Clinical Neurology and Neurosurgery 237 (2024) 108130 Contents lists available at ScienceDirect Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro Case report Delayed hydrocephalus and visual field defect due to perianeurysmal inflammation after treating a large unruptured aneurysm with flow diverter and coil: A case report Satoru Takahashi 1, Mariko Ishikawa , Hirotaka Sagawa 2, Hikaru Wakabayashi , Shoko Fujii 3, Kyohei Fujita 4, Jiro Aoyama , Sakyo Hirai 5, Kazutaka Sumita *, 6 Department of Endovascular Surgery, Tokyo Medical and Dental University, Tokyo, Japan A B S T R A C T Flow diverter (FD) placement is increasingly used to treat large supraclinoid aneurysms. Here, we report a case of hydrocephalus following FD placement. One patient in her 60 s underwent FD placement combined with coil embolization. Within 1 month, the patient started to show visual field defects and symptoms of hydrocephalus, which worsened within another month. We report that hydrocephalus developed acutely, without high protein levels in the cerebrospinal fluid, and as a complication using a Surpass Streamline. Although the precise mechanisms are unclear, our report suggests a different mechanism for the development of hydrocephalus after FD placement combined with coil embolization. 1. Introduction Flow diverter (FD) placement for treating large supraclinoid aneu­ rysms has increased recently. Based on the SCENT trial, Surpass Streamline (Stryker Neurovascular, Fremont, CA) can be used for unruptured-supraclinoid aneurysms with wide neck (≥4 mm) and large or giant size (≥10 mm) [1]. The combination of FD placement and coil embolization is suggested to prevent rupture after surgery; however, several reports have described the development of hydrocephalus as a complication after treatment with a pipeline embolization device (Medtronic, Minneapolis, MN, USA) combined with coil embolization [2]. Here, we report the case of an unruptured supraclinoid aneurysm treated with a Surpass Streamline in combination with coil embolization in a patient who developed hydrocephalus without septic or aseptic meningitis. 2. Case report A patient in her 60 s was referred to our hospital with a right internal carotid artery (ICA) aneurysm, coincidentally diagnosed using magnetic resonance imaging (MRI). The patient showed no neurological deficits. Pretreatment angiographic images showed a large aneurysm (16 × 15 × 15 mm with a neck of 7.5 mm) arising from the right ICA C2 segment (Fig. 1A, B). The patient underwent placement of a FD, Surpass Streamline (4 × 25 mm), combined with coil embolization using 7 detachable coils (Target 360, Stryker Neurovascular, Fremont, CA, USA) (Fig. 1C, D, E). One week after surgery, the patient was discharged without any neurological deficits and was maintained on dual anti­ platelet therapy with 100 mg aspirin and 3.75 mg prasugrel. The patient presented with a slight defect in the right visual field, gait disturbances, and memory loss one month later. Since the symptoms were mild, we followed up on her symptoms on an outpatient basis. However, the symptoms gradually worsened within a month of the last visit, and urinary incontinence was observed. Angiographic images showed a coil composition with a loop at the tip of the aneurysm (Fig. 1F, G). The Goldmann visual field test revealed defects in both visual fields, which were more severe on the right side (Fig. 1J). Fluidattenuated inversion recovery (FLAIR) MRI detected edema around the * Correspondence to: Department of Endovascular Surgery, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8519, Japan. E-mail address: sumita.nsrg@tmd.ac.jp (K. Sumita). 