Embolization in the External Carotid Artery
2006; Elsevier BV; Volume: 17; Issue: 12 Linguagem: Inglês
10.1097/01.rvi.0000247301.64269.27
ISSN1535-7732
Autores Tópico(s)Cerebral Venous Sinus Thrombosis
ResumoThe technical skill set of peripheral interventional radiologists is well-suited to the performance of most transcatheter embolization procedures in the external carotid artery (ECA). These procedures center in large part on hypervascular tumors, epistaxis, and trauma. ECA embolization in the trauma patient is well-defined, albeit in small patient series. The transcatheter treatment of epistaxis is still mostly reserved for cases that are intractable to conservative therapy. Preoperative embolotherapy for vascular tumors remains popular, although it is somewhat controversial in terms of its risk–benefit ratio. The purpose of this review is to highlight pertinent anatomy, selected technical procedural aspects, and the available literature to better characterize the role of ECA embolization in the hands of the practicing peripheral interventionist. The technical skill set of peripheral interventional radiologists is well-suited to the performance of most transcatheter embolization procedures in the external carotid artery (ECA). These procedures center in large part on hypervascular tumors, epistaxis, and trauma. ECA embolization in the trauma patient is well-defined, albeit in small patient series. The transcatheter treatment of epistaxis is still mostly reserved for cases that are intractable to conservative therapy. Preoperative embolotherapy for vascular tumors remains popular, although it is somewhat controversial in terms of its risk–benefit ratio. The purpose of this review is to highlight pertinent anatomy, selected technical procedural aspects, and the available literature to better characterize the role of ECA embolization in the hands of the practicing peripheral interventionist. THE external carotid artery (ECA) is anatomically complex, providing the blood supply to the extracranial head and neck and most of the meninges intracranially. Despite this significant arterial network, angiography is presently reserved almost completely as a precursor to highly anticipated transcatheter intervention. ECA intervention is almost exclusively performed in the form of embolotherapy except in unusual situations such as revascularization for atherosclerosis and transcatheter chemotherapeutic instillation, with the latter showing promising results but still limited to experimental protocols at this stage (1Homma Furuta Y Suzuki et al.Rapid superselective high-dose cisplatin infusion with concomitant radiotherapy for advanced head and neck cancer.Head Neck. 2005; 27: 65-71Crossref PubMed Scopus (40) Google Scholar). Transcatheter embolization is likewise limited to relatively few situations. However, because many of these situations are emergent/urgent or preoperative situations in which the surgery is widely performed, intervention in the ECA should be a skill set for not only neurointerventionists, but also peripheral interventionists. The purpose of this review is to provide an outline of ECA embolization procedures, including technical aspects, results, and possible complications. This review is limited to urgent and preoperative situations and does not include the vast array of arteriovenous malformations and, in particular, intracranial malformations involving the dural and cavernous sinuses. Extracranial arteriovenous malformations of the ECA are treated much like those in the peripheral circulation, which also takes a special skill set, and is beyond the scope of this review. The review will begin with a discussion of the pertinent arterial anatomy, followed by a focused description of the technical aspects of these procedures, and then by a discussion of intervention in the particular disease entities. An understanding of the anatomy of the ECA is essential for safe and effective endovascular therapy and is the subject of extensive reviews in several excellent texts. The ECA originates from the bifurcation of the common carotid artery and lies anterior to the internal carotid artery (ICA) in 94% of patients (2Ito H Mataga I Kageyama I et al.Clinical anatomy in the neck region— the position of external and internal carotid arteries may be reversed.Okajimas Folia Anat Jpn. 2006; 82: 157-167Crossref PubMed Scopus (22) Google Scholar). The short trunk of the common ECA progressively decreases in size as it gives rise to eight branches, terminating in the largest of those, the internal maxillary artery (IMA) (Fig 1). The anatomy of the ECA is quite variable and is best considered on a functional basis. In particular, when one artery is small, that area is then supplied by an enlarged neighboring branch. Such variations are important when endovascular therapy is considered. The first branch of the ECA is traditionally the superior thyroidal artery, which arises anteriorly and courses inferiorly to supply the larynx and thyroid gland. It is