropriate recipient M4 segment to be selected based on the patient’s condition. In our study, a connection between M2 and M4 on the brain surface was confirmed in approximately 84.6% of RAG cases. Moreover, postoperative DWI revealed no ischemic complications, which is believed to be associated with the surgical procedure. We believe that this method is useful for rapid and simple verification of the connection between the proximal and distal blood vessels. However, depending on the number of M2 branches running along the M4, the connection may not always be apparent. To increase the success rate, we used a wider dural incision and utilized the corical perfusion measurement indocyanin green video angiography with Pentero FLOW 800 system [18] and Doppler flowmetry [19,20]. There is a possibility that that the narrow observational range with ICG imaging and the dural incision has an impact on the success rate. Therefore, we emphasize the importance of an adequate observation area with ICGVAG. Intraoperative ICG videoangiography with the Flow 800 system is helpful in detecting the effects on the vascular supply during the temporary occlusion of the proximal artery. There are some reports indicating that the Pentero Flow 800 system [18] increases the sensitivity of ICGVAG and improves the capability to detect changes in cerebral blood flow [18]. Additionally, Doppler flowmetry would be helpful to detect the effects on the vascular supply during the temporary occlusion of the proximal artery [19,20]. 4.2. Benefits of TCI We investigated the time for the dissection of the sylvian fissure before TCI technique from operative videos in seven cases. The time for the dissection of sylvian fissure to confirm the communication of M2 and the distal M4 was 22–43 min (mean 28 min), and in one case, continuity could not be confirmed because of a tortuous M3 segment. Using TCI, it would be possible to shorten this time. 5. Conclusions Of the 13 RAG cases in our study, TCI was useful in 11 cases, suggesting that unnecessary dissection in the subarachnoid space may be reduced.
The communication between blood vessels could not be clarified in 2 cases. In cases with developed collateral circulation, inadequate temporary clipping occlusion, or narrow circulation area of the occluded M2, it was difficult to ascertain the relationship between the parent artery and the distal/peripheral blood vessels by TCI. Utilization of Doppler flowmetry or the Pentero FLOW 800 system may increase the success rate. Disclosure The author reports no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. References [1] Kamiyama H. Bypass with radial artery graft. No Shinkei Geka 1994;22: 911–24. [2] Sekhar LN, Stimac D, Bakir A, Rak R. Reconstruction options for complex middle cerebral artery aneurysms. Neurosurgery 2005;56(1 (Suppl)):66–74. [3] Houkin K, Kamiyama H, Kuroda S, Ishikawa T, Takahashi A, Abe H. Long-term patency of radial artery graft bypass for reconstruction of the internal carotid artery. Technical note. J Neurosurg 1999;90:786–90. [4] Mizunari T, Murai Y, Kim K, Kobayashi S, Kamiyama H, Teramoto A. Posttraumatic carotid-cavernous fistulae treated by internal carotid artery trapping and high-flow bypass using a radial artery graft – two case reports. Neurol