1 https://orcid.org/0000–0001-6969–8046 2 https://orcid.org/0000–0002-8476–7721 3 https://orcid.org/0000-0002-0695-4716 4 https://orcid.org/0000–0002-5240–6884 5 https://orcid.org/0000–0002-3077–1821 6 https://orcid.org/0000–0002-1348–1099 https://doi.org/10.1016/j.clineuro.2024.108130 Received 7 September 2023; Received in revised form 12 December 2023; Accepted 20 January 2024 Available online 23 January 2024 0303-8467/© 2024 Elsevier B.V. All rights reserved. S. Takahashi et al. Clinical Neurology and Neurosurgery 237 (2024) 108130 treated aneurysm along the optic tract, lateral geniculate body, inferior horn of the lateral ventricles, and even the contralateral posterior horn of the lateral ventricles, which was not observed immediately after surgery (Fig. 2A, C). In addition, the ventricles were enlarged with an Evans index (EI) of 0.37 compared with a preoperative FLAIR EI of 0.3 (Fig. 2B, D). No mechanical obstruction of the cerebrospinal fluid (CSF) pathway was detected on cisternography (Fig. 2G). The CSF examina­ tion showed a normal level of protein (23 mg/dL), glucose (86 mg/dL), and no increased cells (1 lymphocyte/μL). Although the patient was treated with steroids, the disturbance of consciousness worsened, and the patient underwent ventriculoperitoneal shunt placement three months after the FD placement (Fig. 2H, I). Because both aspirin and prasugrel were in therapeutic range confirmed by point-of-care platelet function tests, we stopped prasugrel before shunt placement for safety. Angiographic images 1 year after endovascular surgery showed coil compaction with the disappearance of the loop in the space on the tip of the aneurysm, suspected to be due to change in the composition of thrombus inside the aneurysm (Fig. 1H, I). In the FLAIR MR images, the Fig. 1. Images before and after coil embolization and flow diverter placement. A. An angiographic image of the aneurysm before endovascular surgery. B. A 3Dreconstructed image of the aneurysm. C. An angiographic image of the aneurysm after coil embolization. D. A cone-beam computed tomographic image after coil embolization and flow diverter placement. E. A 3D-reconstructed image. Blue indicates the embolized coil. Time course for the change in the shape of treated aneurysm. F-I. Angiographic (F and H) and 3D reconstructed (G and I) images of the aneurysm after endovascular surgery. Blue indicates the embolized coil. F and G: 3 months after endovascular surgery when the symptoms from hydrocephalus were the most severe. The arrowheads indicate a coil loop in the tip of the aneurysm, H and I: 1 year after endovascular surgery. J. The results of the Goldmann visual field test. The test was performed 2 months after endovascular surgery. 2 S. Takahashi et al. Clinical Neurology and Neurosurgery 237 (2024) 108130 Fig. 2. Time course for edema change around ventricles. A-F. MRI FLAIR images just after flow diverter placement and coil embolization (A, B), just before ven­ triculoperitoneal shunt (C, D), and 6 months after endovascular surgery or 3 months after shunt placement (E, F). Arrowheads indicate the edema along the optic tract. G. A cisternographic image before shunt placement. H, I. An X-ray image (H) and a CT scan image (I) after shunt placement. edema clearly decreased, and the ventricles were no longer enlarged (Fig. 2E, F; edema along the optic tract is indicated by arrowheads). The patient almost completely recovered from the hydrocephalus symptoms, and the visual field defect improved slightly. 3. Discussion Hydrocephalus is a complication of FD placement for large aneu­ rysms. To the best of our knowledge, this is the first report of hydro­ cephalus as a complication of Surpass Streamline. Five patients from four reports, including ours, had progressive gait disturbances, demen­ tia, or urinary incontinence due to hydrocephalus [2–4]. In all patients, 3 S. Takahashi et al. Clinical Neurology and Neurosurgery 237 (2024) 108130 shunt placement improved symptoms. An increasing number of reports have revealed the possibility of developing hydrocephalus after FD placement; however, the etiology of hydrocephalus development re­ mains unclear. Fanning et al. reported that aseptic meningitis is associated with the development of hydrocephalus [5]. Indeed, all other cases that devel­ oped hydrocephalus after FD placement showed high protein levels without increased