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Improved diagnosis of actively bleeding aneurysm on CT angiography using delayed CT images
European Journal of Radiology 79 (2011) 328–331
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Case report
Improved diagnosis of actively bleeding aneurysm on CT angiography using delayed CT images Sudhir Kathuria a,b,∗ , John P. Deveikis c , Per-Lennart Westesson c , Dheeraj Gandhi a,b a
Division of Interventional Neuroradiology, Department of Radiology, Johns Hopkins University School of Medicine, Baltimore, MD, United States b Division of Interventional Neuroradiology, Department of Neurology and Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, MD, United States c Division of Diagnostic & Interventional Neuroradiology, Department of Imaging Sciences, University of Rochester Medical Center, Rochester, NY 14642, United States
a r t i c l e
i n f o
Article history: Received 14 September 2009 Accepted 20 January 2010 Keywords: CT angiography Active bleeding Aneurysm Delayed imaging
a b s t r a c t Computed tomographic angiography (CTA) is being increasingly utilized in the non-invasive diagnosis of aneurysmal subarachnoid hemorrhage (SAH). There are emerging reports of diagnosis of active aneurysmal bleeding on CTA, furthering our understanding of imaging features of active extravasation on cross-sectional studies. We demonstrate imaging characteristics of two such cases of active contrast extravasation from intracranial aneurysms. Additionally, we demonstrate that delayed CT images greatly improve the confidence of this diagnosis by demonstrating pooling of contrast in the subarachnoid space. Prompt recognition and management can improve prognosis of this potentially lethal condition. © 2010 Elsevier Ireland Ltd. All rights reserved.
1. Introduction
2. Case reports
Computed tomographic angiography (CTA) is frequently becoming the initial step in detecting ruptured intracranial aneurysms and planning therapeutic interventions [1,2]. Active bleeding during intra-arterial angiography is well documented in the literature [3–7]. However, a few recent case reports have demonstrated that this phenomenon can be recognized on CT angiography [8–11]. The use of CTA in the diagnosis and treatment planning of aneurysmal SAH is increasing and now considered routine at many centers around the world. Despite such widespread use of CTA, the reports of actively bleeding aneurysms are few and further understanding of imaging appearances of this condition is necessary. This report describes two patients with active bleeding on CTA, one from a saccular aneurysm arising from the supraclinoid internal carotid artery (ICA) and another from a right vertebral artery (RVA) dissecting aneurysm. In both patients, active bleeding was suspected on CTA, and confirmed with immediate delayed head CT. This prompted immediate therapeutic intervention and the final outcome was excellent for both patients.
2.1. Case 1
∗ Corresponding author at: Division of Interventional Neuroradiology, Department of Radiology, Johns Hopkins Hospital, 600 North Wolfe St, B100, Baltimore, MD 21287, United States. Tel.: +1 4105028525; fax: +1 4106148238. E-mail address: [email protected] (S. Kathuria). 0720-048X/$ – see front matter © 2010 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2010.01.020
A 67-year-old woman presented with acute onset of thunderclap headache and elevated blood pressure. A non-contrast CT scan showed acute hemorrhage in the basal cisterns, sylvian fissures as well as the occipital horns of the lateral ventricles. Three-dimensional CTA demonstrated a single, posteriorly pointing saccular aneurysm arising from the supraclinoid segment of the right ICA. An additional long, tubular structure with an undulant contour was noticed starting near the aneurysm and extending inferiorly along the clivus and mimicking a vascular structure (Fig. 1A). On the source images, the attenuation values of this structure were similar to that of the basilar artery. On preliminary review, this imaging appearance was confusing and a consideration was given to an arterio-venous fistula. However, on careful re-evaluation, it was considered to be an aneurysm that was actively bleeding at the time of acquisition of this CT angiography. Three minute delayed axial sections showed pooling of large amounts of extravasated contrast within the subarachnoid space, confirming the diagnosis of active bleeding (Fig. 1B). A digital subtraction angiogram (DSA) was obtained emergently and the aneurysm was confirmed. This aneurysm was successfully treated by endovascular coil embolization (Fig. 1C) and the patient made an excellent recovery.