Med Chir (Tokyo) 2011;51:113–6. [5] Murai Y, Mizunari T, Umeoka K, Tateyama K, Kobayashi S, Teramoto A. Radial artery grafts for symptomatic cavernous carotid aneurysms in elderly patients. Neurol India 2011;59:537–41. [6] Murai Y, Mizunari T, Umeoka K, Tateyama K, Kobayashi S, Teramoto A. A simple technique to prevent and correct graft vessel kinking in the subcutaneous tunnel: technical note. Clin Neurol Neurosurg 2011;113:835–8. [7] Kubo Y, Ogasawara K, Tomitsuka N, Otawara Y, Kakino S, Ogawa A. Revascularization and parent artery occlusion for giant internal carotid artery aneurysms in the intracavernous portion using intraoperative monitoring of cerebral hemodynamics. Neurosurgery 2006;58:43–50. [8] Murai Y, Mizunari T, Umeoka K, Tateyama K, Kobayashi S, Teramoto A. Ischemic complications after radial artery grafting and aneurysmal trapping for ruptured internal carotid artery anterior wall aneurysm. World Neurosurg 2012;77:166–71. [9] Ishikawa T, Kamiyama H, Kobayashi N, Tanikawa R, Takizawa K, Kazumata K. Experience from “double-insurance bypass.” Surgical results and additional techniques to achieve complex aneurysm surgery in a safer manner. Surg Neurol 2005;63:485–90. [10] Murai Y, Adachi K, Takagi R, Koketsu K, Matano F, Teramoto A. Intraoperative Matas test using microscope-integrated intraoperative indocyanine green videoangiography with temporary unilateral occlusion of the A1 segment of the anterior cerebral artery. World Neurosurg 2011:76, 477.e7–10. [11] Murai Y, Adachi K, Matano F, Tateyama K, Teramoto A. Indocyanin green videoangiography study of hemangioblastomas. Can J Neurol Sci 2011;38: 41–7. [12] 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;52:132–9. [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;102:692–8. [14] Hacein-Bey L, Connolly Jr ES, Mayer SA, Young WL, Pile-Spellman J, Solomon RA. Complex intracranial aneurysms: combined operative and endovascular approaches. Neurosurgery 1998;43:1304–12. [15] Niiro M, Shimozuru T, Nakamura K, Kadota K, Kuratsu J. Long-term follow-up study of patients with cavernous sinus aneurysm treated by proximal occlusion. Neurol Med Chir (Tokyo) 2000;40:88–97. [16] Lee SH, Bang JS. Distal middle cerebral artery M4 aneurysm surgery using navigation-CT angiography. J Korean Neurosurg Soc 2007;42:478–80. [17] Schmid-Elsaesser R, Muacevic A, Holtmannspötter M, Uhl E, Steiger HJ. Neuronavigation based on CT angiography for surgery of intracranial aneurysms: primary experience with unruptured aneurysms. Minim Invasive Neurosurg 2003;46:269–77. [18] Holling M, Brokinkel B, Ewelt C, Fischer BR, Stummer W. Dynamic ICG fluorescence provides better intraoperative understanding of arteriovenous fistulae. Neurosurgery 2013;73(1 (Suppl)):ons93-99. [19] Stadie A, Fukui K, Schramm P, Werner C, Oertel J, Engelhard K, Fischer G. Measurement of cortical microcirculation during intracranial aneurysm surgery by combined laser-Doppler flowmetry and photospectrometry. Neurosurgery 2011;69:391–8. [20] Kawamata T, Kawashima A, Yamaguchi K, Hori T, Okada Y. Usefulness of intraoperative laser Doppler flowmetry and thermography to predict a risk of postoperative hyperperfusion after superficial temporal artery-middle cerebral artery bypass for moyamoya disease. Neurosurg Rev 2011;34:355–6.
