Neurosurg Rev (2015) 38:523–530 DOI 10.1007/s10143-015-0611-9

ORIGINAL ARTICLE

Surgical treatment of distal anterior cerebral artery aneurysms aided by electromagnetic navigation CT angiography Elvis J. Hermann & Ioannis Petrakakis & Friedrich Götz & Götz Lütjens & Josef Lang & Makoto Nakamura & Joachim K. Krauss

Received: 23 April 2014 / Revised: 3 September 2014 / Accepted: 16 November 2014 / Published online: 10 February 2015 # Springer-Verlag Berlin Heidelberg 2015

Abstract The surgical treatment of distal anterior cerebral artery (DACA) aneurysms still presents a challenge for neurosurgeons because of their small size and their location in the depth of the narrow frontal interhemispheric fissure. This study aimed to investigate feasibility, safety, accuracy, and usefulness of electromagnetic (EM) navigation to aid clipping of DACA aneurysms. Eight patients (age between 2 and 68 years, mean age 49.8 years) with a DACA aneurysm underwent EM-guided neuronavigated microsurgery for clipping of the aneurysm. All patients underwent craniocervical 3D-CT angiography preoperatively. After planning the optimal approach and surgical trajectory avoiding opening of the frontal sinus, the head was fixed. Intraoperative screenshots were correlated with the microscopical view of the DACA aneurysms before clipping. EM-guided neuronavigation using CT angiography for DACA aneurysms enabled fast and accurate referencing of the patient and planning of a tailored craniotomy without opening of the frontal sinus. Intraoperative accuracy was highly reliable except in one instance due to dislocation of the dynamic reference frame (DRF). There was a good correlation between the 3D-CT angiographybased navigation data sets and the intraoperative vascular anatomy. In all patients, bridging veins were spared. The aid of EM neuronavigation was considered useful in all instances. EM-guided neuronavigation using CT angiography for surgery of DACA aneurysms is a useful tool optimizing the surgical approach directly to the aneurysm minimizing additional E. J. Hermann (*) : I. Petrakakis : G. Lütjens : J. Lang : M. Nakamura : J. K. Krauss Department of Neurosurgery, Medical School Hannover, Hannover, Germany e-mail: [email protected] F. Götz Institute of Neuroradiology, Medical School Hannover, Carl-Neuberg-Str.1, 30625 Hannover, Germany

damage to the surrounding tissue during preparation of the aneurysm and the parent vessel.

Keywords CT angiography . DACA aneurysms . Electromagnetic (EM) navigation

Introduction Aneurysms originating from the distal anterior cerebral artery (DACA) or its branches are rare and account only for about 1 to 6 % in most published series on cerebral aneurysms. These aneurysms are often small and rupture, in general, at smaller size than other intracranial aneurysms [1–4]. Typically, ruptured DACA aneurysms cause frontal interhemispheric subarachnoid hemorrhage, and they may also result in frontal intraparenchymal hemorrhage or corpus callosum hematoma [5]. Treatment is challenging both with surgical and endovascular approaches even in unruptured aneurysms because of their usually small size, distal location, and adherence to the frontal lobes inside the narrow interhemispheric fissure [3, 6]. One particular challenge in operating these deep-seated aneurysms is to select a convenient surgical approach and to localize the aneurysm promptly with adequate proximal control of the supplying vessel. Optoelectric navigation based on CT or MR angiography for localization of unruptured cerebral aneurysm was shown to minimize the morbidity related to the surgical approach in selected cases [7–9]. Although electromagnetic (EM) navigation was already used more than a decade ago [10, 11], it gained limited acceptance only more recently [12–15]. It may have certain advantages in comparison to optoelectric navigation in aneurysm surgery.

Yes IV Yes Yes—complete occlusion No No Yes—complete occlusion 4×4 4×6 F M

Intraoperative EM-navigation accuracy was not reliable (deviation of 5 mm from the target point) a

63 52 7. 8.

F

Basal DACA—A2—A. frontoorbitalis and A2/A3— Bifurcation to A. pericallosa and A. callosomarginalis A2/A3—Bifurcation to A. pericallosa and A. callosomarginalis 9 A2/A3—Bifurcation to A. pericallosa and A. callosomarginalis 5 55 6.

