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Intraoperative cerebral angiography in arteriovenous malformation resection in children: a single institutional experience Clinical article Marian Gaballah, B.S.,1 Phillip B. Storm, M.D., 3 Deborah Rabinowitz, M.D., 5 Rebecca N. Ichord, M.D., 2 Robert W. Hurst, M.D., 4 Ganesh Krishnamurthy, M.D.,1 Marc S. Keller, M.D.,1 Adeka McIntosh, M.D.,1 and Anne Marie Cahill, M.B.B.Ch.1 Departments of 1Radiology, 2Neurology and Pediatrics, and 3Neurosurgery, Children’s Hospital of Philadelphia; Departments of 4Radiology, Neurosurgery, and Neurology, Hospital of the University of Pennsylvania, Philadelphia, Pennsylvania; 5Department of Radiology, Nemours/Alfred I. duPont Hospital for Children, Wilmington, Delaware Object. The use of cerebral intraoperative angiography has been described in resection of arteriovenous malformations (AVMs) in adults. More recently, studies have described experiences with intraoperative angiography in a small number of children. However, data on the safety and clinical utility of intraoperative angiography in the pediatric population remains limited in comparison with available data in adults. The aim of the study was to evaluate the use of cerebral intraoperative angiography in children undergoing AVM resection. The clinical utility of intraoperative angiography and procedure-related complications were evaluated. Methods. A retrospective review was performed for all patients undergoing cerebral AVM resection with intraoperative angiography at The Children’s Hospital of Philadelphia between 2008 and 2012. Patient imaging and operative and medical notes were reviewed to evaluate for end points of the study. A total of 17 patients (8 males, 9 females) were identified, with a median age of 12.1 years (range 1.2–17.9 years) and median weight of 45.5 kg (range 12.1–78.9 kg). Results. A total of 21 intraoperative angiography procedures were performed for 18 AVM resections in 17 patients. The technical success rate was 94%. In 2 cases (11%), intraoperative angiography demonstrated a residual AVM, and repeat resections were performed. In both cases, no recurrent disease was noted on postoperative followup. One procedure-related complication (4.8%) occurred in 1 patient who was positioned prone. Recurrence to date was noted in 2 (14%) of the 14 cases with available postoperative follow-up at 3.5 and 4.7 months following resection with intraoperative angiography. The median follow-up time from intraoperative angiography to the most recent postoperative angiography was 1.1 years (range 4.3 months to 3.8 years). Conclusions. Intraoperative angiography is an effective and safe adjunct for surgical management of cerebral AVMs in the pediatric population. (http://thejns.org/doi/abs/10.3171/2013.10.PEDS13291)

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Key Words      •      arteriovenous malformation     •      vascular disorders     •      intraoperative angiography      •    pediatric     •    neurosurgery

arteriovenous malformations (AVMs) are uncommon vascular lesions in children, and differ pathologically from those occurring in adults.2,10 The exact prevalence and origin of pediatric cerebral AVMs remain unknown. While pediatric AVMs are presumed to occur during embryological development, only 18%–20% present before 15–20 years of age,6,18,29 with the majority remaining asymptomatic until 20–40 years of age, when they present with hemorrhage or seizures.2,29,40 The risk of hemorrhage in children has been reported to be 3.2% per year29 with 50%–80% of symperebral

Abbreviations used in this paper: AVM = arteriovenous malformation; DAP = dose-area product.

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tomatic AVMs in children presenting as hemorrhage.18,29 Resulting mortality from hemorrhage occurs at a rate of 20%–25% in children,18,24,29 which is higher than rates observed in adults,6,18,31 potentially due to varying locations of AVMs and more severe hemorrhage in children compared with adults.24 Treatment of AVMs includes complete elimination of the arterial nidus while attempting to preserve normal vasculature,12 and can be accomplished with resection or radiosurgery, either of which may be combined with endovascular embolization to make surgery more effective.26 This article contains some figures that are displayed in color on­line but in black-and-white in the print edition.

