J Neurosurg 111:1158–1164, 2009 Clinical implications of intraoperative infrared brain surface monitoring during superficial temporal artery–middle cerebral artery anastomosis in patients with moyamoya disease Clinical article Atsuhiro Nakagawa, M.D., Ph.D.,1 Miki Fujimura, M.D., Ph.D.,1 Tatsuhiko Arafune, Ph.D., 2 Ichiro Sakuma, Ph.D., 2 and Teiji Tominaga, M.D., Ph.D.1 Department of Neurosurgery, Tohoku University Graduate School of Medicine, Sendai, Miyagi; and 2Bio-Medical Precision Engineering Laboratory, Institute of Environmental Studies, Graduate School of Frontier Sciences, The University of Tokyo, Japan 1 Object. Surgical revascularization for moyamoya disease prevents cerebral ischemic attacks by improving cerebral blood flow (CBF). Symptomatic cerebral hyperperfusion is a potential complication of this procedure, but its treatment is contradictory to that for ischemia. Because intraoperative techniques to detect hyperperfusion are still lacking, the authors performed intraoperative infrared monitoring in moyamoya disease using a novel infrared imaging system. Methods. During superficial temporal artery–middle cerebral artery anastomosis in 25 patients (26 hemispheres) with moyamoya disease, the authors monitored the brain surface temperature intraoperatively with the IRIS-V infrared imaging system. The average gradation value change (indicating temperature change) was calculated using commercial software. Magnetic resonance imaging, MR angiography, and N-isopropyl-p-[123I]iodoamphetamine SPECT studies were performed routinely before and within 10 days after surgery. Results. Patency of bypass, detailed local hemodynamics, and changes in cortical surface temperature around the anastomosis site were well recognized by the IRIS-V infrared imaging system in all cases. In the present study, 10 patients suffered transient neurological symptoms accompanied by an increase in CBF around the anastomosis site, recognized as symptomatic hyperperfusion. The increase in temperature was significantly higher in these patients. Intensive blood pressure control was undertaken, and free-radical scavengers were administered. No patient in the present study suffered a permanent neurological deficit. Conclusions. Although the present method does not directly monitor surface CBF, temperature rise around the anastomosis site during surgery might be an indicator of postoperative hyperperfusion. Prospective evaluation with a larger number of patients is necessary to validate this technique. (DOI: 10.3171/2009.4.JNS08585) Key Words • extracranial-intracranial bypass • thermal artery imaging • intraoperative monitoring • minimally invasive neurosurgery • neurocritical care M oyamoya disease is a chronic, occlusive cere- brovascular disease with unknown etiology and is characterized by bilateral stenoocclusive changes at the terminal portion of the internal carotid artery and an abnormal vascular network at the base of the brain.22 Surgical revascularization for moyamoya disease is believed to be beneficial to prevent cerebral ischemic attacks by improving CBF, and STA-MCA anastomosis with or without indirect bypass is generally used as Abbreviations used in this paper: CBF = cerebral blood flow; DW = diffusion weighted; EDMS = encephaloduromyosynangiosis; 123 I-IMP = N-isopropyl-p-[123I]iodoamphetamine; MCA = middle cerebral artery; ROI = region of interest; STA = superficial temporal artery; TIA = transient ischemic attack. 1158 the standard surgical treatment.11,12 On the other hand, several lines of evidence support that not only ischemia but symptomatic cerebral hyperperfusion is a potential complication of this procedure in the acute stage.5–8,16 Accurate and early diagnosis of postoperative hyperperfusion is important because its treatment is contradictory to that for ischemia. Because intraoperative techniques to estimate subsequent occurrence of symptomatic hyperperfusion are still lacking, we performed intraoperative infrared monitoring of the surface brain temperature by using a novel infrared imaging system in the hope that we can indirectly evaluate changes in surface CBF. We also evaluated the clinical impact of temperature change on occurrence of symptomatic hyperperfusion during the acute stage after revascularization. J Neurosurg / Volume 111 / December 2009 Intraoperative infrared brain surface monitoring in moyamoya disease Methods Between March 2005 and December 2006 at Tohoku University Hospital, we conducted intraoperative monitoring of brain surface blood flow by using the IRIS-V infrared imaging system (Sparkling Photon, Inc.) during STA-MCA anastomosis on 26 hemispheres in 25 patients with moyamoya