Contents lists available at ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Target-controlled infusion technique with indocyanine green videoangiography for radial artery graft Yasuo Murai a,∗ , Takayuki Mizunari b , Kenta Koketsu b , Kojiro Tateyama a , Shiro Kobayashi b , Katsuya Umeoka b , Akira Teramoto a , Akio Morita a a b
Department of Neurosurgery, Nippon Medical School, Tokyo, Japan Department of Neurosurgery, Nippon Medical School Chiba Hokuso Hospital, Chiba, Japan
a r t i c l e
i n f o
Article history: Received 2 August 2013 Received in revised form 27 December 2013 Accepted 19 January 2014 Available online 31 January 2014 Keywords: Cerebral aneurysm Clip Indocyanine green Parent artery Radial artery
a b s t r a c t Object: To understand the relationship between the parent artery and its distal arteries, blood vessels running through the subarachnoid space need to be extensively dissected, which is time-consuming. We examined the efficacy of temporary clipping with the indocyanine green (ICG) technique (targetcontrolled infusion (TCI) technique), in which the parent artery is occluded using a temporary clip, and ICGV (videoangiography) is performed to clarify the relationship between the distal M4 and proximal M2. Methods: Thirteen radial artery grafts (RAGs) for internal carotid aneurysm underwent TCI to confirm the relationship between M2 and cortical M4. To monitor the perfusion pressure of the cortical middle cerebral artery, superficial temporal artery (STA) to M4 anastomosis was performed before RA-M2 anastomosis. We performed anastomosis of the recipient of STA- M4 that was distal and downstream of the M2 segment that is the recipient of RA-M2 anastomosis. To select the proper recipient M4 of the STA-M4 anastomosis, the ICGV image range was set sufficiently wide to accommodate the possibility that the distal artery was not the one anticipated. ICGV followed complete occlusion by temporary clipping of the recipient M2. Results: In 2 of the 13 cases, the relationship between the M2 and M4 could not be clarified. Conclusions: In cases with developed collateral circulation or small perfusion area of the occluded M2, it was difficult to ascertain the relationship by TCI. Nevertheless, TCI was useful in 11 of the 13 cases, suggesting that unnecessary dissection in the subarachnoid space may be reduced using this technique. © 2014 Elsevier B.V. All rights reserved.
1. Introduction The procedure for radial artery graft (RAG) [1–2] has been described in many reports [3–9], which strongly recommended [7–9] performing a superficial temporal artery (STA) to distal middle cerebral artery (M4 segment of MCA) anastomosis before performing the anastomosis of the radial artery (RA) to the M2 segment of the MCA. Our main therapeutic approach [1,4–6] for complex carotid aneurysms is one-stage cervical internal carotid artery ligation and RAG combined with STA–MCA anastomosis (Fig. 1). In our opinion [1,2,4–8], it is difficult to determine the best surgical strategy in the presence of high flow bypass, solely on the basis of preoperative angiographic findings or cerebral blood flow studies including single photon emission CT with short time temporary occlusion. Additionally, the preoperative occlusion test has the risk of ischemic complications [1,3,4,5]. Therefore, the decision about the surgical strategy was made after direct intraoperative determination of MCA pressure findings via the STA branch
∗ Corresponding author. Tel.: +81 3 3822 2131; fax: +81 3 5685 0986. E-mail address: [email protected] (Y. Murai). 0303-8467/$ – see front matter © 2014 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.clineuro.2014.01.015
[1,4,5,7]. When the investigators performed RAG, a superficial temporal artery (STA)–MCA bypass is used in all patients. The main purpose of the STA–MCA bypass is to monitor MCA pressure by the superficial temporal artery (also called double insurance bypass) [1,4,5,8,9]. This procedure is otherwise known as an assisted bypass [1,4,7,9], and its purpose [1,4,7,9] is to avoid ischemia during the temporary occlusion period in the M2–RA anastomosis. Other key purposes [1,4,7,9] of the technique were to allow the measurement of perfusion pressure on the brain surface after completion of RAG to monitor the patency of the anastomoses and to verify that blood flow through the graft was neither excessive or inadequate. Because the STA–MCA anastomosis is only one step [1,3–6] in the surgical procedure of high-flow bypass including RAG, the M4 segment on the brain surface, which is the M2 peripheral blood vessel, needs to be confirmed along with the continuation of M2 to M4. This requires extensive dissection of the sylvian fissure. The purpose of this study was to confirm the benefits of temporarily occluding the proximal recipient M2 and performing indocyanine green videoangiography (ICGVAG) [8–13] (targetcontrolled infusion (TCI) technique) to confirm the continuation of the distal/peripheral M4.