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Intraoperative cerebral angiography in AVM resection in children The goal of neurosurgery for AVMs is complete excision of the lesion while preserving adjacent brain parenchyma.14,37 Postoperative angiography was described by Allcock and Drake as early as 1963 to confirm successful surgical management of intracranial vascular lesions,3 because partially resected AVMs have an increased risk of hemorrhage in comparison with untreated AVMs.30 However, intraoperative angiography allows assessment of the surgical vascular bed, facilitating modification of surgical technique prior to cranial closure in cases of incomplete lesion resection, potentially eliminating the need for repeat craniotomy and surgery.37,39 Intraoperative angiography was first described in 3 case reports by Loop and Foltz in 1966, and the first large adult study was described by Grossart and Turner in 1973.15,27 Ghosh et al. published the first experience describing the use of intraoperative angiography in the pediatric population in 1998,14 and more recently, Ellis et al. demonstrated the safety and feasibility of the technique in children.12 Lastly, Lang et al. demonstrated the utility of intraoperative angiography in detecting residual AVMs in children by reporting equal recurrence rates for resected AVMs imaged using intraoperative angiography and those imaged with postoperative angiography.26 However, data on the safety and clinical utility of intraoperative angiography in the pediatric population remains limited in comparison with published data in adults. Prior to the availability of intraoperative angiography at our institution, the imaging protocol included a diagnostic cerebral angiogram on the first postoperative day, followed by additional surgery if required. Currently, intraoperative angiography has replaced early postoperative angiography (within 24 hours) as the standard of care at our institution, with the first postoperative angiography now performed at 3 months following resection. This study is a single-institution retrospective consecutive cohort study describing the technique of intraoperative angiography in children, and evaluating diagnostic utility, procedure-related complications, and the effect of intraoperative angiography on surgical management. Patient Population

Methods

Following approval by the institutional review board of the Children’s Hospital of Philadelphia, a retrospective review of the interventional radiology database was performed to identify all children who met the following inclusion criteria: diagnosis of cerebral AVM, which underwent resection; use of intraoperative angiography during AVM resection at our institution. The interventional radiology database includes all interventional procedures performed. A query of the database demonstrated the earliest intraoperative angiography to have been performed in January of 2008. Therefore all intraoperative angiographies performed between January 2008 and December of 2012 were included. Medical records were reviewed for all patients to confirm presence of a preoperative cerebral angiogram performed at our institution. Electronic medical and radiological records were reviewed for relevant clinical and procedural data.

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Angiographic Technique

All procedures were performed on patients under general anesthesia in the operating room. Patients were placed supine and prepared and draped in standard fashion. Using ultrasound guidance, the common femoral artery was accessed using a 21-gauge single-wall needle. A 4.0-Fr or 5.0-Fr vascular sheath was placed, sutured in position, and secured with a sterile occlusive dressing during the neurosurgical procedure. A continuous low-dose heparin infusion (2 units/ml) was administered through the sheath at a rate of 2–4 ml/hour to maintain sheath and arterial patency. Patients then remained supine or were placed prone for the neurosurgical procedure, depending on the location of the neurovascular lesion. For patients placed in a prone intraoperative position, the short sheath was secured in a similar fashion. Following the neurosurgical procedure, the vascular sheath was accessed using a sterile technique, and a 4- or 5-Fr, Berenstein, JB1, or Harwood-Nash catheter (Cook Medical Inc.) was used for cerebral angiography depending on operator preference. Accessing the sheath in the prone position is challenging with a short sheath and our current practice modification is to use a long sheath (25 cm) and secure it to the side of the patient’s thigh. Single or two-vessel digital subtraction angiography was performed via hand injection using nonionic contrast media (Omni­ paque 300, GE Healthcare) on a portable C-arm system with angiographic capability (Philips Medical Systems or GE Healthcare). Images were immediately interpreted by the radiologist and reviewed with the neurosurgeon. Positive findings on intraoperative angiography following initial neurosurgical intervention included a residual arterial nidus, an early draining vein, or early visualization of the venous sinus, and allowed for modification of surgical technique. Repeat intraoperative angiography was performed following any additional neurosurgical intervention, and dural closure was completed following a negative intraoperative angiogram. The femoral sheath was removed using standard manual hemostatic techniques. Resection was terminated when the surgeon believed the AVM nidus was completely resected and confirmation was achieved with intraoperative angiography. In lesions located in eloquent brain areas, the surgical approach was less aggressive and more dependent on the result of the intraoperative angiography.