F

M F

SAH subarachnoid hemorrhage, ICH intracerebral hemorrhage, DSA digital subtraction angiography, HH Hunt and Hess grade

No No

4×5 No

5×5.5 No

28—giant Infra aneurysm 5 and 4 Infra and supra 51 5.

Supra Supra

Yes—complete occlusion Yes— complete occlusion Yes V Yes No (patient died because of vasospasm) Yes III No Yes—complete occlusion No No Yes III No 4.5×5 4×4.5 No No Pre-coiled 4 53 54 3. 4.

Infra Supra

Yes—complete occlusion Yes—complete occlusion No No No No 3×5 4×4 No No Supra Supra

ICH DSA postoperatively

9 9

A3/A4—A. callosomarginalis A2/A3—Bifurcation to A. pericallosa and A. callosomarginalis Basal DACA—A2—A. frontoorbitalis A2/A3—Bifurcation to A. pericallosa and A. callosomarginalis Basal DACA—A2—A. frontoorbitalis

Preoperatively, cranial CT was performed on a LightSpeed 16 [GE, Milwaukee, WI, USA]. We used the helical mode for CT angiography (CTA) with 120 kV, 440 mA, a slice thickness of 0.625 mm, a pitch of 0.983:1, and an interval of 0.4 mm. The additional scanning time was about 5 min. This image modality is routinely performed in all patients with a subarachnoid hemorrhage as a noninvasive image modality. Scanning was performed in the caudocranial direction beginning at the level of C1 up to the vertex. After injection of 70 ml of contrast medium with 300 mg/ml iodine (Imeron, Bracco, Italy) and 30 ml of saline for flushing, both with a flow rate of 3.5 ml/s, using an automated injector (Stellant CT Injection System, Medrad, Warrendale, PA, USA), scanning

M F

Imaging data acquisition

2 68

For EM navigation, the AxiEM neuronavigation system (Medtronic, Minneapolis, MN, USA) was used. The system is working at a field strength of 100 A/m at 50 mm off face of transmitter coil array (TCA), decrease by 1/r3 (NORM IEC 61000-4-8). The field of the emitter is between 0 and 3.57 G over the working volume (earth magnetic field ∼1 G). The Busable field^ enfolds a roughly cubic shaped area of 650× 525 mm. While we used fiducials fixed to the osseous skull in earlier studies [15], we have modified our technique thereafter by surface-rendering of the face [13].

1a. 2.

Technical specifications of the EM navigation system

Relation to GCC Opening of Craniotomy SAH frontal sinus Size (cm) HH

We prospectively collected data from eight patients who underwent CT angiography-guided EM navigation for surgery of DACA aneurysms between October 2008 and April 2013 in the Department of Neurosurgery at Hannover Medical School. In each instance, the decision to clip the aneurysm was only made after thorough interdisciplinary discussion between neurosurgery and neuroradiology. Mean age at surgery was 49.8 years (range, 2–68 years). Feasibility, usefulness, and safety of EM navigation in the surgical treatment of these challenging deep-seated aneurysms were evaluated according to a standard protocol. Included in this study were four patients with unruptured DACA aneurysms and four patients with ruptured DACA aneurysms. Preoperatively, a 3D-CT angiography was performed in addition to the diagnostic CT in all eight patients for navigation. Patient demographics and a summary of the characteristics of the treated aneurysms are provided in Table 1.

Aneurysm size (mm)

Material and methods

Case no. Age at Sex Aneurysm operation (years) location

Here, we demonstrate the feasibility and usefulness of EM navigation based on CT angiography for surgery of DACA aneurysms.