rarely involved in interventional procedures. The second branch of the ECA is the lingual artery, which arises anteriorly and consists of two portions: a posterior carotid segment and an anterior lingual segment. The former supplies the hypoglossal region, which is important in endovascular terms for tumors hemorrhaging from the floor of the mouth. The more distal anterior lingual segment also supplies the floor of the mouth and most importantly the tongue via the sublingual and deep branches, respectively. Most endovascular procedures for the tongue per se are related to arteriovenous malformations. One must be aware that distal branches of the lingual artery supplying the tongue are terminal branches, the only collateral supply originating from the contralateral lingual artery. Endovascular occlusion of one branch proximally is well-tolerated, but distal or bilateral embolotherapy is poorly tolerated (3Bynoe RP Kerwin AJ Parker III, HH et al.Maxillofacial injuries and lifethreatening hemorrhage: treatment with transcatheter arterial embolization.J Trauma. 2003; 55: 74-79Crossref PubMed Scopus (76) Google Scholar). Superior to the lingual artery and also arising anteriorly is the facial artery, which is complex but can be divided into two segments: the submental horizontal and ascending superficial facial segments. The horizontal segment provides branches to the lateral pharynx and the tonsillar region as well as the hard and soft palates before continuing in the submandibular region, where it supplies the submandibular gland and the floor of the mouth. The superficial segment crosses the mandible before passing superiorly, supplying branches to the chin and the upper and lower lips. The facial artery usually terminates at the nasolabial fold as the angular artery, which is important in endovascular terms for its contributions to the nasal region communicating with the sphenopalatine and ethmoidal vessels, which are of particular interest in the treatment of epistaxis. The next branch, the ascending pharyngeal artery, originates from the ECA posteriorly just inferior to the occipital artery, although its origin may be quite variable. The ascending pharyngeal artery is usually a relatively small, delicate vessel that courses superiorly, giving rise to an anterior and posterior division. The anterior division supplies the pharyngeal tissues for the most part but terminates in tympanic branches, which are important in the endovascular realm in the embolization of tympanicum and jugulare paragangliomas. The posterior division is also of interest to interventionists because it supplies the paravertebral muscles and the meninges, with the latter therefore having an intracranial anastomotic network. The paravertebral muscular supply is important for its rich collateral network with muscular branches of the occipital and vertebral arteries. The posterior division also contributes arterial branches to the ninth, 10th, 11th, and potentially 12th cranial nerves. The occipital artery usually arises from the posterior ECA superior to the ascending pharyngeal artery. Three segments have been variably described as the ascending, horizontal, and second ascending segments. The first ascending segment provides muscular branches and branches to the 12th cranial nerve, and gives rise to the stylomastoid artery in a minority of individuals. This artery usually arises from the posterior auricular artery and is crucial because it provides a portion of the blood supply to the facial nerve. The horizontal segment of the occipital artery provides muscular and meningeal branches. Because of the proximity of this segment to the vertebral artery, there are commonly muscular collaterals to this vessel (4Russell EJ Functional angiography of the head and neck.AJNR Am J Neuroradiol. 1986; 7: 927-936PubMed Google Scholar) (Table 1). Therefore, whenever intervention in the occipital distribution is considered, angiography must exclude collateral supply to the vertebral artery. Posterior meningeal branches from the occipital artery are most often encountered endovascularly in the embolization of meningiomas and dural arteriovenous malformations. The last ascending segment of the occipital artery for the most part provides supply only to the skin and tissues of the posterior cranium.Table 1ECA Anastomoses with Intracranial Branches and Nerve Supply (4Russell EJ Functional angiography of the head and neck.AJNR Am J Neuroradiol. 1986; 7: 927-936PubMed Google Scholar)Branch/ArteryAnastomosis/Neural SupplyVidian arteryICA via vidian arteryPharyngeal arteryICA via basal intracavernous branchesArtery of the foramen rotundumICA via inferolateral trunkEthmoidal branchesOphthalmic arteryMMA petrous branchICA via intra and supracavernous branches/CN VIIAnterior branchOphthalmic artery/CN IV, VCarotid branchICA via small branch of inferolateral trunk or recurrent artery of foramen lacerumJugular arteryVI, IX, X, XIHypoglossal arteryBranches to vertebral artery/CN XIICervical branches 1 and 2Branches to vertebral artery/CN XIIStylomastoid arteryCN VIINote.