disease (female/male ratio 16:9; age range 7–63 years, mean age 33.4 years). All patients met the criteria of the Research Committee on Spontaneous Occlusion of the Circle of Willis, of the Ministry of Health, Labor, and Welfare, Japan. Standard angiography was performed preoperatively in all adult patients and whenever possible in pediatric patients. All patients underwent STA-MCA anastomosis consisting of EDMS and dural pedicle insertion.20 During surgery the patients were kept normotensive with normocapnia and a rectal temperature of 36°C. The room temperature was maintained at 23°C to keep the background cortical surface temperature as constant as possible. After completion of anastomosis, the high-resolution infrared camera of the IRIS-V infrared imaging system was set 30 cm above the brain, and blood flow was continuously monitored for as long as 3 minutes, including time for placement and release of the temporary clip (Fig. 1). We used this method instead of monitoring before and after the surgical procedure because the cortical temperature before starting the surgical procedure would have been recorded long before completion of the bypass procedure, and thus might not have been as accurate as the baseline value because of temperature changes from the time of craniotomy until the end of the bypass procedure.17 The IRIS-V infrared imaging system is composed of 3 parts: a main computer, a camera head, and a display monitor. The size of the camera head is 14 × 16 × 19 cm. The camera is connected to the main computer part by folded 5-joint arms (maximum horizontal distance: 80 cm, possible vertical motorized distance 125–155 cm above floor) so that surgeons can bring the camera head over the operative field whenever necessary. The infrared focal plane array detector (barium strontium titanate, 320 × 240 pixels) shows an area of 110 × 82 mm using an F50 infrared lens. The detectable temperature is limited to 35 ± 10°C. Temperatures > 45°C are shown in black, whereas those < 25°C are shown in white and are presented as 8-bit black-and-white images in each pixel. The detectable wavelength band is 7–14 µm. No contrast medium or radiation was used to obtain the images. The recording speed was 30 frames/second. All of the images were stored in the installed computer and recorded with a digital video device. Obtained images were analyzed with imaging software by changes in gradation value.13,17,24 In addition, the ROI was set around the anastomosis site (diameter 100 pixels), and the average gradation value within the ROI was calculated by Matrox Inspector software (version 8.0, Matrox Electronics Systems, Ltd.). Probability values < 0.05 were considered to be statistically significant. In all cases, preoperative CBF was measured using 123 I-IMP-SPECT. The 123I-IMP-SPECT studies were routinely performed before surgery and 1 and 7 days after J Neurosurg / Volume 111 / December 2009 surgery in all cases. Before surgery and within 10 days of surgery, 1.5-T MR imaging and MR angiography were routinely performed. Standard angiography was not performed postoperatively.6 The MR imaging studies included DW images, FLAIR images, T1- and T2-weighted images, and T2*-weighted images. Results Patency of bypass could be evaluated in all cases attempted, and it was also confirmed by conventional Doppler ultrasonography during the operation and by postoperative MR angiography during the follow-up period. Information regarding local hemodynamics, which includes flow direction and distribution, could also be evaluated in all cases by the IRIS-V infrared imaging system throughout the craniotomy. Among the 25 patients who underwent 26 surgeries, 10 suffered transient postoperative neurological deterioration. These patients exhibited an intense increase in CBF around the anastomosis site as detected by 123I-IMP-SPECT and a thick STA on MR angiography.5–7 Intensive blood pressure control with administration of oxygen radical scavengers was performed, and no patient suffered permanent neurological deterioration compared with his or her preoperative neurological status. Transient ischemic attacks disappeared or improved in all cases during the follow-up period. Case 1 Representative Cases Presentation. This 54-year-old man presented with frequent TIAs (transient weakness in the left extremity). Stage III moyamoya disease was identified, and 123I-IMPSPECT showed that his right CBF and cerebrovascular reserve capacities were markedly impaired. Therefore, STA-MCA anastomosis with EDMS was performed in the right hemisphere. Operation. After exploration of the parietal branch of the right STA, a frontotemporoparietal craniotomy was