S. Kathuria et al. / European Journal of Radiology 79 (2011) 328–331
2.2. Case 2 A 7-month-old male fell off the bed and hit his head onto a hardwood floor. He initially cried and, over the next hour, became gradually sleepier and started to vomit. He was brought to the emergency room where a non-contrast CT scan revealed acute hemorrhage in the basal cisterns, fourth ventricle, and right cerbellopontine angle cistern. On computed tomographic angiography (CTA), a tubular structure with an undulant contour was noticed coursing in between the intradural segments of the vertebral arteries (Fig. 2A). On the source images, the attenuation of this structure was similar to that of the contrast-opacified vertebral artery (140–160 Hounsfield
329
Units). The diagnosis of traumatic vertebral artery dissection with active bleeding was suspected. Delayed CT images obtained 3 min after the contrast injection showed pooling of contrast within the third and fourth ventricles as well as around cervicomedullary junction, confirming extravasation of contrast (Fig. 2B). This newly pooled contrast showed attenuation values of 80–100 Hounsfield Units (HU), which were in between that of the vertebral artery (150–170 HU) and the subarachnoid blood (50–70 HU). The patient’s neurological status was found to have dramatically worsened immediately following the CTA. Emergent ventriculostomy was carried out and CSF drained as very high opening pressure was encountered at the time of ventriculostomy. A DSA was emergently carried out under general anesthesia and
Fig. 1. Actively bleeding supraclinoid ICA aneurysm during CTA in a 67-year-old woman. (A) Sagittal reformats of 3D-CTA showing long tubular structure arising along the superior wall of aneurysm extending below anterior to basilar artery representing actively extravasating contrast material from bleeding aneurysm. (B) Delayed CT images 3 min after the contrast injection demonstrating “Pooling of contrast” within the subarachnoid space confirming extravasation. (C) Digital subtraction angiogram showing successfully coiled aneurysm.
330
S. Kathuria et al. / European Journal of Radiology 79 (2011) 328–331
Fig. 2. Actively bleeding psuedoaneurysm during CTA in a 7-month-old boy. (A) Coronal reformats showing tubular structure in between two vertebral arteries that represents the actively extravasating contrast material from the bleeding pseudoaneurysm. (B) Delayed CT images 3 min after the contrast injection demonstrating “Pooling of contrast” within the third and fourth ventricle confirming extravasation. (C and D) Digital subtraction angiogram confirmed the pseudoaneurysm that was successfully treated by parent artery occlusion.
confirmed the right vertebral artery dissection with a saccular collection consistent with a pseudoaneurysm, several millimeters distal to the origin of the posterior–inferior cerebellar artery (Fig. 2C). This was successfully treated with complete occlusion of RVA segment distal to PICA with coils (Fig. 2D) after initial attempt of parent vessel preservation by deploying a stent did not occlude the aneurysm completely. The patient made complete neurological recovery and was discharged after 1 month. 3. Discussion Re-rupture of an intracranial aneurysm is associated with a high mortality and poor prognosis [12,5]. With increasing utilization of CTA in diagnosis and treatment planning of ruptured aneurysms, it is important to recognize an actively bleeding aneurysm. Prompt