Patient Follow-Up

Children were followed with postoperative angiography at 3-month, 1-year, and 5-year intervals following surgical management. For each patient, images from postoperative angiography were compared with those of intraoperative angiography to evaluate for accuracy of the intraoperative angiogram. Four patients had not yet received postoperative angiography at the completion of the study. For patients demonstrating an AVM on postoperative angiography, intraoperative images were reviewed to evaluate for residual disease to differentiate recurrent versus residual AVM on follow-up. Images were reviewed twice, first via 2-reader consensus, and then re-reviewed via 4-reader consensus to confirm the findings on intraoperative angiography. 223

M. Gaballah et al. Statistical Analysis

Comparison of dose-area product (DAP) and fluoroscopy times between intraoperative and postoperative angiography was performed using the Mann-Whitney Utest. Statistical significance was determined at p ≤ 0.05.

Results Patient Characteristics

Seventeen patients met eligibility criteria and were included in the analysis of intraoperative angiography. Patient demographics and clinical features are shown in Table 1. Among the patients managed with intraoperative angiography, symptomatic hemorrhage was the most common presentation, and headache in the absence of hemorrhage was the second most common presentation. One patient presented with asymptomatic papilledema diagnosed during a routine eye examination, and 1 patient presented with increased head circumference and bulging fontanelles accompanied by vomiting and seizures from increased intracranial pressure. Three AVMs were recurrent from a previous resection and therefore presented asymptomatically on routine follow-up imaging, while the fourth asymptomatic AVM was an incidental finding on imaging following head

trauma. One child requiring a second resection of a recurrent AVM also required intraoperative angiography, and therefore underwent two intraoperative angiography sessions. All patients underwent pretreatment angiography, and their vascular anatomy is described in Table 1. Treatment

Fourteen embolizations were performed preoperatively in 12 patients, with 2 patients receiving staged embolizations prior to surgery. In the 7 patients presenting with symptomatic hemorrhage, the median length of time from presentation to diagnostic angiography was 3 days (range 1–4 days), and the median length of time from presentation to surgical management was 3.9 months (range 5 days to 25.2 months). Twenty-one successful intraoperative angiography procedures were performed in 17 children during 18 neurosurgical procedures. In 15 procedures, patients were supine, while in 3 they were prone. The technical success rate was 94%. One angiogram could not be completed due to a left vertebral artery dissection that occurred in 1 prone patient. Median fluoroscopy time for the 18 cases was 6.7 minutes (range 0.9–17.1 minutes), with 5 unknown values. Median DAP was 0.54 mGy-m2 (range 0.2–1.8 mGy-m2; Table 2), with 12 unknown values. Data for fluoroscopy time and DAP were not available for ear-

TABLE 1: Patient demographics Variable demographics   male sex (%)   median age in yrs (range)   median patient weight in kg (range) clinical presentation   symptomatic acute intracranial hemorrhage   other neurological symptoms, w/o hemorrhage    headache, new acute or recurrent   seizures    papilledema on routine eye exam w/o headache    bulging fontanelle w/ emesis & seizures  asymptomatic    recurrent AVM on surveillance posttreatment imaging     incidental finding on imaging after minor trauma vascular lesion location (%)  frontal  parietal  temporal  occipital  frontoparietal  frontotemporal  parietooccipital  cerebellar   side of vascular lesion   left   right

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Value 8 (47) 12.1 (1.2–17.9) 45.5 (12.1–78.9) 7 4 1 1 1 3 1 7 (38.9) 2 (11.1) 1 (5.6) 1 (5.6) 3 (16.7) 1 (5.6) 2 (11.1) 1 (5.6) 13 (72.2) 5 (27.8)