performed. The recipient artery at the M4 segment of the anterior parietal branch of the MCA was explored, and anastomosis was performed between the stump of the STA (2.0 mm in diameter) and the M4 segment (1.0 mm in diameter). Then, EDMS and dural pedicle insertion were performed. Intraoperative infrared monitoring disclosed changes in the color of the bypass to white after the temporary occlusion (indicating decrease in temperature) (Fig. 2 upper left), and then a change to black (indicating increase in temperature) 2 seconds after removal of the clip (Fig. 2 lower left), indicating presence of blood flow and patency of the bypass. During the color change, the cooled blood was shown to be pushed away toward the cranial artery, in both proximal and distal directions of the M4 segment at 1.00 second (Fig. 2 upper right), indicating the presence of a perfusion pressure gradient (Fig. 2 upper right). The patency of the bypass was also confirmed by intraoperative Doppler ultrasonography. The color of the exposed brain around the anastomosis site did 1159 A. Nakagawa et al. Fig. 1. Photograph of the IRIS-V infrared imaging system in the operating theater.   Inset: The infrared and charge-coupled device camera. not show significant change before and after removal of the temporary clip (Fig. 2). The change in average gradation value within the ROI was within 5 points, indicating no significant increase in temperature after release of the temporary clip (Fig. 3). Postoperative Course. The patient’s postoperative course was uneventful. Patency of the bypass was also confirmed by MR angiography. The 123I-IMP-SPECT studies performed 1 and 7 days after surgery showed a slight increase in CBF in the right hemisphere compared with the preoperative findings. Postoperative DW MR imaging showed no evidence of ischemic change, and MR angiography demonstrated the apparently patent STAMCA bypass as a higher intensity signal than the opposite side STA. The patient did not experience neurological deterioration during the follow-up period. Case 2 Presentation. This 26-year-old woman presented with a TIA (transient weakness in the left upper extremity). Stage III moyamoya disease was identified, and 123IIMP-SPECT showed that her bilateral CBF and cerebrovascular reserve capacities were markedly impaired. Therefore, bilateral bypass surgery was planned. Operation. An STA-MCA anastomosis with EDMS was performed in the right hemisphere. After exploration of the parietal branch of the right STA, a frontotemporoparietal craniotomy was performed. The recipient artery at the M4 segment of the anterior parietal branch of the MCA was explored, and anastomosis was performed between the stump of the STA (1.0 mm in diameter) and the M4 segment (0.8 mm in diameter). Then an EDMS procedure and dural pedicle insertion were performed. Intraoperative infrared monitoring disclosed changes in the color of the bypass to white after the temporary occlusion (indicating a decrease in temperature) (Fig. 4 upper left), and a change to black (indicating an increase in temperature) after removal of the clip, indicating presence of 1160 Fig. 2. Case 1. Microscopic views of the surgical field around the anastomosis (inset, upper left) and intraoperative infrared monitoring showing changes in color of the STA (arrows) to white after temporary occlusion, indicating decrease in temperature (upper left) due to the absence of blood flow. Right after removal of the clip at 1 second, the color of the bypass transiently changed to white by cooled blood flow (upper right, arrowheads) and then changed to black (indicating an increase in temperature) at 2 seconds (lower left), indicating patency of the bypass. Note that the brain surface color around the anastomosis site (circle, lower right) did not significantly change throughout the process. F = frontal lobe; P = parietal lobe; T = temporal lobe; TC = temporary clip. blood flow and patency of the bypass (Fig. 4 upper right and lower left). Patency of the bypass was also confirmed by intraoperative Doppler ultrasonography. The images also disclosed that the color of the brain surface around the anastomosis changed significantly to black after removal of the temporary clip until the end of monitoring (Fig. 4 lower right). The change of average gradation value within the ROI increased 15–20 points, indicating a significant increase of temperature after release of the temporary clip (Fig. 5). Operation. The patient showed no evidence of neu- Fig. 3. Graph showing the relationship between time after removal of the temporary clip and changes of the average gradation value within the ROI around the anastomosis site as