diagnosis and treatment of this condition may help improve the prognosis of this otherwise potentially lethal complication. Although the use of CTA in aneurysmal SAH is widespread, only a handful of cases with active bleeding during CTA have been reported [8–11]. Further reporting of this condition may result in improved understanding of its imaging appearances as well as potentially, increased diagnosis. A few authors have reported on the description of actively bleeding intracranial aneurysms as seen on CT images. The diagnosis of acute rupture is difficult based only on these varied imaging appearances as well as lack of dynamic information on routing multislice CTA. Holodny et al. [9] reported a “nebulous area of increased attenuation” adjacent and outside to the right internal carotid artery representing extravasated contrast. They also reported a gradual decrease in attenuation of this area of increased
S. Kathuria et al. / European Journal of Radiology 79 (2011) 328–331
density as one moves further away from the aneurysm due to dilution effect, which was also found in both of the cases in the current report. Nakatsuka et al. [10] similarly reported the “cap sign” and the “corkscrew sign” based upon the imaging appearance of extravasated contrast to suggest active bleeding. The undulating, tubular high-density structures that we detected in both present cases are similar to a previously reported finding of twisted, ribbonlike structure mimicking a vessel [5]. Extravasated contrast was seen in the ventricular system in the case of an actively bleeding anterior communicating aneurysm reported by Im et al. [13]. Active bleeding from an intracranial aneurysm (or vessel injury) during CTA will result in extravasation of contrast into the subarachnoid space. As shown in our two cases, this extravasated contrast can easily be detected if an immediate delayed (postcontrast) CT scan is obtained which in both present cases were obtained approximately after 3 min. Addition of a post-contrast scan in the protocol for imaging acute SAH may improve the detection as well as provide increase confidence in the diagnosis of this potentially lethal complication. At the very least, such additional post-contrast scan should be strongly considered in patients that demonstrate clinical deterioration during, or immediately preceding, the CTA study. Delayed CT images will confirm the diagnosis of acute re-rupture by demonstrating the pooling of contrast within the subarachnoid space, which has not been mentioned in any of the previous reports. In the literature, the incidence of aneurysmal rebleeding during intra-arterial angiography varies from 0.01% to 0.35% [4,6,7]. The risk of re-rupture is even higher in pseudoaneurysms, presumably due to their more fragile walls [1]. It may be suggested that the diagnosis of acute rebleed on CTA is rare since the contrast injection is made in a peripheral vein and therefore this technique is unlikely to result in aneurysm re-rupture. Although it has not been thoroughly studied in the setting of subarachnoid hemorrhage, transient hypertension has been reported as a response to intravenous contrast medium in 0.1–0.17% of patients [14–16]. In future longitudinal studies, careful documentation and observation of hemodynamic changes in patients undergoing CTA for aneurysmal bleed may be helpful in demonstrating the true incidence of re-bleeds. 4. Conclusion With the increasing use of CTA, it is important to recognize imaging characteristics and appearances of an actively bleed-
331
ing aneurysm. As shown in this report, delayed CT images can greatly improve the confidence of this diagnosis by demonstrating immediate pooling of contrast in the subarachnoid space. Timely recognition of this potentially devastating condition resulted in prompt institution of endovascular treatment in both our patients and excellent neurological outcomes. Conflict of interest No disclosures, no conflict of interest by any of the authors. References [1] Marshall SA, Kathuria S, Nyquist P, et al. Non-invasive imaging techniques in the diagnosis and management of aneurysmal subarachnoid hemorrhage. Neurosurg Clin North Am 2010;21(2). [2] Matsumoto M, Sato M, Nakano M, et al. Three-dimensional computerized tomography angiography-guided surgery of acutely ruptured cerebral aneurysms. J