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Intraoperative cerebral angiography in AVM resection in children lier studies. Intraoperative angiography altered patient care in 2 (11%) of 18 neurosurgical procedures. Two repeat intraoperative angiograms were obtained during 1 AVM resection, and 3 repeat intraoperative angiograms were obtained in another. In the first procedure, 1 positive intraoperative angiogram demonstrating a large draining vein and persistent feeding vessels to the AVM resulted in 1 additional AVM resection (Fig. 1). In the second procedure, 2 positive intraoperative angiograms demonstrating early visualization of the internal cerebral vein resulted in 2 re-explorations and 1 surgical coagulation of a small abnormal-appearing nidal vein (Fig. 2). Hence, 21 intraoperative angiography sessions were performed during 18 neurosurgical procedures. Both patients in whom intraoperative angiography altered surgical management had no evidence of residual or recurrent neurovascular abnormality on the most recent follow-up angiography performed at 1 and 2.5 years, respectively. The AVM demonstrated in Fig. 2 was a recurrent AVM. Therefore, although a small lesion, the decision was made to re-resect it using intraoperative angiography. The initial intraoperative angiogram demonstrated early opacification of the internal cerebral vein (Fig. 2B), and the first re-exploration intraoperatively did not demonstrate any nidal vessels. A second intraoperative angiography was performed to assess continued early visualization of the internal cerebral vein, which was still present, necessitating a second re-exploration. At that point a periventricular abnormal-appearing vein was isolated and surgically coagulated. The third intraoperative angiography session revealed no further early opacification of the internal cerebral vein. Follow-up at 2.5 years demonstrated no recurrent or residual disease. A comparison of fluoroscopy time and DAP between single-vessel intraoperative angiography and conventional postoperative angiography performed in the same patient population is shown in Table 2. Dose-area products were available for 6 of 18 cases and fluoroscopy times were available for 13 of 18 cases. Six DAPs and 13 fluoroscopy times for postoperative angiography were chosen from the 17 patients in the cohort, accounting for both age and weight at the time of the procedure. A significant difference was observed between the DAP for intraoperative angiography in comparison with postoperative angiography (p = 0.004), while the fluoroscopy time was not statistically different between intraoperative and postoperative angiography. For conventional postoperative angiography, the protocol includes a complete angiogram

of the bilateral anterior and posterior circulation. For intraoperative angiography, only the vessels of interest are imaged, accounting for the difference in DAP. Complications

There was 1 major procedure-related complication for 21 intraoperative angiography sessions (4.8%), which was a left vertebral artery occlusion believed to be due to dissection in a prone patient with a dominant right vertebral artery. The nondominant left vertebral artery was inadvertently catheterized by the operator. Secondary thrombus formation extending into the basilar artery and bilateral posterior cerebral arteries was noted on CT angiography after the procedure. Follow-up imaging 5 days after intraoperative angiography revealed multiple infarcts in the posterior circulation and a small patent left vertebral artery.

Postoperative Follow-Up

To date 14 (78%) of 18 cases of neurosurgical management with intraoperative angiography have received follow-up postoperative angiography, with 3 of 4 patients not yet due for follow-up evaluation. Median follow-up time from intraoperative angiography to the first postoperative angiogram was 4 months (range 1 day to 8 months), and median follow-up time from intraoperative angiography to the most recent postoperative angiogram was 1.1 years (range 4.3 months to 3.8 years). Two (14%) of 14 postoperative angiograms were positive for the presence of an AVM at 3.5 and 4.7 months from intraoperative angiography. In the first case, postoperative angiography at 3.5 months postoperatively showed a faint arterial blush without associated early venous drainage suspicious for recurrent AVM, which was confirmed on 14-month follow-up imaging. In the second case, postoperative angiography at 4.7 months follow-up revealed a small AVM, which was found to enlarge on 1-year followup. Both patients underwent a second neurosurgery for AVM resection and postoperative angiography at 1-year follow-up showed no residual or recurrent anomalies. For both patients with positive postoperative angiograms on follow-up, the intraoperative angiogram was reviewed via 2-reader consensus followed by 4-reader consensus and confirmed to be negative, without disagreement, indicating probable recurrent rather than residual disease.

Discussion

The importance of postoperative imaging to confirm

TABLE 2: Comparison of DAP and fluoroscopy times between intraoperative and postoperative angiography* Assessment

Intraoperative Angiography

Conventional Postop Angiography

p Value

0.5 0.2–1.8

10.6 3.4–23.9

0.004

6.7 0.9–17.1

11.9 4.4–21.5

NS

DAP (mGy-m ) (n = 6)  median  range fluoroscopy time (min) (n = 13)  median  range 2

*  NS = nonsignificant.