Neurosurg Rev (2015) 38:523–530 Table 1 Overview of the demographics, aneurysm size, and location in relation to genu of the corpus callosum (GCC), craniotomy size, presence of SAH and ICH, and angiographic result postoperatively of eight patients harboring aneurysms of the DACA, consecutively operated using EM neuronavigation based on CT angiography

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was triggered by a commercially available (GE) bolus detection program. We used source images of CTA for diagnostic purposes and to feed the navigation system. In each patient, maximumintensity projections were reconstructed in the axial, coronal, and sagittal planes. In addition, 3D-reformations were generated also. Intraoperative registration of the patient For preoperative 3D-reconstruction, a workstation was used (Stealth Station, Medtronic Navigation, Minneapolis, MN, USA). After attaching the dynamic reference frame (DRF) to the patient’s head fixed by adhesive tape just above the mastoid process, the Mayfield clamp was fixed to the head, but not to the table. The transmitter coil was fixed to the table at the side where the DRF was attached. Finally, intraoperative registration was achieved by surface matching over the facial surface bilaterally in supine position. Thereafter, registration was achieved by automatical computing of a correlation matrix. Confirmation of accuracy was achieved by checking for deviations of the position of tragus, bregma, nasion (x = lateral, y = anteroposterior, z = vertical) and in addition by checking surface markers of the skull in the frontal and parietal region (sagittal and coronal sutures). Surgery using EM navigation based on CT angiography First, the upper boarder of the frontal sinus was marked on the patient’s forehead allowing to avoid unnecessary opening during craniotomy. A tailored unilateral craniotomy for the interhemispheric approach was planned in order to have a short and straight access to the DACA aneurysm and also to have proximal control of the feeding artery. Also, bridging veins were identified and the trajectory was adjusted accordingly. The trajectory and the craniotomy were then planned such as to reach the aneurysm without damaging the corpus callosum especially for aneurysms below the genum of the corpus callosum (GCC). Following this planning procedure, the Mayfield clamp was fixed to the operation table in an appropriate head flexion to secure an optimal trajectory for the surgeon. Figure 1 shows the intraoperative set-up with the navigation device, transmitter coil, and the pointer. After craniotomy was performed and before opening of the dura, we used the EM navigation pointer with the virtual tip extension to obtain precise orientation with regard to the direction and the distance to the aneurysm. Then, after microsurgical opening of the dura and CSF release, the EM pointer was used again for orientation. Here, additional care was taken

Fig. 1 a The navigation pointer in the intraoperative set-up; b the transmitter coil (in black) fixed to the table and the dynamic reference frame (in white) attached to the patient’s head

not to blindly rely on the navigation because of possible brainshift especially in patients with ruptured aneurysms and brain swelling. Thereafter, the operation was continued in standard microneurosurgical technique following the trajectory to the target point. Subsequently, the surgeon alternated various times from microsurgical preparation under microscopical view to on-line tracking navigation via the tip of the EM pointer to check the distance and control the right direction to the target. Once reaching the aneurysm by microscopical view, we checked again accuracy by direct positioning of the tip of the EM pointer on the aneurysm and comparing its position with the 3D-CT angiography data set on the navigation screen. This was documented by an intraoperative photo under the microscope and a screenshot on the EM navigation system. An intraoperative indocyanine green (ICG) angiography [16–18] was performed to delineate the occlusion of the clipped aneurysm and the patency of the afferent and efferent vessels.

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Postoperative imaging Postoperative CT scans were obtained 6 h after surgery to rule out any postoperative complications like bleeding, infarction, brain swelling, hydrocephalus, or pneumocephalus. A postoperative digital subtraction angiography (DSA) which serves as Bgold standard^ in our department was performed to control and document occlusion of the clipped aneurysm and to rule out additional aneurysms within 7 days postoperatively.

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surrounding vascular and pial structures especially in patients with ruptured aneurysms. Particularly, no damage to frontal bridging veins occurred. Immediate identification of the parent vessel was possible in all cases, which was temporarily clipped except in one instance. There were no problems with line-of-sight issues at any time during surgery establishing an atmosphere of calmness for the whole surgical team, which was reassuring especially in ruptured aneurysms.