Neurosurg 2001;94:718–27. [3] Gailloud P, Murphy KJ. Rupture of cerebral aneurysm during angiography. N Engl J Med 1998;340(18):1442. [4] Perret G, Nishioka H. Report on the Cooperative study of Intracranial Aneurysms and Subarachnoid Hemorrhage. IV. Cerebral angiography. An analysis of the diagnostic value and complications of carotid and vertebral angiography in 5,484 patients. J Neurosurg 1996;25:94–114. [5] Komiyama M, Tamura K, Nagata Y, et al. Aneurysmal rupture during angiography. Neurosurgery 1993;33:798–803. [6] Murray JB, Wortzmann G. Contrast medium extravasation from aneurysmal rupture during cerebral angiography. Clin Radiol 1977;28:277–85. [7] Zaehringer M, Wedekin C, Gossmann A, et al. Aneurysmal re-rupture during selective cerebral angiography. Eur Radiol 2002;12(Suppl):S18–24. [8] Desai S, Friedman JA, Hlavin J, et al. Actively bleeding intracranial aneurysm demonstrated by CT angiography. Clin Neurol Neurosurg 2009;111:94–6. [9] Holodny AI, Farkas J, Schlenk R, et al. Demonstration of an actively bleeding aneurysm by CT angiogram. Am J Neuroradiol 2003;24:962–4. [10] Nakatsuka M, Mizuno S, Uchida A. Extravasation on three-dimensional CT angiography in patients with acute subarachnoid hemorrhage and ruptured aneurysm. Neuroradiology 2002;44:25–30. [11] Chang WR, Sang JK, Deok HL, et al. Extravasation of intracranial aneurysm during computed tomography angiography mimicking a blood vessel. J Comput Assist Tomogr 2005;29:677–9. [12] Sorimachi T, Takeuchi S, Koike T, et al. Intra-aneurysmal pressure changes during angiography in coil embolization. Surg Neurol 1997;48:451–7. [13] Im SH, Oh CW, Hong SK, et al. CT angiography demonstration of the development of intraventricular hemorrhage during aneurysm rupture. Clin Neurol Neurosurg 2007;109(3):299–301. [14] Saitoh H, Hayakawa K, Nichimura K, et al. Intracarotid blood pressure changes during contrast medium injection. Am J Neuroradiol 1996;17:51–4. [15] Kurabayashi T, Ida M, Fukayama H, et al. Adverse reactions to nonionic iodine in contrast-enhanced computed tomography: usefulness of monitoring vital signs. Dentomaxillofac Radiol 1998;27:199–202. [16] Hasegawa N. Change of blood pressure and pulse rate in intravenous urography. Nippon Igaku Hoshasen Gakkai Zasshi 1989;49(October(10)):1258–71.
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Case report
Improved diagnosis of actively bleeding aneurysm on CT angiography using delayed CT images Sudhir Kathuria a,b,∗ , John P. Deveikis c , Per-Lennart Westesson c , Dheeraj Gandhi a,b a
Division of Interventional Neuroradiology, Department of Radiology, Johns Hopkins University School of Medicine, Baltimore, MD, United States b Division of Interventional Neuroradiology, Department of Neurology and Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, MD, United States c Division of Diagnostic & Interventional Neuroradiology, Department of Imaging Sciences, University of Rochester Medical Center, Rochester, NY 14642, United States
a r t i c l e
i n f o
Article history: Received 14 September 2009 Accepted 20 January 2010 Keywords: CT angiography Active bleeding Aneurysm Delayed imaging
a b s t r a c t Computed tomographic angiography (CTA) is being increasingly utilized in the non-invasive diagnosis of aneurysmal subarachnoid hemorrhage (SAH). There are emerging reports of diagnosis of active aneurysmal bleeding on CTA, furthering our understanding of imaging features of active extravasation on cross-sectional studies. We demonstrate imaging characteristics of two such cases of active contrast extravasation from intracranial aneurysms. Additionally, we demonstrate that delayed CT images greatly improve the confidence of this diagnosis by demonstrating pooling of contrast in the subarachnoid space. Prompt recognition and management can improve prognosis of this potentially lethal condition. © 2010 Elsevier Ireland Ltd. All rights reserved.