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Fig. 1.  Angiograms obtained in a 15-month-old male presenting with a bulging fontanelle and increased head circumference with vomiting and seizures.  A: Pretreatment diagnostic angiogram demonstrating a left medial occipital AVM (arrowhead) and early venous drainage to the superior sagittal sinus (arrow).  B: Intraoperative angiogram demonstrating persistence of the arterial nidus (arrowhead) with some residual early venous drainage (arrow).  C: Final intraoperative angiogram after repeat resection demonstrating nonvisualization of the arterial nidus (arrowhead) or early venous drainage.  D: Postoperative angiogram obtained at 1-year follow-up demonstrating no evidence of recurrent AVM.

complete neurosurgical resection has been documented by several authors, with Allcock and Drake being the first to describe such an idea in 1963 for the treatment of cerebral aneurysms.3 The benefits of intraoperative angiography include the ability to assess for and address a residual vascular lesion prior to dural closure, thereby reducing the risk of complications from residual lesions, and potentially eliminating the need for future surgeries and associated surgical complications.5 However, the use of routine intraoperative angiography remains controversial, and has been described in a limited fashion in the pediatric population.12,14 Although some authors have recommended selective use of intraoperative angiography, 4.4% of adult patients not chosen to receive intraoperative angiography following aneurysm repair had residual disease requiring intervention, as described by Klopfenstein et al.22 226

Fig. 2.  Angiograms obtained in an 18-year-old female with a recurrent, left frontal AVM.  A: Pretreatment diagnostic angiogram demonstrating an arterial nidus (arrowhead) and early filling of the internal cerebral vein (arrow).  B: Intraoperative angiogram after resection demonstrating absence of an arterial nidus, but persistent early internal cerebral vein opacification (arrow) following initial resection.  C: Final intraoperative angiogram after repeat resection demonstrating absence of early opacification of the internal cerebral vein (arrow).  D: Postoperative angiogram obtained at the 2.5-year follow-up demonstrating no evidence of recurrent AVM.

The current study demonstrated a surgical correction rate of 11%, with 2 of 18 cases meriting altered surgical management as a result of findings on intraoperative angiography. A review of the literature has demonstrated correction rates of 19% (4/22 cases),14 22.2% (4/18),26 and 22.7% (5/22 cases)12 in 3 previously published studies evaluating intraoperative angiography in children. Intraoperative angiography changed management in 10.4%– 29% of AVM resections in the adult population.28,37 Additional studies in the adult population assessed the use of intraoperative angiography in a wider distribution of cerebrovascular anomalies including arterio­venous fistulas and in patients requiring carotid endarterectomies. Barrow et al. described 115 cases of neurovascular anomalies, 19 of which required further surgical management, and 14 of which consisted of AVMs and aneurysms.5 Derdeyn et al. described 112 total neurovascular procedures in which intraoperative angiography changed management in 5 of 18 AVMs, 5 of 66 aneurysms, and 3 of 28 endarterectomies.9 Yanaka et al. reported altered J Neurosurg: Pediatrics / Volume 13 / February 2014