cells or decreased glucose in the CSF, indicating aseptic meningitis. Previous reports on hydrocephalus after coil embo­ lization for unruptured aneurysm suggested aseptic meningitis due to inflammatory response from thrombus formation was the cause of hy­ drocephalus (Table 1) [6–11]. However, in our case, the CSF protein levels were normal, indicating the absence of aseptic meningitis. Several reports have indicated hydrocephalus after coil embolization of unrup­ tured aneurysms without elevated CSF protein levels [12]. They pre­ dicted that the use of a hydrogel-coated coil or an inflammatory response due to incomplete occlusion of the aneurysms was the cause of hydrocephalus. Since we did not use a hydrogel-coated coil for embo­ lization, we suspected that the inflammatory response around the treated aneurysm was the cause of the hydrocephalus. In our case, the edema detected on FLAIR images spread from the optic tract, lateral geniculate body, the inferior horn of the lateral ventricles, and even the contralateral-posterior horn of the lateral ventricles, which was broader than previous report [2]. The severe inflammatory response around the treated aneurysm may have been the cause of hydrocephalus without aseptic meningitis. All aneurysms in the anterior circulation that developed hydro­ cephalus after endovascular surgery arose superiorly from the ICA and were physically closer to the ventricles. In addition, all patients under­ went FD placement in combination with coil embolization. In one case that followed the aneurysmal size, the diameter temporarily increased, resulting in perianeurysmal edema, and the patient developed a defect in the visual field. The aneurysm was also temporarily enlarged, showing a change in coil composition. Changes in the aneurysm size and coil composition reflect thrombosis in the treated aneurysm. Thrombosis leads to perianeurysmal inflammation, which increases mediators and cytokines in the subarachnoid space, causing edema [13]. When hy­ drocephalus developed, the coil deformed, and although it appeared to deviate slightly from the original aneurysm, edema may have occurred due to the direct contact of the coil-embolized aneurysm with the optic tract from the thrombosed part. Although the number of cases was small, there may be a correlation between the severity of perianeurysmal inflammation, location of aneurysms, and treatment strategy, leading to the development of hydrocephalus. Table 1 Literature review of hydrocephalus as late complications in unruptured aneurysms after coil embolization. author age/ sex aneurysm location aneurysm size coils Meyers et al. (2004) 52/F paraophthalmic > 20 mm Berenstein et al. (2006) 75/F 46/M 79/M paraophthalmic ICA PCoA 10-25 mm < 10 mm 10-25 mm Im et al. (2007) 56/F ICA 8.2 mm Kang et al. (2007) 67/F 64/F 67/F 41/M 51/F ICA ICA ICA ICA BA 11.4 mm 9.6 mm 3.7 mm 12.4 mm 9.3 mm Mitha et al. (2008) 57/F 56/F PCoA BA 26 mm 12 mm Fanning et al. (2008) 56/M 67/F 45/F BA paraophthalmic BA 6 mm 13.2 mm 13.9 mm Misaki et al. (2010) Ozaki et al. (2011) Zanaty et al. (2014) Teranishi et al. (2017) Ichinose et al. (2022) Present case 69/F ICA 18.8 mm 69/F 66/F 75/F PCoA ICA PCoA 15 mm 22 mm 12 mm 64/M 68/F 75/F ICA ophthalmic ICA 27 mm 16.5 mm 21 mm BC 69/F ICA 16 mm BC flow diverter time to postoperative hydrocephalus shunt placement predicted cause of hydrocephalus BC/ HC/ MC BC/ HC BC/ HC BC/ HC BC/ HC BC/ HC BC/ HC BC/ HC BC/ HC BC/ HC BC/ HC BC/ HC BC/ HC BC/ HC BC/ HC BC NA yes chemical meningitis 2.3 months 1.5 months 1 week yes yes yes aseptic meningitis due to inflammatory response from HC in two of the three patients 6 months yes NA NA NA NA NA no yes yes no yes aseptic meningitis due to inflammatory response from HC aseptic meningitis due to inflammatory response from HC 3 weeks 2.5 months yes yes impaired CSF absorption due to elusion of the hydrogel polymer or an associated breakdown product into CSF 30.6 months 11.8 months 7.8 months yes no no inflammatory response from HC 7 months no BC