1. Introduction
2. Case reports
Computed tomographic angiography (CTA) is frequently becoming the initial step in detecting ruptured intracranial aneurysms and planning therapeutic interventions [1,2]. Active bleeding during intra-arterial angiography is well documented in the literature [3–7]. However, a few recent case reports have demonstrated that this phenomenon can be recognized on CT angiography [8–11]. The use of CTA in the diagnosis and treatment planning of aneurysmal SAH is increasing and now considered routine at many centers around the world. Despite such widespread use of CTA, the reports of actively bleeding aneurysms are few and further understanding of imaging appearances of this condition is necessary. This report describes two patients with active bleeding on CTA, one from a saccular aneurysm arising from the supraclinoid internal carotid artery (ICA) and another from a right vertebral artery (RVA) dissecting aneurysm. In both patients, active bleeding was suspected on CTA, and confirmed with immediate delayed head CT. This prompted immediate therapeutic intervention and the final outcome was excellent for both patients.
2.1. Case 1
∗ Corresponding author at: Division of Interventional Neuroradiology, Department of Radiology, Johns Hopkins Hospital, 600 North Wolfe St, B100, Baltimore, MD 21287, United States. Tel.: +1 4105028525; fax: +1 4106148238. E-mail address: [email protected] (S. Kathuria). 0720-048X/$ – see front matter © 2010 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2010.01.020
A 67-year-old woman presented with acute onset of thunderclap headache and elevated blood pressure. A non-contrast CT scan showed acute hemorrhage in the basal cisterns, sylvian fissures as well as the occipital horns of the lateral ventricles. Three-dimensional CTA demonstrated a single, posteriorly pointing saccular aneurysm arising from the supraclinoid segment of the right ICA. An additional long, tubular structure with an undulant contour was noticed starting near the aneurysm and extending inferiorly along the clivus and mimicking a vascular structure (Fig. 1A). On the source images, the attenuation values of this structure were similar to that of the basilar artery. On preliminary review, this imaging appearance was confusing and a consideration was given to an arterio-venous fistula. However, on careful re-evaluation, it was considered to be an aneurysm that was actively bleeding at the time of acquisition of this CT angiography. Three minute delayed axial sections showed pooling of large amounts of extravasated contrast within the subarachnoid space, confirming the diagnosis of active bleeding (Fig. 1B). A digital subtraction angiogram (DSA) was obtained emergently and the aneurysm was confirmed. This aneurysm was successfully treated by endovascular coil embolization (Fig. 1C) and the patient made an excellent recovery.
S. Kathuria et al. / European Journal of Radiology 79 (2011) 328–331
2.2. Case 2 A 7-month-old male fell off the bed and hit his head onto a hardwood floor. He initially cried and, over the next hour, became gradually sleepier and started to vomit. He was brought to the emergency room where a non-contrast CT scan revealed acute hemorrhage in the basal cisterns, fourth ventricle, and right cerbellopontine angle cistern. On computed tomographic angiography (CTA), a tubular structure with an undulant contour was noticed coursing in between the intradural segments of the vertebral arteries (Fig. 2A). On the source images, the attenuation of this structure was similar to that of the contrast-opacified vertebral artery (140–160 Hounsfield
329
Units). The diagnosis of traumatic vertebral artery dissection with active bleeding was suspected. Delayed CT images obtained 3 min after the contrast injection showed pooling of contrast within the third and fourth ventricles as well as around cervicomedullary junction, confirming extravasation of contrast (Fig. 2B). This newly pooled contrast showed attenuation values of 80–100 Hounsfield Units (HU), which were in between that of the vertebral artery (150–170 HU) and the subarachnoid blood (50–70 HU). The patient’s neurological status was found to have dramatically worsened immediately following the CTA. Emergent ventriculostomy was carried out and CSF drained as very high opening pressure was encountered at the time of ventriculostomy. A DSA was emergently carried out under general anesthesia and
Fig. 1. Actively bleeding supraclinoid ICA aneurysm during CTA in a 67-year-old woman. (A) Sagittal reformats of 3D-CTA showing long tubular structure arising along the superior wall of aneurysm extending below anterior to basilar artery representing actively extravasating contrast material from bleeding aneurysm. (B) Delayed CT images 3 min after the contrast injection demonstrating “Pooling of contrast” within the subarachnoid space confirming extravasation. (C) Digital subtraction angiogram showing successfully coiled aneurysm.