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Fig. 2. Preoperative lateral view of left internal carotid digital subtraction angiography showing a giant cavernous carotid aneurysm.
saphenous vein or the radial artery [2,7,13,14], simple proximal internal carotid artery occlusions [15], endovascular treatment, or a combination of these strategies [14]. We [4,5,8] have successfully used RAG, while treating a complex internal carotid artery aneurysm that we found difficult to clip. Low flow bypass using STA–MCA anastomosis and simple ligation for poor collateral patients are known risk factors for ischemic complications [2,7,8,14,15]. Therefore, RAG was performed in all the patients for the occlusion of the ICA. This approach was adopted along with the cerebral blood flow (CBF) study with the short-time balloon occlusion or the angiographical findings were not reliable enough to determine whether the ICA could be safely ligated without exposing the patient to the risk of short- or long-term cerebral ischemia or de novo formation of aneurysms, as this procedure is also associated with an approximately 3% risk of complications [2,7,8,14,15]. 2.2. Basic procedure for TCI
Fig. 1. Schematic drawing of the concept of external carotid artery–radial artery–middle cerebral artery (M2) anastomosis and superficial temporal artery to middle cerebral artery (M4) anastomosis for giant cavernous carotid aneurysms.
1.1. Materials From March 2007 to July 2013, we used this method for the following 13 patients: 9 cases with cavernous carotid aneurysm, 1 with petrous carotid aneurysm, 1 with paraclinoid aneurysms, and 2 with internal carotid artery anterior wall aneurysms. The patients were 3 men and 10 women, ranging in age from 62 to 74 years (mean, 68.2 years), with 2 ruptured aneurysms (World Federation of Neurological Societies (WFNS) scale grade II) and 11 unruptured large or giant complex carotid aneurysms. These cases were retrospectively examined. During this period, 411 cases received treatment for cerebral aneurysms at our institutions. TCI was used to determine the correct distal MCA for performing the STA–MCA anastomosis for complex internal carotid artery aneurysms. Informed consent was obtained from each patient or their families. This study was approved by the ethics committee of Nippon Medical School Hospital.
RAG involves opening the sylvian fissure and identifying the M2 segment that is suitable for RA–M2 anastomosis without perforating arteries or disturbing the arteriosclerotic changes. A rubber sheet was stretched under the M2 segment for preparation of the anastomosis, and the brain surface was carefully examined to include the M4–M5 segment and to identify blood vessels ≥1 mm in diameter for inclusion in the ICGVAG imaging range. Using a temporary clip, the recipient M2 was temporarily occluded, and ICGVAG (0.3 mg/kg) was performed to confirm that the recipient M4 segment was suitable for STA–MCA anastomosis [3,4,6,7,9]. 3. Results No ICG allergic reactions were observed in any of the cases, and ICG imaging was possible in all cases. In 2 of the 13 RAG cases, the M4 segment within the ICGVAG range on the brain surface covered the entire area and the relationship with the proximal M2 could not be ascertained. This may have occurred due to one or more of the following reasons: (1) temporary clipping occlusion was inadequate; (2) there was sufficient collateral circulation; or (3) the area of the occluded M2 segment was narrow and not within the range of the dural incision.
2. Methods
3.1. Representative cases
Aneurysmal surgical treatments in thirteen cases were performed using a Carl Zeiss Surgical Microscope OPMI Pentero INFRARED 800 (Carl Zeiss Co., Tokyo, Japan).
3.1.1. Case 1 In a 63-year-old female suffering double vision due to abducens nerve palsy, a giant aneurysm in the cavernous portion of the left internal carotid artery (ICA) (Fig. 2) was confirmed by cerebral angiography, which revealed a narrow posterior communicating artery (Pcom), hypoplasia of the right A1, and poor collateral circulation. RAG and ligation of the cervical internal carotid artery were performed.
2.1. Basic strategies of RAG Various treatment strategies adopted for complex carotid aneurysms include the following: revascularization using the
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Fig. 3. Left: Microscopic findings in the surgical field using the left trans-sylvian approach. Middle. ICGVAG image taken 9 s after ICG infusion. The M2 segment of the middle cerebral artery has been temporary clipped. Peripheral middle cerebral arteries on the temporal cortex were not enhanced (white arrow) and frontal cortex were enhanced (black arrow). Right An ICGVAG image was obtained 28 s after the ICG infusion showed the patency of the STA–MCA and ECA–RA–MCA anastomoses. The small white arrow indicates the superficial temporal artery, and the white arrowhead indicates the radial artery.