—CN = cranial nerve. Modified from Russell EJ. Functional angiography of the head and neck. AJNR Am J Neuroradiol 1986; 7:927–936. Used with permission. Open table in a new tab Note.—CN = cranial nerve. Modified from Russell EJ. Functional angiography of the head and neck. AJNR Am J Neuroradiol 1986; 7:927–936. Used with permission. The posterior auricular artery arises from the posterior ECA just above the occipital artery. It presents radiographically as a small vessel and supplies the medial surface of the pinna, the postauricular scalp, and the parotid gland. It is of endovascular interest in the treatment of vascular malformations involving the pinna. The superficial temporal artery arises from the ECA superiorly and gives branches to the parotid gland before coursing superiorly to supply the muscular and cutaneous tissues of the posterior face, anterior pinna, and a large portion of the scalp. It of interest surgically as a conduit for ECA-to-ICA bypass and endovascularly for arteriovenous malformations of the scalp. The IMA is the terminal branch of the ECA. It arises at the neck of the mandible past the origin of the superficial temporal artery, where it gives supply to the parotid gland. The initial segment of the maxillary artery courses anteriorly, becoming the second segment over the pterygoid muscle and giving rise to the middle meningeal artery (MMA) and the accessory meningeal artery, although the latter is quite variable. The third segment courses around the maxilla lying in the pterygopalatine fossa and is therefore better seen in the anteroposterior projection angiographically. Variably, 14 branches arise from the maxillary artery before its terminal branch, the sphenopalatine artery. The accessory meningeal artery supplies the pharynx and Eustachian tube and, inconsistently, the meninges as well. There are numerous muscular branches, including three to the temporal muscles. Three small but important vessels arise near the termination of the IMA and course posteriorly: the vidian artery, the pharyngeal branch, and the artery of the foramen rotundum, all of which represent potential collateral supply to the cavernous ICA (Table 1). Descending branches of the IMA include the masseteric, pterygoid, dental, and buccal arteries. Anterior branches consist of the dental and palatine branches, as well as the easily identified infraorbital artery, which is seen to run on the floor of the orbit (Fig 1a). The terminal branch of the IMA is the sphenopalatine artery, which supplies the medial and lateral walls of the nasal cavity and the sphenoid, ethmoid, and maxillary paranasal sinuses. It characteristically divides into two terminal branches, the posterior nasal and posterior septal arteries. Here, there is an extensive collateral network involving small vessels, including ethmoidal collaterals offering a pathway to the internal carotid circulation via the ophthalmic artery (Fig 2). The sphenopalatine artery is of greatest interest in the performance of embolotherapy for epistaxis and for tumors of the nasopharynx, most notably juvenile nasopharyngeal angiofibroma (JNA). The MMA arises from the IMA in its first segment and passes superiorly through the foramen spinosum, making it the only large branch of the ECA that terminates intracranially. The trunk of the MMA gives rise to four branches: extracranial, basal, anterior, and posterior. The latter two are those seen draped across the dura mater and are most often of interest in endovascular terms in embolization of meningiomas. These may anastomose with the contralateral MMA. There are variations in the anatomy of the MMA; of which the most important to the interventionist involves the ophthalmic artery. This variation entails the development of the lacrimal branch from the MMA instead of the ophthalmic artery, resulting in partial or complete replacement of the ophthalmic artery (Fig 3). Among 170 autopsy specimens, Hayreh and Dass (5Hayreh SS Dass R The ophthalmic artery.Br J Ophthalmol. 1962; 46: 65-98Crossref PubMed Scopus (146) Google Scholar) found four cases in which the ophthalmic artery had a dual origin with a contribution from the MMA and the ICA, with the main contribution to the ophthalmic circulation being from the MMA. Angiographically, it is therefore not enough to simply visualize an ophthalmic artery from the ICA. In two other cases, Hayreh and Dass (5Hayreh SS Dass R The ophthalmic artery.Br J Ophthalmol. 