330
S. Kathuria et al. / European Journal of Radiology 79 (2011) 328–331
Fig. 2. Actively bleeding psuedoaneurysm during CTA in a 7-month-old boy. (A) Coronal reformats showing tubular structure in between two vertebral arteries that represents the actively extravasating contrast material from the bleeding pseudoaneurysm. (B) Delayed CT images 3 min after the contrast injection demonstrating “Pooling of contrast” within the third and fourth ventricle confirming extravasation. (C and D) Digital subtraction angiogram confirmed the pseudoaneurysm that was successfully treated by parent artery occlusion.
confirmed the right vertebral artery dissection with a saccular collection consistent with a pseudoaneurysm, several millimeters distal to the origin of the posterior–inferior cerebellar artery (Fig. 2C). This was successfully treated with complete occlusion of RVA segment distal to PICA with coils (Fig. 2D) after initial attempt of parent vessel preservation by deploying a stent did not occlude the aneurysm completely. The patient made complete neurological recovery and was discharged after 1 month. 3. Discussion Re-rupture of an intracranial aneurysm is associated with a high mortality and poor prognosis [12,5]. With increasing utilization of CTA in diagnosis and treatment planning of ruptured aneurysms, it is important to recognize an actively bleeding aneurysm. Prompt
diagnosis and treatment of this condition may help improve the prognosis of this otherwise potentially lethal complication. Although the use of CTA in aneurysmal SAH is widespread, only a handful of cases with active bleeding during CTA have been reported [8–11]. Further reporting of this condition may result in improved understanding of its imaging appearances as well as potentially, increased diagnosis. A few authors have reported on the description of actively bleeding intracranial aneurysms as seen on CT images. The diagnosis of acute rupture is difficult based only on these varied imaging appearances as well as lack of dynamic information on routing multislice CTA. Holodny et al. [9] reported a “nebulous area of increased attenuation” adjacent and outside to the right internal carotid artery representing extravasated contrast. They also reported a gradual decrease in attenuation of this area of increased
S. Kathuria et al. / European Journal of Radiology 79 (2011) 328–331
density as one moves further away from the aneurysm due to dilution effect, which was also found in both of the cases in the current report. Nakatsuka et al. [10] similarly reported the “cap sign” and the “corkscrew sign” based upon the imaging appearance of extravasated contrast to suggest active bleeding. The undulating, tubular high-density structures that we detected in both present cases are similar to a previously reported finding of twisted, ribbonlike structure mimicking a vessel [5]. Extravasated contrast was seen in the ventricular system in the case of an actively bleeding anterior communicating aneurysm reported by Im et al. [13]. Active bleeding from an intracranial aneurysm (or vessel injury) during CTA will result in extravasation of contrast into the subarachnoid space. As shown in our two cases, this extravasated contrast can easily be detected if an immediate delayed (postcontrast) CT scan is obtained which in both present cases were obtained approximately after 3 min. Addition of a post-contrast scan in the protocol for imaging acute SAH may improve the detection as well as provide increase confidence in the diagnosis of this potentially lethal complication. At the very least, such additional post-contrast scan should be strongly considered in patients that demonstrate clinical deterioration during, or immediately preceding, the CTA study. Delayed CT images will confirm the diagnosis of acute re-rupture by demonstrating the pooling of contrast within the subarachnoid space, which has not been mentioned in any of the previous reports. In the literature, the incidence of aneurysmal rebleeding