evaluated using imaging software in Case 1. The increase of gradation value after removal of the temporary clip was within 5 points, indicating no significant change in surface temperature. J Neurosurg / Volume 111 / December 2009 Intraoperative infrared brain surface monitoring in moyamoya disease Fig. 4. Case 2. Images obtained during intraoperative infrared monitoring disclosing changes in color in the color in the STA (arrows) to white after temporary occlusion (indicating decrease in temperature; upper left) due to the absence of blood flow. Immediately after removal of clip at 1 second, the color of the bypass changes to black (upper right), indicating the presence of blood flow. The area is even darker after 4 seconds (lower left). Note that the color of the brain surface around the anastomosis site (circle, lower right) gradually changes to black (indicating an increase in temperature). rological deficit immediately after surgery. The 123I-IMPSPECT studies obtained 1 day after surgery showed a slight increase in CBF in the right hemisphere (Fig. 6 center) compared with the preoperative findings (Fig. 6 upper). Postoperative DW MR imaging showed no evidence of ischemic change, and MR angiography demonstrated the apparently patent STA-MCA bypass as a higher intensity signal than the contralateral STA (Fig. 7 arrowhead). One day later, she suffered from fluctuating dysarthria, left facial palsy, and numbness in the left upper limb. A 123 I-IMP-SPECT study showed a focal intense increase in CBF at the site of anastomosis 7 days after surgery (Fig. 7 lower). A diagnosis of hyperperfusion was thus made based on neurological symptoms along with 123I-IMP Fig. 5. Graph showing the relationship between time after removal of the temporary clip and changes in average gradation value within the ROI around the anastomosis site as evaluated by imaging software in Case 2. There was a significant rise of gradation value after removal of the temporary clip, indicating significant change in surface temperature. J Neurosurg / Volume 111 / December 2009 Fig. 6. The 123I-IMP-SPECT studies obtained preoperatively (upper), 1 day after surgery (center) and 8 days after surgery (lower). Note the focal intense increase in the CBF at the site of anastomosis (arrowheads in lower). SPECT and MR angiography findings. Intensive blood pressure control and the use of a free radical scavenger relieved her symptoms, which completely disappeared 13 days after surgery, at which time she was discharged from the hospital without neurological deficit. We performed second-stage surgery on the left side 1 month later. Postoperative Course. She was discharged uneventfully after successful left STA-MCA anastomosis and EDMS, which resulted in disappearance of her ischemic attacks as well as a significant improvement in CBF on the bilateral cerebral hemisphere. She did not exhibit neurological deterioration during the follow-up period. Neurological Deterioration In all, 10 patients suffered from transient postoperative neurological deterioration, which were proved to be due to hyperperfusion in the present series. The aver1161 A. Nakagawa et al. Fig. 8. Graph showing the differences in average gradation value within the ROI around the anastomosis site among 10 patients who had transient neurological deficits due to focal increase of CBF around the anastomosis site and 16 patients who did not, showing significant increase in gradation value (indirectly showing significant increase in surface cortical temperature) in the former group (up to 60 seconds after removal of the temporary clip). * p < 0.05; ** p < 0.05. Fig. 7. Upper Left: Preoperative MR angiogram. Upper Right: Preoperative FLAIR study. Lower Left: Postoperative MR angiogram showing the apparently patent STA-MCA bypass (arrowheads). Lower Right: Postoperative FLAIR study showing high intensity signal around the site of anastomosis. age gradation value change (representing temperature) was significantly higher in the patients who experienced symptomatic hyperperfusion (Fig. 8) immediately after and up to 60 seconds following removal of the temporary clip. Discussion In the present study, our novel infrared imaging system allowed us not only successful monitoring of the bypass patency and comprehensive visual evaluation of local hemodynamics, but also for the first time, it showed the possibility of estimating the risk of subsequent occurrence of postoperative symptomatic hyperperfusion by temperature rise around the anastomosis site during the operation. Importance of Estimating Risk of Postoperative Symptomatic Hyperperfusion in Patients With Moyamoya Disease Occurrence of transient