1962; 46: 65-98Crossref PubMed Scopus (146) Google Scholar) found that the ophthalmic artery arose completely from the MMA without an orbital contribution from the ICA, resulting in the so-called meningolacrimal variant. Anterior branches of the MMA must therefore be closely evaluated angiographically and one must be assured that the characteristic choroidal blush is not seen before MMA embolization. It should be kept in mind that the choroidal blush represents ciliary arterial supply indicative of an arterial contribution to the orbital contents, but not specifically the central retinal artery, which is inferred. Embolization of the central retinal artery results in blindness. It is therefore essential that the orbits are visualized on the lateral angiographic view of the ECA injection and certainly the MMA injection. During ECA embolization, the peripheral neurologic complication most often encountered is ischemic injury to the facial nerve, and therefore its arterial supply is critical to understand (6Minatogawa T Kumoi T Hosomi H et al.The blood supply of the facial nerve in the human temporal bone.Auris Nasus Larynx. 1980; 7: 7-18Abstract Full Text PDF PubMed Scopus (27) Google Scholar). The blood supply to the facial nerve is vast, which fortunately makes ischemic injury rare. The petrosal branch of the MMA, which arises from the basal or posterior segment, reaches the geniculate ganglion and forms a profuse, fine arterial network. The nutrient arteries of the facial nerve originate from the stylomastoid artery of the posterior auricular artery, the facial nerve branches of the superficial temporal artery, and the transverse facial artery, as well as a variety of smaller branches (7Liao JM Wang XH Li ZH Applied anatomic study on blood supply for extracranial segment of facial nerve.Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi. 2004; 18: 131-134PubMed Google Scholar). Ischemic injury from embolization usually therefore requires the administration of small particles or liquid agents into numerous branches. However, one must keep in mind previous interventions and vascular compromise by tumors and radiation, for example, altering a normally rich vascular supply. The most useful angiographic view of the ECA is the lateral view, which profiles nearly all vessels (Fig 1). Only distal portions of the occipital and internal maxillary arteries are best seen on the frontal projection. Angiography for proposed embolotherapy of the ECA must include views of the extracranial and intracranial ICA and the ECA, as well as superselective views of each ECA branch before embolotherapy. Injection of the common carotid artery is usually adequate for visualization of important ICA anatomy, particularly vessel occlusion(s) and the origin of the ophthalmic artery. The two most important aspects of ECA angiography are to completely visualize the abnormality in question and to identify intracranial and ophthalmic artery connections (Table 1). Recognition of occlusion of the extracranial ICA or its intracranial branches is of utmost importance before embolization because of the presence of potential ECA-to-ICA collateral vessels. Although one may not always be aware of the exact anatomic names for these connections, careful angiography with adequate contrast medium injections and high-quality imaging over the cranium will identify the presence of intracranial circulation. When one is embolizing posteriorly, particularly in the ascending pharyngeal and occipital arteries, the integrity of the vertebrobasilar system must also be assessed to prevent inadvertent embolization via muscular collaterals. Superselective catheterization of the feeding vessels with a microcatheter system produces better results based on blood loss and operative times and is associated with fewer complications than subselective placement of a diagnostic catheter into the proximal ECA. In a series of 52 meningioma embolization procedures, Ng et al (8Ng SH Wan YL Wong HF et al.Preoperative embolization of meningiomas: comparison of superselective and subselective techniques.J Formos Med Assoc. 1998; 97: 153-158PubMed Google Scholar) reported a 7% rate of postoperative scalp necrosis when particle embolization was performed with the catheter proximal to the distal IMA (n 30) versus no postoperative scalp necrosis with a superselective microcatheter technique (n = 22). Embolization through the diagnostic catheter placed in the ECA trunk should be performed today only in an emergent life-threatening situation that precludes microcatheter superselective techniques. Choice of a microcatheter should be based on the proposed embolic agent and preference of the interventionist. Embolization of ECA branches is performed with particles or coils for the most part, and less often with glue or gelatin sponge. The most common proximal agent is coils, which are most often used for trauma. For tumors and epistaxis, particles remain the most commonly used agent and most of the literature reviewed herein involved the use of traditional nonspherical polyvinyl alcohol (PVA) sponge. For tumors, particularly meningiomas, superselective embolization with smaller particles (50–150 μm) has been shown to induce greater tumor necrosis than larger particles (150–300 μm), suggesting superior embolization; however, tumor swelling is much more prevalent (9Wakhloo AK Juengling FD Van Velthoven V et al.Extended preoperative polyvinyl alcohol microembolization of intracranial meningiomas: assessment of two embolization techniques.AJNR Am J Neuroradiol. 