Intraoperative cerebral angiography in AVM resection in children management after intraoperative angiography in 1 (5%) of 20 cases of AVMs and arteriovenous fistulas.39 Intraoperative angiography is not without complications, which include stroke, arterial dissection, emboli, and hematoma.25 Complication rates described in earlier pediatric studies were 4.5%14 and 3.3%,12 and those reported in the adult population ranged from 0.4% to 3.7%.1,7,9,22,25,32,36,37 The complication rate of 4.8% in our study was slightly higher than total complication rates previously reported. However, this may be attributable to the small sample size of the current study. Although intraoperative angiography may play an important role in resection of cerebrovascular anomalies, the literature emphasizes inferior image quality in intraoperative angiography in comparison with that of postoperative angiography.21 Limiting factors include subop­ timal fluoroscopic visibility, contrast via hand injection, nonstandard patient positioning, and artifacts from surgical equipment.21,39 Even with advances in available technology and improved imaging equipment increasing the reliability of intraoperative angiography,39 postoperative angiography has been considered the gold standard in the management of neurovascular anomalies.21 Ellis et al. described a false negative rate of 6.25% for intraoperative angiography in the pediatric population, with 1 of 15 patients demonstrating a positive postoperative angiogram.12 In the management of adult AVMs and aneurysms, the literature describes a false negative rate for intraoperative angiography of 4.8%–5.2%.28,37 However, Lang et al. compared results of postoperative angiography in children who received intraoperative angiography during AVM resection and those who received postoperative angiography on the first day following resection. This study reported similar rates of positive postoperative angiography in both groups, demonstrating intraoperative angiography to be equally sensitive to postoperative angiography for confirming complete AVM resection.26 Several large studies have concluded that patients with complete AVM resection confirmed by negative postoperative angiography do not develop recurrent bleeds.8,11,16,19,38 However, there have been a small number of reported cases of recurrent AVMs following presumed complete resection confirmed by postoperative angiography in the pediatric population.4,20,24 In the current study, the rate of negative intraoperative angiography found to be positive on follow-up postoperative angiography was 14%, indicating probable recurrence in these patients. Recurrences in the pediatric population are reported to occur early.26 The majority of children with negative postoperative angiography at 3 and 6 month follow-up imaging were not found to have recurrent AVMs on further follow-up as reported by Lang et al. However, positive postoperative angiography at approximately 1-year follow-up did occur in a small number of children with negative postoperative angiography at 3 and 6 months postoperatively, emphasizing the importance of postoperative angiography at 1 year in children.26 Furthermore, Lang et al. reports a strong correlation between a low compactness score and the risk for recurrence following complete AVM resection, with diffuse AVMs being more likely to recur.26 J Neurosurg: Pediatrics / Volume 13 / February 2014

Ali et al. reviewed several large pediatric studies and reported a mean of 5.5 years from initial AVM resection to a secondary recurrence in children,2 with a range of 1–9 years.20 However, follow-up was performed using MRI, which is not as sensitive for detection of AVMs as cerebral angiography. The mechanism underlying recurrent AVMs remains unknown. Whether recurrent lesions occur as a de novo malformation or from a residual, angiographically invisible nidus remains unclear.4 The literature describes several factors as potentially contributing to recurrent AVMs, including the immaturity of the growing pediatric cerebrovascular system.20 Hino et al. suggest that small immature vessels, retaining the capability to grow and form another AVM, may have been left in the surgical field.17 Alternative ideas include stimulation of angiogenesis by brain injury, tumors, or inflammation,13,33 as well as by inappropriate expression of humoral growth factors such as vascular endothelial growth factor.2,23,34,35

Conclusions

Intraoperative angiography is an effective and safe adjunct for surgical management of cerebral AVMs in children. Demanding conditions of the intraoperative angiography technique in comparison with postoperative angiography require angiographers with experience and diagnostic acumen; however, the results obtained appear to improve surgical management of neurovascular anomalies in children and reduce both the risks associated with incomplete resection of cerebrovascular anomalies and the need for additional surgery. Disclosure Dr. Ichord is a member of the Clinical Event Committee for the Berlin EXCOR pediatric IDE trial. Author contributions to the study and manuscript preparation include the following. Conception and design: Cahill. Acquisition of data: Gaballah, Rabinowitz, Cahill. Analysis and interpretation of data: Gaballah, Storm, Rabinowitz, Ichord, Cahill. Drafting the article: Gaballah, Storm, Ichord, Cahill. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Gaballah. Study supervision: Cahill. References   1.  Alexander TD, Macdonald RL, Weir B, Kowalczuk A: Intraoperative angiography in cerebral aneurysm surgery: a prospective study of 100 craniotomies. Neurosurgery 39:10–18, 1996   2.  Ali MJ, Bendok BR, Rosenblatt S, Rose JE, Getch CC, Batjer HH: Recurrence of pediatric cerebral arteriovenous malformations after angiographically documented resection. Pediatr Neurosurg 39:32–38, 2003   3.  Allcock JM, Drake CG: Postoperative angiography in cases of ruptured intracranial aneurysm. J Neurosurg 20:752–759, 1963   4.  Andaluz N, Myseros JS, Sathi S, Crone KR, Tew JM Jr: Recurrence of cerebral arteriovenous malformations in children: report of two cases and review of the literature. Surg Neurol 62:324–331, 2004   5.  Barrow DL, Boyer KL, Joseph GJ: Intraoperative angiography in the management of neurovascular disorders. Neurosurgery 30:153–159, 1992