Postoperative angiography Results Feasibility In all eight cases, CT angiography-based EM navigation for DACA aneurysms was technically feasible. Additional scan time for the 3D-CT angiography was about 5 min in average and additional time for setup of the EM navigation system in the operating room was about 10–15 min. Safety and accuracy Fast and accurate referencing was possible in all patients. Accuracy of registration was within 2 mm in any case in all three axes as determined by checking the positions for tragus, nasion, and bregma. Intraoperative accuracy was not reliable in one patient (deviation of 5 mm from the target point) where dislocation of the DRF fixed in the frontal region occurred during the surgical approach by skin retraction. This failure was excluded in the other seven patients by fixation of the DRF right above the mastoid process avoiding the risk for dislocation during frontal surgical approach. The intraoperative target localization in these seven cases coincided exactly with the predetermined localization of the aneurysm. There was little interference of electromagnetic impulses with metallic artifacts. On the surface, accuracy was checked before the wound retractor was placed and also thereafter. In the depth of the interhemispheric fissure, no interferences were noted when the tip of the EM stylet was used for navigation. Usefulness EM navigation was rated as very helpful in all cases by the operating neurosurgeon. A tailored frontal craniotomy, sized about 4 cm in diameter, was performed in each instance. Opening of the frontal sinus was prevented in all cases avoiding associated morbidity. Moreover, the extent of the surgical corridor needed could be reduced following the chosen ideal navigated trajectory to the aneurysm. This method helped minimizing the surgical dissection and damage to the

Postoperative DSA showed complete occlusion of the aneurysms in all patients who underwent postoperative DSA. The patient with a ruptured giant aneurysm (case no. 5) died following devastating vasospasm prior to the planned postoperative DSA.

Case vignette A 54-year-old woman (Table 1, case no. 4) with a ruptured 4 mm bifurcation aneurysm (pericallosal/callosomarginal) was selected for urgent EM-guided surgery based on CT angiography. Preoperative CT of the head showed a subarachnoid hemorrhage in the frontal interhemispheric fissure without intracerebral or intraventricular hematoma. Clinical examination revealed a somnolent patient without further neurological deficits corresponding to Hunt and Hess III. The aneurysm could be visualized clearly in the preoperative 3D-CT angiography (Fig. 2). After referencing the patient in supine position with the head fixed in the Mayfield clamp first, an external ventricular drainage on the right side was inserted via Kocher’s point using the EM-navigation stylet without CSF release [13]. Only after the angle for the optimized trajectory was confirmed by the EM navigation, the Mayfield clamp was fixed to the table. Thereafter, a tailored craniotomy and the optimal trajectory to the aneurysm were planned on the navigation screen using the tip extension view (Fig. 3). The frontal sinus was left intact avoiding unnecessary possible complications and sparing operative time. Choosing a straightforward trajectory helped to avoid damage to the surrounding tissue and the bridging veins on the way to the aneurysm in this narrow anatomical corridor. Figure 4 shows a good correlation between the intraoperative localization of the aneurysm with the CT angiography data set. There was good control of the parent vessel. After clipping of the aneurysm, ICG angiography was performed to confirm occlusion of the aneurysm and patency of the parent vessel distal and proximal to the clipped aneurysm. Postoperative CT control 6 h after clipping showed no infarction and postoperative transfemoral DSA reconfirmed complete occlusion of the aneurysm.

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Fig. 2 A 54-year-old patient with a 4-mm sized A2/A3 aneurysm (arrows pointing out the aneurysm) at the junction between pericallosal (PC) and callosomarginal (CM) artery of the left ACA. Triplanar CTangiogram scans show the exact aneurysm location in relation to the genu of the corpus callosum (a axial, b sagittal, c coronal). 3Dcomputed tomography angiography reconstructed with 3D imaging software shows the aneurysm at the PC-CM junction, the projection of the aneurysmal dome, and its relationship to the surrounding vessels (d)

Our study indicates that EM-guided neuronavigation using CT angiography is not only feasible with ease, but that it is very useful and safe in the surgical treatment of cerebral aneurysms,

especially in the case of DACA aneurysms which are rarer compared to aneurysms located at other sites and which pose special challenges [1–4, 19]. Given the sometimes small size of these aneurysms, navigation will only provide added value when it provides sufficient accuracy as shown here.