1993; 14: 583-586PubMed Google Scholar). More recent publications have used spherical agents, but with mixed results. Rodiek et al (10Rodiek SO Stolzle A Lumenta CB Preoperative embolization of intracranial meningiomas with Embosphere microspheres.Minim Invasive Neurosurg. 2000; 47: 299-305Crossref Scopus (28) Google Scholar) reported a favorable experience with microspheres in the preoperative embolization of 17 intracranial meningiomas. Kai et al (11Kai Y Hamada J-I Morioka M et al.Clinical evaluation of cellulose porous beads for the therapeutic embolization of meningiomas.AJNR Am J Neuroradiol. 2006; 27: 1146-1150PubMed Google Scholar) recently published a series of 128 consecutive patients with meningiomas successfully embolized with cellulose beads. Alternatively, Bendszus et al (12Bendszus M Rao G Burger R et al.Is their a benefit to preoperative meningioma embolization?.Neurosurgery. 2000; 47: 1306-1312Crossref PubMed Google Scholar) performed preoperative meningioma embolization with hydrophilic gelatin microspheres (Embosphere Microspheres; Biosphere Medical, Rockland, MA; 40–120 μm [n = 12] or 100–300 μm [n = 165]) or hydrogel microspheres (BeadBlock; BioCure, Norcross, GA; 100–300 μm [n = 8]). There were two tumor hemorrhages (one with each agent) and one stroke. The stroke and hemorrhage related to hydrogel microspheres were both in patients treated with the smaller microspheres (40–120 μm). The authors speculated that tumor infarction or flow of particles across the arterial bed into the venous outflow resulted in hemorrhage. Few studies have compared embolic agents for preoperative tumor embolization. Interestingly, mannitol was used as an embolic agent in 23 patients with meningioma and compared favorably with PVA sponge particles, which were used in 31 patients (13Feng L Kienitz BA Matsumoto C et al.Feasibility of using hyperosmolar mannitol as a liquid tumor embolization agent.AJNR Am J Neuroradiol. 2005; 26: 1405-1412PubMed Google Scholar). Finally, tools and techniques continue to undergo evolution at a rapid rate, and therefore more dated reporting may have little impact today. Gelatin sponge particles have been a popular agent, but their use for embolization of vascular tumors of the head and neck is recommended with caution because of their very small and often inconsistent size (14Suyama T Tamaki N Fujiwara K et al.Peritumoral and intratumoral hemorrhage after gelatin sponge embolization of malignant meningioma: case report.Neurosurgery. 1987; 21: 944-946Crossref PubMed Scopus (29) Google Scholar). Major complications of ECA embolotherapy can be divided into necrosis (ie, skin, meninges) from embolization too distally or of too many contiguous branches, stroke or blindness from reflux of embolic agent or undetected ECA-to-ICA collaterals, and cranial nerve ischemia from distal embolization and inappropriate catheter placement. Provocative pharmacologic testing consists of injecting an agent that anesthetizes neural tissue in the arterial distribution in question followed by a clinical neurologic examination directed to the area of concern (eg, central nervous system, eye, facial nerve). Provocative testing has been shown to be a useful means for avoiding complications during embolization of intracranial arteriovenous malformations, most often encompassing the superselective injection of a shortacting barbiturate, usually amobarbital sodium (Amytal sodium; Ranbaxy, Jacksonville, FL). Provocative testing before ECA branch embolization has been described and usually involves the injection of a short-acting barbiturate as well as 2% lidocaine HCl injection (15Horton JA Kerber CW Lidocaine injection into external carotid branches: provocative test to preserve cranial nerve function in therapeutic embolization.AJNR Am J Neuroradiol. 1986; 7: 105-108PubMed Google Scholar, 16Sadato A Taki W Nakahara I et al.Improved provocative test for the embolization of arteriovenous malformations— technical note.Neurol Med Chir. 1994; 34: 187-190Crossref PubMed Scopus (19) Google Scholar). Amobarbital sodium elicits effects on the central nervous system, but often not on peripheral nerves or the retina, unlike lidocaine. Deveikes (17Deveikis JP Sequential injections of amobarbital sodium and lidocaine for provocative neurologic testing in the external carotid circulation.AJNR Am J Neuroradiol. 1996; 17: 1143-1147PubMed Google Scholar) performed provocative testing of both agents in 66 vascular pedicles of 26 patients undergoing ECA branch embolization. Interestingly, only one showed a positive result with sodium amobarbital sodium, whereas seven showed positive results with lidocaine. It is therefore reasonable to perform testing with both medications. The dose of amobarbital sodium is usually 30–50 mg and the dose of 2% lidocaine is 20–50 mg. Lidocaine may cause burning, which can be lessened by adding a few drops of 4.2% sodium bicarbonate. Both agents can be mixed with contrast material for injection to determine distal filling and assess reflux. If the provocative test findings are negative, one can undertake the embolization procedure with a reasonable degree of certainty. However, one is always left with the situation of what to do with positive findings of a provocative test (17Deveikis JP Sequential injections of amobarbital sodium and lidocaine for provocative neurologic testing in the external carotid circulation.AJNR Am J Neuroradiol. 