BC PED 18 months 18 months 2.5 months yes yes yes inflammatory response from aneurysm recurrence aseptic meningitis due to chronic inflammatory response from HC chronic inflammatory response from HC PED PED PED 11 months 5 months 10 months yes yes yes Surpass Streamline 1 month yes aseptic meningitis due to exaggerated inflammation aseptic meningitis due to chronic inflammatory response acute inflammatory response ICA:internal carotid artery, BA:basilar artery, PCoA:posterior communicating artery, BC:bare platinum coils, HC:HydroCoils, MC:Matrix coils, NA:not available, PED: pipeline embolization device 4 S. Takahashi et al. Clinical Neurology and Neurosurgery 237 (2024) 108130 In our case, the patient started to show gait disturbance and de­ mentia only 1 month after endovascular surgery. Previous cases showed symptoms of hydrocephalus within 2.5–14 months. The short time course until the appearance of symptoms also supports our hypothesis that the cause of hydrocephalus was not a chronic inflammatory response leading to aseptic meningitis, but rather an acute response. The precise mechanisms are unclear; however, our report suggests a poten­ tially different mechanism for the development of hydrocephalus after FD placement combined with coil embolization compared with previous reports. request. Disclosure statement K.S received lecture fees from Stryker. The other authors have no potential conflict of interest. References [1] P.M. Meyers, A.L. Coon, P.T. Kan, A.K. Wakhloo, R.A. 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[11] M. Ozaki, Y. Murayama, M. Ebara, H. Takao, T. Abe, Delayed hydrocephalus after embolization of unruptured aneurysms using bare platinum coils: report of 2 cases, Am. J. Neuroradiol. 32 (2011) 188–190, https://doi.org/10.3174/ajnr.A2317. [12] A.P. Mitha, J.H. Wong, J.Q. Lu, W.F. Morrish, M.E. Hudon, W.Y. Hu, Communicating hydrocephalus after endovascular coiling of unruptured aneurysms: report of 2 cases, J. Neurosurg. 108 (2008) 1241–1244, https://doi. org/10.3171/JNS/2008/108/6/1241. [13] R.D. Turner, L.D.B. Da Costa, K.G. TerBrugge, A multicenter registry of hydrocephalus following coil embolization of unruptured aneurysms: which patients are at risk and why it occurs, J. Neurointerv. Surg. 5 (2013) 207–211, https://doi.org/10.1136/neurintsurg-2011-010194. 4. Conclusion Herein, we present the case of a patient who developed hydroceph­ alus as a complication of FD placement combined with coil emboliza­ tion. Although the mechanism is unclear, we suggest that severe perianeurysmal inflammation alone, without aseptic meningitis, could lead to the acute onset of hydrocephalus. Further research and accu­ mulation of case reports are necessary to clarify the pathophysiological mechanisms underlying the development of hydrocephalus after FD placement in combination with coil embolization. Author contributors Dr. Takahashi and Ishikawa contributed to the conception and design of the study, data acquisition, drafting of the manuscript. Dr. Sumita contributed to the design of the study, data acquisition, and drafting of the manuscript. Drs. Sagawa, Wakabayashi, Fujii, Fujita, Aoyama and Hirai contributed to data interpretation and critical revi­ sion of the manuscript for important intellectual content. Funding This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors. CRediT authorship contribution statement Sumita Kazutaka: Conceptualization, Supervision, Writing – orig­ inal draft, Data curation. Wakabayashi Hikaru: Data curation, Writing – review & editing. Sagawa Hirotaka: Data curation, Writing – review & editing. Ishikawa Mariko: Conceptualization, Data curation, Writing – original draft. Takahashi Satoru: Conceptualization, Data curation, Writing – original draft. Hirai Sakyo: Writing – review & editing. Aoyama Jiro: Writing – review & editing. Fujita Kyohei: Writing – review & editing. Fujii Shoko: Writing – review & editing. Acknowledgments None. Patient consent We obtained written consent from the patient. This is available on 5