Fig. 3 The neuronavigation system monitor displays in real-time tracking the correlation between the position of the navigation pointer on the skin surface and the vascular lesion prior to skin incision. With the yellow tip extension, the distance between skin and aneurysm can be measured precisely. Moreover, an optimal surgical trajectory through the narrow

interhemispheric fissure can be meticulously planned prior to fixation of the Mayfield clamp. Thus, an optimal head positioning regarding flexion/ extension and a circumscribed skin flap for a Btailored^ craniotomy can be performed, with an optimal trajectory, identifying the frontal sinus and surface bridging veins

Discussion

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Fig. 4 The dissection along the interhemispheric fissure can be performed with the aid of real-time neuronavigation tracking, optimizing the surgical corridor and minimizing surgical maneuvers. This figure shows the exactly predetermined location of the aneurysm at the PC-

CM junction in the operation field with the navigation pointer directed to the aneurysm (b) and at the same time the display of the neuronavigation monitor matching the CTA data precisely and confirming the location of the aneurysm (a)

There are three categories of DACA aneurysms with regard to their relation to the genu of the corpus callosum (GCC). First, aneurysms arising proximal to the GCC (located between frontobasal branches of the anterior cerebral artery and GCC). These basally located aneurysms need a very flat angulated trajectory to be reached without damaging the corpus callosum. Second, aneurysms around the GCC (located in most cases in the bifurcation between pericallosal and callosomarginal branches). Third, aneurysms distal to the GCC (located superior to the corpus callosum along the distal A3 and A4 branches of the anterior cerebral artery). These aneurysms need a rather long trajectory to be reached in the depth of the interhemispheric fissure [2, 19]. DACA aneurysms present various challenges for both surgical and endovascular treatment even in experienced hands. Both procedures are accepted treatment options for DACA aneurysms [3]. Nevertheless, in each case, the decision about what kind of treatment is favored should be made only after thorough interdisciplinary discussion between the neurosurgeon and the neuroradiologist. Although, they are usually small in size, it is known that DACA aneurysms rupture at smaller size than other intracranial aneurysms [2, 19]. The small size, the rather wide base, and the sometimes calcified but thin dome of these aneurysms which may be adherent to the surrounding structures in the interhemispheric fissure and not least the involvement of the thin and vulnerable parent vessels make these aneurysms particularly difficult to treat [4]. The limited surgical corridor in the interhemispheric frontal fissure with the narrow pericallosal arachnoidal cistern poses a further challenge for surgery especially after subarachnoid hemorrhage and intracerebral bleeding. Surgery needs frontal lobe retraction to gain access to the aneurysm. This harbors the risk of tearing bridging veins with subsequent venous infarction and of intraoperative rupture of the

aneurysm [20, 21]. During dissection, damage to the vulnerable vascular structures and surrounding tissue is a veritable risk even in high-load centers. Other difficulties in the surgical treatment are to choose a tailored approach to locate the aneurysm directly in the interhemispheric fissure, and to clip its neck adequately with appropriate control and without obstruction of the parent vessel during dissection of the aneurysm [2, 19]. The interhemispheric approach used should be selected such as the GCC does not hinder the view to the aneurysm. The size of the bone flap should not be too small to maintain the chance to work between the bridging veins. In our patients, the bone flaps were about 4 cm in diameter which was smaller as compared to other studies [2, 19]. Nevertheless, EM navigation allowed a straightforward approach through the interhemispheric fissure even in patients with subarachnoid hemorrhage with swollen brain tissue and blood constraining the view of the surgeon. Optoelectric navigation nowadays is an integral component of neurosurgical equipment and a very helpful tool in different neurosurgical procedures [22]. It was already shown that optoelectric navigation for localization of unruptured aneurysm may minimize the morbidity related to the surgical approach especially in media bifurcation aneurysms and in few cases also in DACA aneurysms [7–9]. The reported series used optoelectric navigation based on CT or MR angiography. CT angiography, a noninvasive and fast imaging method, was shown to be as sensitive and specific as DSA in aneurysms larger than 2 mm [23–25]. Visualization of DACA aneurysms by CT angiography may obviate the need for digital subtraction angiography under certain circumstances. CT angiography-based neuronavigation was shown to be an interesting alternative even in emergency cases in ruptured aneurysms with subarachnoid hemorrhage [26].