The cervical carotid artery was dissected, and the external carotid artery (ECA) was exposed to the bifurcation of the occipital artery. Following fronto-temporal craniotomy, a 24 F chest tube was inserted from the space between the 12th cranial nerve and the digastric muscle to the extracranial middle fossa under the temporal muscle [3,9]. The sylvian fissure was widely opened, exposing the M1 to the proximal M4 segment of the MCA. Based on the arteriosclerotic findings and the perforating branch, we selected the M2 segment believed to be appropriate for RA–M2 anastomosis. Thereafter, microscopic magnification and visual axis were configured so that the ICGVAG range would include the entire brain surface within the dural incision (Fig. 3, left). The M2 segment prepared for anastomosis was temporarily occluded using a Sugita No. 51 temporary clip followed by ICGVAG. The distal cortical MCA branch on the brain surface was identified without visualizing the temporal lobe (Fig. 3, middle). The STA (frontal branch) to M4 anastomosis on the temporal side of the MCA was performed (temporary occlusion time was 16 min). Next, the extracted RA was inserted into the chest tube passing from below the temporal muscle along the middle fossa through the space between the 12th cranial nerve and the digastric muscle. The RA–MCA anastomosis was performed (temporary occlusion duration, 38 min) and followed by the ECA–RA anastomosis. ICGVAG findings of the STA–MCA and ECA–RA–MCA anastomoses indicated patency in both bypasses (Fig. 3, right). Invasive blood pressure (BP) measurements using the STA parietal branch revealed an STA pressure of 110/64 mm Hg (systemic BP of 118/71 mm Hg). On occlusion of the proximal STA,
the systemic BP was 116/68 and the pressure in the cortical MCA was 92/57 mm Hg. When the cervical ICA was occluded using a bulldog clamp, the MCA pressure on the brain surface was 32/28 mm Hg, which increased to 76/48 mm Hg after opening the RAG. When the cortical MCA pressure from the RAG reached 80% of the normal flow from the ICA, it was deemed satisfactory. The patient recovered well with no postoperative neurological deterioration. Diffusion-weighted imaging (DWI) (Fig. 4, left) on postoperative day 2 revealed no new ischemic findings. Threedimensional computed tomographic (3D CT) angiography on day 8 identified the RAG and STA–MCA anastomosis (Fig. 4, right). 3.1.2. Case 2 A 67-year-old male presented with change in mental status caused by a left ICA anterior wall aneurysm (ICAW) (Fig. 5. upper left). Aneurysm trapping and RAG were performed. The surgical procedure was similar to that performed in case 1. The sylvian fissure was opened, and the microscopic magnification and visual axis were configured to visualize the range of the entire dural incision on the brain surface (Fig. 5, upper right). The M2 to RA–M2 anastomosis was temporarily occluded using a Sugita No. 51 temporary clip followed by ICGVAG. The entire cortical MCA on the brain surface within the opened dura was enhanced on ICGVAG (Fig. 5, lower left). Therefore, the distal cortical MCA branch on the brain surface was not identified. Subarachnoid hemorrhage (SAH) was irrigated on opening of the sylvian fissure to confirm the relationship between the distal cortical MCA and M2. Because the appropriate
Fig. 4. Left: Diffusion-weighted image on day 2 showing no abnormal ischemic findings on the surgical side. Right: Postoperative three-dimensional CT angiography demonstrating good patency of the STA–MCA (small arrow) anastomosis and ECA–RA–M2 bypass (large arrow).