1996; 17: 1143-1147PubMed Google Scholar, 18Barr JD Mathis JM Horton JA Provocative pharmacologic testing during arterial embolization.Neurosurg Clin N Am. 1994; 5: 403-411PubMed Google Scholar). More superselective catheter placement may be an option. In addition, provocative testing provides the anticipated results of a very distal embolization (as with a liquid agent) and the same problems may not occur with a particulate agent. One should always keep in mind why the embolization is being performed and the degree to which it is clinically necessary. If it is preoperative, embolization may not be essential and the particular vascular pedicle that tested positive need not be embolized. However, if the clinical situation necessitates embolotherapy, embolization may be performed with larger particles (such as PVA particles 500–750 μm in size or larger) or proximal agents in the hope of avoiding neurologic compromise. Catheter-induced vasospasm is a common difficulty encountered with superselective catheterization of ECA branches. Embolization, particularly for tumors, is most effective when particles flow distally into the tumor bed. Vasospasm around the catheters will significantly alter flow even to the extent of hemostasis. Several maneuvers are effective in preventing and treating vasospasm. Very gentle microcatheter technique, particularly keeping microwire manipulation to a minimum, helps prevent procedure-induced vasospasm. Vasospasm is also common with very distal microcatheterization, particularly through small, tortuous vessels. It is always a dilemma in patients prone to vasospasm how distally one can place the microcatheter for embolization. The more distal the catheter placement, the safer and more effective the embolization, but unfortunately, the greater the chances of vasospasm being induced. Vasospasm will abate when the catheter is removed, so the catheter can be pulled proximal to the area of vasospasm for a time of watchful waiting. Unfortunately, additional attempts to catheterize the vessels may again elicit vasospasm, often more severe than the initial episode. Intraarterial vasodilators have been used to relieve vasospasm throughout the body (19Stoeckelhuber BM Suttmann I Stoeckelhuber M et al.Comparison of the vasodilating effect of nitroglycerin, verapamil, and tolazoline in hand angiography.J Vasc Interv Radiol. 2003; 14: 749-754Abstract Full Text Full Text PDF PubMed Scopus (7) Google Scholar). ICA vasospasm resulting from distal protection devices is well-recognized and successfully treated with intraarterial nitroglycerine (20MacDonald S Venables GS Cleveland T et al.Protected carotid stenting: Safety and efficacy of the MedNova NeuroShield filter.J Vasc Surg. 2002; 35: 966-972Abstract Full Text Full Text PDF PubMed Scopus (42) Google Scholar). ECA vasospasm can also be effectively treated with 50–100 mg of nitroglycerine via the catheters, including microcatheters. Other intraarterial agents have been successfully used including papaverine (100 mg) and mannitol (10 mL of 25%) (21Vardiman AB Kopitnik TA Purdy PD et al.Treatment of traumatic arterial vasospasm with intraarterial papaverine infusion.AJNR Am J Neuroradiol. 1995; 16: 319-321PubMed Google Scholar, 22Fortin D Osztie E Neuwelt EA Iatrogenic arterial spasm relieved by intraarterial mannitol infusion.AJNR Am J Neuroradiol. 2000; 21: 968-970PubMed Google Scholar). Again, the catheters need to be pulled below the areas of vasospasm before injection, and repeated catheterization is prone to again induce vasospasm. The intravenous administration of calcium-channel blockers has also been reported to be effective in mitigating small artery spasm, particularly nifedipine (23Yoshimura S Tsukahara T Hashimoto N et al.Intraarterial infusion of papaverine combined with intravenous administration of highdose nicardipine for cerebral vasospasm.Acta Neurochir (Wien). 1995; 135: 186-190Crossref PubMed Scopus (17) Google Scholar). Finally, the application of 2–5 inches of nitroglycerine ointment 2% (Nitro-Bid; E. Fougera, Melville, NY) has been shown to be effective in the prevention of vasospasm (24Erba M Jungreis CA Horton JA Nitropaste for prevention and relief of vascular spasm.AJNR Am J Neuroradiol. 1989; 10: 155-156PubMed Google Scholar, 25Lesley WS Lazo A Chaloupka JC et al.Successful treatment of cerebral vasospasm by use of transdermal nitroglycerin ointment (Nitropaste).AJNR Am J Neuroradiol. 2003; 24: 1234-1236PubMed Google Scholar). Traditionally, there are three
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