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Unfortunately, optoelectric navigation has some disadvantages, in particular line-of-sight problems which not only result in prolonged and repeated registration procedures to reach an acceptable accuracy for surgery, but which may also hinder the procedure because of interferences with the microscope. Furthermore, it is not possible to change position of the head, once registration has been accomplished. Before we used EM navigation for surgery of DACA aneurysms, we occasionally had applied an optoelectric navigation system. Although no direct comparison can be made, according to our anectodal experience, EM navigation is clearly advantageous for this purpose since surgical time was shorter, and there are no line-of-sight problems and better comfort was provided to the surgeon after reangulation of the patient’s head to determine the most appropriate trajectory after registration. EM navigation is a relatively new technique, but it has already been demonstrated to have several advantages as compared to the established optical navigation systems not only in children [13, 27] but also in adults [12, 14, 15, 28]. It obviates the need for sharp head fixation in shunt surgery [29] and in neuronavigated endoscopy [30–32]. Possible interferences with electromagnetic objects need to be taken into account. EM navigation has been already established in many other medical fields such as interventional bronchoscopy, arthroscopy, interventional vascular surgery, and gastrointestinal endoscopy [33–36]. In neurosurgery, EM navigation is slowly gaining more popularity as well. The major reason for its slow propagation may be that it is manufactured only by one company, nowadays, and it is not in the focus of marketing. It was shown that the accuracy of EM navigation is comparable to that of optoelectric navigation systems [37, 38]. Comparative studies investigating the accuracy of optoelectric versus EM navigation, however, are limited. In the present study, registration errors were minimal and also target localization was accurate except in one patient due to human error. We think that the high accuracy in our study may be related both to the image acquisition technique using CT and CTA and to the intraoperative registration technique using surface rendering with large matrix [39]. Flexible EM navigation with a dynamic reference frame appears to be a very useful method in planning the tailored craniotomy and the optimal trajectory to the DACA aneurysms because even changes of the head position after referencing of the patient in the Mayfield clamp to optimize head angulation for surgery is possible and useful without loss of navigation accuracy.

Conclusions EM-guided neuronavigation based on CT angiography for surgery of DACA aneurysms is technically feasible and enables fast and accurate referencing of the patient for navigation. It is a very useful tool for treating these relatively rare and

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challenging aneurysms. It allows precise planning of the surgical approach and trajectory to access the aneurysm and the parent vessel for bleeding control in the depth of the interhemispheric fissure avoiding disorientation especially in patients with subarachnoid hemorrhage. With the present study, we extend the limited navigation experience with this technique demonstrating its usefulness in selected patients for an optimal and straightforward approach to DACA aneurysms. Conflict of interest None.

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Comments Nicholas C. Bambakidis, Cleveland, USA This article is a review of a technique of stereotactic localization called electromagnetic CT angiography (EM CTA) in the use of surgery for distal anterior cerebral artery aneurysms (DACA). The authors do have an important point in that DACAs can be difficult to address surgery due to their location and relative rarity, and stereotactic localization during surgery can be helpful. This is compounded by the fact that the surgical approach can be treacherous as proximal control may not be obtained until after the aneurysm is exposed. For our cases, we have utilized CTA images merged with traditional optical navigation systems to limit dissection and aid in proximal vessel identification with good results. The described study, however, does propose an additional tool which could be used in treating these difficult lesions. Ludwig Benes, Arnsberg, Germany This is an interesting paper on electromagnetic navigation in surgical treatment of distal anterior cerebral artery aneurysms (DACA), although the procedure is not new and even published for neurosurgical use a couple of years ago. The EM-navigation technique is well descripted in the present paper, but we should be aware of the fact that this technique bears the risk of target registration errors and possible electromagnetic impulses by, e.g., metal artifacts. Therefore, EM navigation is according to some experts not so precise compared to optical navigation devices. Furthermore, considering the possible lower accuracy compared to optical systems, the question comes up how can the surgeon find very small aneurysms with 2 or 3 mm in size with the help of electromagnetic navigation? And do we need electromagnetic navigation with reduced accuracy in these vascular cases at all?

Surgical treatment of distal anterior cerebral artery aneurysms aided by electromagnetic navigation CT angiography.

The surgical treatment of distal anterior cerebral artery (DACA) aneurysms still presents a challenge for neurosurgeons because of their small size an...
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