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Fig. 5. Upper left: Preoperative oblique view of internal carotid artery three-dimensional angiography showing an internal carotid artery anterior wall aneurysm (white arrow). A posterior communicating artery and an anterior choroidal artery were branching from almost the same segment of the internal carotid artery. Upper right: Microscopic findings of the surgical field using the left trans-sylvian approach. Lower left: ICGVAG image taken 24 s after ICG infusion. The M2 segment of the middle cerebral artery has been temporary clipped. All cortical branches of the middle cerebral arteries were enhanced within the surgical field. Lower right: Postoperative three-dimensional CT angiography demonstrating good patency of the STA (small arrow)–MCA anastomosis and ECA–RA (large arrow)–M2 bypass.
distal cortical MCA branch could not be identified, the temporal M4 on the brain surface was selected for anastomosis to avoid complications related to excessive dissection of the sylvian fissure. Once all anastomoses had been completed, invasive blood pressure (BP) measurements using the STA parietal branch revealed an STA pressure of 92/54 mm Hg (systemic BP of 110/64 mm Hg). On occlusion of the proximal STA, the systemic BP was 108/68 mm Hg and the pressure in the cortical MCA was 84/48 mm Hg. When the cervical ICA was occluded using a bulldog clamp, the MCA pressure on the brain surface was 43/32 mm Hg, which increased to 64/38 mm Hg after opening the RAG. Invasive BP measurements were continued following occlusion of the proximal STA with a Sugita temporary clip no. 51. The ICAW was trapped using Yasargil aneurysm clips FT747T and FT750T (Aesculap, San Francisco, CA, USA). ICGVAG imaging revealed retrograde blood flow from the RAG and Pcom circulation. Immediately before suturing the dura and adherence of fibrin glue to the outside of the dura, direct measurement of arterial BP was continued for 96 min, during which time the MCA–BP on the surface of the brain increased to 79/60 mm Hg. DWI on postoperative day 4 revealed no new ischemic findings. 3D CT angiography on day 9 identified the RAG and STA–MCA anastomosis (Fig. 5. lower right). At 7 weeks after surgery, diffuse muscular weakness was the only symptom that required treatment, and the patient was transferred for rehabilitation. 4. Discussion Because there are few anatomical markers for the distal MCA, identifying the M2–M3 bifurcation is more difficult than identifying the circle of Willis [16,17]. We used TCI and a combination
of temporary clipping and ICGVAG to confirm the continuity of arteries. This study indicated that TCI may help reduce surgical time and avoid brain damage by reducing the size of the opening in the subarachnoid space. Although the 13 cases treated in our study represent a limited group, intraoperative findings, postoperative DWI–MRI, and postoperative magnetic resonance angiography revealed no complications associated with TCI. In the 2 cases that underwent RAG, a connection could not be confirmed between M2 (occluded by temporary clipping) and M4 within the range of the dural incision. 4.1. The significance of STA–MCA anastomosis in RAG Temporary occlusion requires more time with a RA–M2 anastomosis than with a STA–MCA anastomosis because of the deep surgical field and long suture line [1,9]. To avoid ischemia during the anastomosis and for the purpose of post-bypass monitoring, several reports [1,3,7,9] have recommended STA–MCA anastomosis. With respect to the recipient artery for the STA–MCA anastomosis, previous reports [1,3,7,9] have recommended performing the STA–M4 bypass as the “assisted bypass”, and we have used this method as well. We [7,9] believe that the following are the 3 main objectives of this method: (1) to maintain blood flow of the peripheral MCA when performing the RA–MCA anastomosis; (2) to monitor the adequacy of blood flow after completion of RAG; and (3) to supplement blood flow when the RA lumen is restricted. The STA–MCA bypass was first termed “assisted bypass” by Kamiyama et al. [1], who used it to maintain blood flow in the peripheral MCA when performing a RA–MCA anastomosis. Experience [7–9] gained from over 98 cases of RAG has led us to