postoperative neurological deficits due to hyperperfusion has been recently recognized as an important potential complication after revascularization surgery for moyamoya disease.5–8,16 It is important to recognize the pathology because strict control of blood pressure is mandatory in patients with hyperperfusion, whereas such treatment is contradictory to that in patients with ischemic episodes.5–7 In addition, from 1162 the viewpoint of cognitive functional impairment, the occurrence of hyperperfusion cannot be ignored.16 The rate of hyperperfusion in the present series was higher than that reported in the series dealing with STA-MCA anastomosis in chronic cerebral ischemia. Postoperative cerebral hyperperfusion syndrome has been considered to be less common in patients with moyamoya disease because of the relatively low-flow revascularization obtained through surgery for moyamoya disease. In our previous study involving 34 consecutive cases of moyamoya disease, we reported that STA-MCA anastomosis in patients with adult-onset moyamoya disease can result in a substantial rate (13 [38.2%] of 34) of temporary neurological deterioration due to transient focal intense increases in CBF at the site of anastomosis and that intensive blood pressure control can relieve this condition.5 However, the clinical manifestation is different from hyperperfusion syndrome after carotid endarterectomy; radical clinical presentation succeeding intracranial hemorrhage was observed in 1 case, but the majority were limited to subtle, transient focal neurological deficits mimicking ischemic attack, with no patient suffering a permanent neurological deficit. Identification of the predictors for cerebral hyperperfusion in patients with moyamoya disease is clinically important. Preoperative cerebrovascular reserve capacity, severity of ischemia during surgery, patients age, and anatomical vascular structures around the site of the anastomosis may affect postoperative cerebral hyperperfusion.5–8,10,16,19,25 In our study, most patients showed a preoperative cerebrovascular reserve capacity of < 0% (steal phenomenon), which may contribute to the high incidence of postoperative symptomatic hyperperfusion. Regarding intraoperative ischemic insult during anas­tomosis, which may facilitate postischemic hyperperfusion, most of the cases were subjected to temporary J Neurosurg / Volume 111 / December 2009 Intraoperative infrared brain surface monitoring in moyamoya disease occlusion (30 minutes) at the distal M4 segment. It is not clear how a rapid increase in CBF affects the ischemic brain in moyamoya disease, although a substantial number of patients may suffer transient neurological deterioration due to an unknown mechanism. As shown in the present study, the mean gradation value around the anastomosis site obtained from an infrared image showed a significant increase in temperature lasting up to 60 seconds in patients who suffer symptomatic hyperperfusion. According to the calibrated data from the manufacturer, the IRIS-V system demonstrates 20° of temperature difference between 25 and 45°C by 8-bit, or 256 gradation values. Therefore, a 1-point difference in gradation value is equivalent to 0.08°C. In the present study, the temperature difference between the 2 groups was calculated to be 0.28°C at 10 seconds, 0.42°C at 30 seconds, 0.41°C at 60 seconds, and 0.77°C at 90 seconds after removal of the temporary clip. However, whether this temperature increase is benign or a sign of abnormal overflow of CBF into a previously poorly perfused area, or merely a reaction unrelated to the postoperative phenomenon, is still uncertain. Even if it is a sign of abnormal overflow, the threshold remains unknown. Both issues are limitations of the present study and should be evaluated prospectively, and for a longer time after removal of the temporary clip. In light of the fact that STA-MCA anastomosis could result in postoperative symptomatic hyperperfusion in childhood7 as well as in adult-onset moyamoya disease,6 it is worth further studying the relationship between the pattern of intraoperative cerebral hemodynamics and postoperative neurological status. Clinical Implications of Intraoperative Infrared Imaging Infrared imaging is an established technique for studying the surface temperature of human organs.18,23 In the past, this technique has been applied in coronary artery bypass graft surgery to measure the cooling effect of cardioplegic solutions, or to evaluate coronary perfusion and graft patency.1,3,4 With advances in infrared technology, including detective wavelength, detective temperature range, cooling system, and filters, as well as data