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25.  Kumar R, Friedman JA: Intraoperative angiography during cerebral aneurysm surgery. Neurocrit Care 11:299–302, 2009 26. Lang SS, Beslow LA, Bailey RL, Vossough A, Ekstrom J, Heuer GG, et al: Follow-up imaging to detect recurrence of surgically treated pediatric arteriovenous malformations. Clinical article. J Neurosurg Pediatr 9:497–504, 2012 27.  Loop JW, Foltz EL: Applications of angiography during intracranial operation. Acta Radiol Diagn (Stockh) 5:363–367, 1966 28.  Martin NA, Bentson J, Viñuela F, Hieshima G, Reicher M, Black K, et al: Intraoperative digital subtraction angiography and the surgical treatment of intracranial aneurysms and vascular malformations. J Neurosurg 73:526–533, 1990 29.  Millar C, Bissonnette B, Humphreys RP: Cerebral arteriovenous malformations in children. Can J Anaesth 41:321–331, 1994 30.  Miyamoto S, Hashimoto N, Nagata I, Nozaki K, Morimoto M, Taki W, et al: Posttreatment sequelae of palliatively treated cerebral arteriovenous malformations. Neurosurgery 46:589– 595, 2000 31.  Mori K, Murata T, Hashimoto N, Handa H: Clinical analysis of arteriovenous malformations in children. Childs Brain 6:13–25, 1980 32.  Payner TD, Horner TG, Leipzig TJ, Scott JA, Gilmor RL, DeNardo AJ: Role of intraoperative angiography in the surgical treatment of cerebral aneurysms. J Neurosurg 88:441–448, 1998 33.  Schmit BP, Burrows PE, Kuban K, Goumnerova L, Scott RM: Acquired cerebral arteriovenous malformation in a child with moyamoya disease. Case report. J Neurosurg 84:677–680, 1996 34.  Sonstein WJ, Kader A, Michelsen WJ, Llena JF, Hirano A, Casper D: Expression of vascular endothelial growth factor in pediatric and adult cerebral arteriovenous malformations: an immunocytochemical study. J Neurosurg 85:838–845, 1996 35.  Sure U, Butz N, Siegel AM, Mennel HD, Bien S, Bertalanffy H: Treatment-induced neoangiogenesis in cerebral arteriovenous malformations. Clin Neurol Neurosurg 103:29–32, 2001 36.  Tang G, Cawley CM, Dion JE, Barrow DL: Intraoperative angiography during aneurysm surgery: a prospective evaluation of efficacy. J Neurosurg 96:993–999, 2002 37.  Vitaz TW, Gaskill-Shipley M, Tomsick T, Tew JM Jr: Utility, safety, and accuracy of intraoperative angiography in the surgical treatment of aneurysms and arteriovenous malformations. AJNR Am J Neuroradiol 20:1457–1461, 1999 38. Wilson CB, Hoi Sang U, Domingue J: Microsurgical treatment of intracranial vascular malformations. J Neurosurg 51: 446–454, 1979 39.  Yanaka K, Matsumaru Y, Okazaki M, Noguchi S, Asakawa H, Anno I, et al: Intraoperative angiography in the surgical treatment of cerebral arteriovenous malformations and fistulas. Acta Neurochir (Wien) 145:377–383, 2003 40.  Zhao J, Wang S, Li J, Qi W, Sui D, Zhao Y: Clinical characteristics and surgical results of patients with cerebral arteriovenous malformations. Surg Neurol 63:156–161, 2005 Manuscript submitted June 11, 2013. Accepted October 14, 2013. Please include this information when citing this paper: published online November 29, 2013; DOI: 10.3171/2013.10.PEDS13291. Address correspondence to: Marian Gaballah, B.S., Department of Radiology, Children’s Hospital of Philadelphia, 3401 Civic Center Blvd., Philadelphia, PA 19104. email: [email protected]. edu.

J Neurosurg: Pediatrics / Volume 13 / February 2014

Intraoperative cerebral angiography in arteriovenous malformation resection in children: a single institutional experience.

The use of cerebral intraoperative angiography has been described in resection of arteriovenous malformations (AVMs) in adults. More recently, studies...
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