during intra-arterial angiography varies from 0.01% to 0.35% [4,6,7]. The risk of re-rupture is even higher in pseudoaneurysms, presumably due to their more fragile walls [1]. It may be suggested that the diagnosis of acute rebleed on CTA is rare since the contrast injection is made in a peripheral vein and therefore this technique is unlikely to result in aneurysm re-rupture. Although it has not been thoroughly studied in the setting of subarachnoid hemorrhage, transient hypertension has been reported as a response to intravenous contrast medium in 0.1–0.17% of patients [14–16]. In future longitudinal studies, careful documentation and observation of hemodynamic changes in patients undergoing CTA for aneurysmal bleed may be helpful in demonstrating the true incidence of re-bleeds. 4. Conclusion With the increasing use of CTA, it is important to recognize imaging characteristics and appearances of an actively bleed-
331
ing aneurysm. As shown in this report, delayed CT images can greatly improve the confidence of this diagnosis by demonstrating immediate pooling of contrast in the subarachnoid space. Timely recognition of this potentially devastating condition resulted in prompt institution of endovascular treatment in both our patients and excellent neurological outcomes. Conflict of interest No disclosures, no conflict of interest by any of the authors. References [1] Marshall SA, Kathuria S, Nyquist P, et al. Non-invasive imaging techniques in the diagnosis and management of aneurysmal subarachnoid hemorrhage. Neurosurg Clin North Am 2010;21(2). [2] Matsumoto M, Sato M, Nakano M, et al. Three-dimensional computerized tomography angiography-guided surgery of acutely ruptured cerebral aneurysms. J Neurosurg 2001;94:718–27. [3] Gailloud P, Murphy KJ. Rupture of cerebral aneurysm during angiography. N Engl J Med 1998;340(18):1442. [4] Perret G, Nishioka H. Report on the Cooperative study of Intracranial Aneurysms and Subarachnoid Hemorrhage. IV. Cerebral angiography. An analysis of the diagnostic value and complications of carotid and vertebral angiography in 5,484 patients. J Neurosurg 1996;25:94–114. [5] Komiyama M, Tamura K, Nagata Y, et al. Aneurysmal rupture during angiography. Neurosurgery 1993;33:798–803. [6] Murray JB, Wortzmann G. Contrast medium extravasation from aneurysmal rupture during cerebral angiography. Clin Radiol 1977;28:277–85. [7] Zaehringer M, Wedekin C, Gossmann A, et al. Aneurysmal re-rupture during selective cerebral angiography. Eur Radiol 2002;12(Suppl):S18–24. [8] Desai S, Friedman JA, Hlavin J, et al. Actively bleeding intracranial aneurysm demonstrated by CT angiography. Clin Neurol Neurosurg 2009;111:94–6. [9] Holodny AI, Farkas J, Schlenk R, et al. Demonstration of an actively bleeding aneurysm by CT angiogram. Am J Neuroradiol 2003;24:962–4. [10] Nakatsuka M, Mizuno S, Uchida A. Extravasation on three-dimensional CT angiography in patients with acute subarachnoid hemorrhage and ruptured aneurysm. Neuroradiology 2002;44:25–30. [11] Chang WR, Sang JK, Deok HL, et al. Extravasation of intracranial aneurysm during computed tomography angiography mimicking a blood vessel. J Comput Assist Tomogr 2005;29:677–9. [12] Sorimachi T, Takeuchi S, Koike T, et al. Intra-aneurysmal pressure changes during angiography in coil embolization. Surg Neurol 1997;48:451–7. [13] Im SH, Oh CW, Hong SK, et al. CT angiography demonstration of the development of intraventricular hemorrhage during aneurysm rupture. Clin Neurol Neurosurg 2007;109(3):299–301. [14] Saitoh H, Hayakawa K, Nichimura K, et al. Intracarotid blood pressure changes during contrast medium injection. Am J Neuroradiol 1996;17:51–4. [15] Kurabayashi T, Ida M, Fukayama H, et al. Adverse reactions to nonionic iodine in contrast-enhanced computed tomography: usefulness of monitoring vital signs. Dentomaxillofac Radiol 1998;27:199–202. [16] Hasegawa N. Change of blood pressure and pulse rate in intravenous urography. Nippon Igaku Hoshasen Gakkai Zasshi 1989;49(October(10)):1258–71.