processing, it is now possible to observe surface blood flow with high spatial and time resolution without contact with blood vessels, radiation exposure, or injection of contrast medium.21 The relationship of infrared camera thermography and quantitative blood flow has been extensively investigated in the heart. Experimental cardiac studies demonstrated a quantitative correlation between blood flow and myocardial temperature.1,3 In the isolated pig heart, in which there is no metabolic contribution to temperature change, graft flow was found to correlate highly with a mathematical expression of the temperature change observed during thermography.3 In the brain literature, Watson et al.24 applied high-resolution infrared imaging to the brain of Cynomolgus monkeys and reported that the cortical arterial temperature was related to blood flow and the temporal temperature profile was identical to that of blood flow measured by Doppler ultrasonography. Moreover, a recent study by Okada et al.17 showed linear relationships between cortical surface CBF and J Neurosurg / Volume 111 / December 2009 temperature that were confirmed using a laser Doppler flowmeter. It is considered that cortical brain temperature is determined by metabolism and blood flow coupling2,9 and sensitive infrared imaging might be a useful measure provided that there is no significant metabolism change during monitoring.24 Therefore, the increase in temperature around the anastomosis site in the present study was considered to be due to an increase in blood flow. The IRIS-V is a new-generation infrared system with higher resolution at minimal temperature differences. In addition, by shifting the sensitive wavelength band up to 7–14 µm from 3–5 µm, it is possible to detect infrared rays from near the surface region. Using a previous prototype, we have evaluated patency of bypass in beagles (vessel diameter as small as 0.5 mm), and we have also reported that flow territory can be delineated by temperature difference.14 Infrared monitoring has also been useful for confirmation of venous drainage during surgical obliteration of a spinal perimedullary arteriovenous malformation.15 Including the novel infrared system presented in this report, future infrared monitoring will not only serve for intraoperative monitoring but may become a useful tool for estimation of postoperative risks, although further examination is necessary. Conclusions Temperature rise around an anastomosis site above a certain threshold during surgery as detected by intraoperative infrared monitoring might indicate the subsequent occurrence of postoperative symptomatic hyperperfusion. Prospective evaluation with a larger number of patients is necessary to validate this technique. Disclosure This work was supported in part by a Grant-in-Aid for Scientific Research (B) (No. 18390388) (T.T.) and (No. 19399372) (A.N.); a Grant-in-Aid for Young Scientists (A) (No. 19689028) (A.N.) offered by the Japanese Ministry of Education, Culture, Sports, Science, and Technology; Mitsubishi Pharma Research Foundation (T.T.); and the Exploratory Research Program for Young Scientists (ERYs) from Tohoku University (A.N.). The authors report no other conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Acknowledgments The authors thank Hideaki Suzuki, M.D., of Tohoku University Hospital, Etsuko Kobayashi, Ph.D., Takahiro Yamaguchi, Ph.D., and Teruko Sakurai of Bio-Medical Precision, Engineering Laboratory, Institute of Environmental Studies, Graduate School of Frontier Sciences, the University of Tokyo, Japan, for analysis of the infrared imaging. References 1. Adachi H, Becker LC, Ambrosio G, Takeda K, Dipaula AF, Baumgartner WA, et al: Assessment of myocardial blood flow by real-time infrared imaging. J Surg Res 43:94–102, 1987 2. Ecker RD, Goerss SJ, Meyer FB, Cohen-Gadol AA, Britton JW, Levine JA: Vision of the future: initial experience with intraoperative real-time high-resolution dynamic infrared imaging. Technical note. J Neurosurg 97:1460–1471, 2002 1163 A. Nakagawa et al. 3. Falk V, Walther T, Kitzinger H, Rauch T, Diegeler A, Autschbach R, et al: An experimental approach to quantitative thermal coronary angiography. Thorac Cardiovasc Surg 46:25– 27, 1998 4. Falk V, Walther T, Philippi A, Autschbach R, Krieger H, Dalichau H, et al: Thermal coronary angiography for intraoperative patency control of arterial and saphenous vein coronary artery bypass grafts: results in 370 patients. J Card Surg 10:147–160, 1995 5. Fujimura M, Kaneta T, Mugikura S, Shimizu H, Tominaga T: Temporary neurologic deterioration due to cerebral hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in patients