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believe that the most important point during the STA–MCA bypass is to monitor the adequacy of blood flow after completion of all bypasses. Data obtained from invasive BP measurements of the MCA using the STA–MCA anastomosis are quantitative and can only confirm lack of blood flow from the RA intraoperatively. When the frontal branches of the STA are used for anastomosis, invasive BP measurements are performed on the parietal branch of the STAs. When the bifurcation of the frontal branch and parietal branch is located proximally, this method cannot be used. Therefore, to take post-RAG measurements in such cases, direct puncture or measurements using the small branch of the anastomosed STA is required. When the M1–M2 bifurcation is shallow or when the surgical field is wide in the M2 segment and prolonged occlusion time is not needed to perform the RA–M2 anastomosis, we select the M4 segment that is not the distal M2 segment used for the RA–M2 anastomosis to monitor the adequacy of blood flow post-RAG. This is because we believe that perfusion pressure is more accurate. In cases where both RA–M2 and STA–M4 anastomoses are performed on the same continuous artery and the anastomosis fails, the RA–M2 bypass flows only peripherally to M4 and perfusion pressure from the STA–MCA anastomosis does not reflect perfusion pressure in other M2 segments. Therefore, when the M1–M2 bifurcation is deep or when arteriosclerotic changes are present in the M2 segment and prolonged occlusion time is needed to perform the RA–M2 anastomosis, both RA–M2 and STA–M4 anastomoses should be performed on the same continuous artery, allowing for the appropriate recipient M4 segment to be selected based on the patient’s condition. In our study, a connection between M2 and M4 on the brain surface was confirmed in approximately 84.6% of RAG cases. Moreover, postoperative DWI revealed no ischemic complications, which is believed to be associated with the surgical procedure. We believe that this method is useful for rapid and simple verification of the connection between the proximal and distal blood vessels. However, depending on the number of M2 branches running along the M4, the connection may not always be apparent. To increase the success rate, we used a wider dural incision and utilized the corical perfusion measurement indocyanin green video angiography with Pentero FLOW 800 system [18] and Doppler flowmetry [19,20]. There is a possibility that that the narrow observational range with ICG imaging and the dural incision has an impact on the success rate. Therefore, we emphasize the importance of an adequate observation area with ICGVAG. Intraoperative ICG videoangiography with the Flow 800 system is helpful in detecting the effects on the vascular supply during the temporary occlusion of the proximal artery. There are some reports indicating that the Pentero Flow 800 system [18] increases the sensitivity of ICGVAG and improves the capability to detect changes in cerebral blood flow [18]. Additionally, Doppler flowmetry would be helpful to detect the effects on the vascular supply during the temporary occlusion of the proximal artery [19,20]. 4.2. Benefits of TCI We investigated the time for the dissection of the sylvian fissure before TCI technique from operative videos in seven cases. The time for the dissection of sylvian fissure to confirm the communication of M2 and the distal M4 was 22–43 min (mean 28 min), and in one case, continuity could not be confirmed because of a tortuous M3 segment. Using TCI, it would be possible to shorten this time. 5. Conclusions Of the 13 RAG cases in our study, TCI was useful in 11 cases, suggesting that unnecessary dissection in the subarachnoid space may be reduced.