with adult-onset moyamoya disease. Surg Neurol 67:273–282, 2007 6. Fujimura M, Kaneta T, Shimizu H, Tominaga T: Symptomatic hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in a child with moyamoya disease. Childs Nerv Syst 23:1195–1198, 2007 7. Fujimura M, Mugikura S, Shimizu H, Tominaga T: [Diagnostic value of perfusion-weighted MRI for evaluating postoperative alteration of cerebral hemodynamics following STAMCA anastomosis in patients with moyamoya disease.] No Shinkei Geka 34:801–809, 2006 (Jpn) 8. Furuya K, Kawahara N, Morita A, Momose T, Aoki S, Kirino T: Focal hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in a patient with moyamoya disease. Case report. J Neurosurg 100:128–132, 2004 9. Gorbach AM, Heiss J, Kufta C, Sato S, Fedio P, Kammerer WA, et al: Intraoperative infrared functional imaging of human brain. Ann Neurol 54:297–309, 2003 10. Houkin K, Ishikawa T, Yoshimoto T, Abe H: Direct and indirect revascularization for moyamoya disease: surgical techniques and peri-operative complications. Clin Neurol Neurosurg 99 (Suppl 2):S142–S145, 1997 11. Ishikawa T, Houkin K, Kamiyama H, Abe H: Effects of surgical revascularization on outcome of patients with pediatric moyamoya disease. Stroke 28:1170–1173, 1997 12. Karasawa J, Kikuchi H, Furuse S, Kawamura J, Sakaki T: Treatment of moyamoya disease with STA-MCA anastomosis. J Neurosurg 49:679–688, 1978 13. Nakagawa A, Fujimura M, Ohki T, Suzuki H, Takayama K, Tominaga T: [Intraoperative brain surface blood flow monitoring using IRIS V thermographic imaging system in patients with Moyamoya disease.] No Shinkei Geka 34:1017–1025, 2006 (Jpn) 14. Nakagawa A, Hirano T, Uenohara H, Sato M, Kusaka Y, Shirane R, et al: Intraoperative thermal artery imaging of an EC-IC bypass in beagles with infrared camera with detectable wave-length band of 7-14 micron: possibilities as novel blood flow monitoring system. Minim Invasive Neurosurg 46:231–234, 2003 15. Nakagawa A, Hirano T, Uenohara H, Utsunomiya H, Suzuki S, Takayama K, et al: Use of intraoperative dynamic infrared imaging with detection wavelength of 7-14 micron in the sur- 1164 gical obliteration of spinal arteriovenous fistula: case report and technical considerations. Minim Invasive Neurosurg 47:136–139, 2004 16. Ogasawara K, Komoribayashi N, Kobayashi M, Fukuda T, Inoue T, Yamadate K, et al: Neural damage caused by cerebral hyperperfusion after arterial bypass surgery in a patient with moyamoya disease: case report. Neurosurgery 56:E1380, 2005 17. Okada Y, Kawamata T, Kawashima A, Hori T: Intraoperative application of thermography in extracranial-intracranial bypass surgery. Neurosurgery 60:362–366, 2007 18. Petibois C, Drogat B, Bikfalvi A, Deleris G, Moenner M: Chemical mapping of tumor progression by FT-IR imaging: towards molecular histopathology. Trends Biotechnol 24: 455–462, 2006 19. Sakamoto T, Kawaguchi M, Kurehara K, Kitaguchi K, Furuya H, Karasawa J: Risk factors for neurologic deterioration after revascularization surgery in patients with moyamoya disease. Anesth Analg 85:1060–1065, 1997 20. Shirane R, Yoshida Y, Takahashi T, Yoshimoto T: Assessment of encephalo-galeo-myo-synangiosis with dural pedicle insertion in childhood moyamoya disease: characteristics of cerebral blood flow and oxygen metabolism. Clin Neurol Neurosurg 99 (Suppl 2):S79–S85, 1997 21. Suma H, Isomura T, Horii T, Sato T: Intraoperative coronary artery imaging with infrared camera in off-pump CABG. Ann Thorac Surg 70:1741–1742, 2000 22. Suzuki J, Takaku A: Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288–299, 1969 23. Ueda M, Sakurai T, Kasai K, Ushikubo Y, Samejima H: Localisation of sensory motor cortex during surgery by changes of cortical surface temperature after median nerve stimulation. Lancet 350:561, 1997 24. Watson JC, Gorbach AM, Pluta RM, Rak R, Heiss JD, Oldfield EH: Real-time detection of vascular occlusion and reperfusion of the brain during surgery by using infrared imaging. J Neurosurg 96:918–923, 2002 25. Yoshimoto T, Houkin K, Kuroda S, Abe H, Kashiwaba T: Low cerebral blood flow and perfusion reserve induce hyperperfusion after surgical revascularization: case reports and analysis of cerebral hemodynamics. Surg Neurol 48:132–138, 1997 Manuscript submitted February 12, 2008. Accepted April 3, 2009. Please include this information when citing this paper: published online May 8, 2009; DOI: 10.3171/2009.4.JNS08585. Address correspondence to: Atsuhiro Nakagawa, M.D., De­part­ ment of Neurosurgery, Tohoku University Graduate School of Med­ icine, 1-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi 980-8574, Japan. email: nakg_neurosurg@yahoo.co.jp. J Neurosurg / Volume 111 / December 2009