The communication between blood vessels could not be clarified in 2 cases. In cases with developed collateral circulation, inadequate temporary clipping occlusion, or narrow circulation area of the occluded M2, it was difficult to ascertain the relationship between the parent artery and the distal/peripheral blood vessels by TCI. Utilization of Doppler flowmetry or the Pentero FLOW 800 system may increase the success rate. Disclosure The author reports no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. References [1] Kamiyama H. Bypass with radial artery graft. No Shinkei Geka 1994;22: 911–24. [2] Sekhar LN, Stimac D, Bakir A, Rak R. Reconstruction options for complex middle cerebral artery aneurysms. Neurosurgery 2005;56(1 (Suppl)):66–74. [3] Houkin K, Kamiyama H, Kuroda S, Ishikawa T, Takahashi A, Abe H. Long-term patency of radial artery graft bypass for reconstruction of the internal carotid artery. Technical note. J Neurosurg 1999;90:786–90. [4] Mizunari T, Murai Y, Kim K, Kobayashi S, Kamiyama H, Teramoto A. Posttraumatic carotid-cavernous fistulae treated by internal carotid artery trapping and high-flow bypass using a radial artery graft – two case reports. Neurol Med Chir (Tokyo) 2011;51:113–6. [5] Murai Y, Mizunari T, Umeoka K, Tateyama K, Kobayashi S, Teramoto A. Radial artery grafts for symptomatic cavernous carotid aneurysms in elderly patients. Neurol India 2011;59:537–41. [6] Murai Y, Mizunari T, Umeoka K, Tateyama K, Kobayashi S, Teramoto A. A simple technique to prevent and correct graft vessel kinking in the subcutaneous tunnel: technical note. Clin Neurol Neurosurg 2011;113:835–8. [7] Kubo Y, Ogasawara K, Tomitsuka N, Otawara Y, Kakino S, Ogawa A. Revascularization and parent artery occlusion for giant internal carotid artery aneurysms in the intracavernous portion using intraoperative monitoring of cerebral hemodynamics. Neurosurgery 2006;58:43–50. [8] Murai Y, Mizunari T, Umeoka K, Tateyama K, Kobayashi S, Teramoto A. Ischemic complications after radial artery grafting and aneurysmal trapping for ruptured internal carotid artery anterior wall aneurysm. World Neurosurg 2012;77:166–71. [9] Ishikawa T, Kamiyama H, Kobayashi N, Tanikawa R, Takizawa K, Kazumata K. Experience from “double-insurance bypass.” Surgical results and additional techniques to achieve complex aneurysm surgery in a safer manner. Surg Neurol 2005;63:485–90. [10] Murai Y, Adachi K, Takagi R, Koketsu K, Matano F, Teramoto A. Intraoperative Matas test using microscope-integrated intraoperative indocyanine green videoangiography with temporary unilateral occlusion of the A1 segment of the anterior cerebral artery. World Neurosurg 2011:76, 477.e7–10. [11] Murai Y, Adachi K, Matano F, Tateyama K, Teramoto A. Indocyanin green videoangiography study of hemangioblastomas. Can J Neurol Sci 2011;38: 41–7. [12] 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;52:132–9. [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;102:692–8. [14] Hacein-Bey L, Connolly Jr ES, Mayer SA, Young WL, Pile-Spellman J, Solomon RA. Complex intracranial aneurysms: combined operative and endovascular approaches. Neurosurgery 1998;43:1304–12. [15] Niiro M, Shimozuru T, Nakamura K, Kadota K, Kuratsu J. Long-term follow-up study of patients with cavernous sinus aneurysm treated by proximal occlusion. Neurol Med Chir (Tokyo) 2000;40:88–97. [16] Lee SH, Bang JS. Distal middle cerebral artery M4 aneurysm surgery using navigation-CT angiography. J Korean Neurosurg Soc 2007;42:478–80. [17] Schmid-Elsaesser R, Muacevic A, Holtmannspötter M, Uhl E, Steiger HJ. Neuronavigation based on CT angiography for surgery of intracranial aneurysms: primary experience with unruptured aneurysms. Minim Invasive Neurosurg 2003;46:269–77. [18] Holling M, Brokinkel B, Ewelt C, Fischer BR, Stummer W. Dynamic ICG fluorescence provides better intraoperative understanding of arteriovenous fistulae. Neurosurgery 2013;73(1 (Suppl)):ons93-99. [19] Stadie A, Fukui K, Schramm P, Werner C, Oertel J, Engelhard K, Fischer G. Measurement of cortical microcirculation during intracranial aneurysm surgery by combined laser-Doppler flowmetry and photospectrometry. Neurosurgery 2011;69:391–8. [20] Kawamata T, Kawashima A, Yamaguchi K, Hori T, Okada Y. Usefulness of intraoperative laser Doppler flowmetry and thermography to predict a risk of postoperative hyperperfusion after superficial temporal artery-middle cerebral artery bypass for moyamoya disease. Neurosurg Rev 2011;34:355–6.
