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Early side effects after embolization of a carotid body tumor using Onyx

2010; Elsevier BV; Volume: 52; Issue: 3 Linguagem: Inglês

10.1016/j.jvs.2010.04.026

1097-6809

Susanne Wiegand, Ingo Kureck, René Chapot, Andreas M. Sesterhenn, Siegfried Bien, Jochen A. Werner,

Pituitary Gland Disorders and Treatments

The case of a 20-year-old woman with a carotid body tumor of Shamblin class III is reported. Ten hours after preoperative direct intralesional embolization with 20 mL Onyx (ethylene-vinyl alcohol copolymer; Micro Therapeutics, Irvine, Calif), the patient showed symptoms of Horner syndrome and deficits of the hypoglossal and glossopharyngeal nerves. Intraoperative examination 12 hours after Onyx embolization revealed a massive swelling of the hypoglossal and glossopharyngeal nerves. The patient's tongue motility and glossopharyngeal function improved after surgery, but Horner syndrome was still present. Owing to the delayed occurrence of these adverse effects, the optimal time of surgical intervention after Onyx embolization should be discussed and perhaps expedited. The case of a 20-year-old woman with a carotid body tumor of Shamblin class III is reported. Ten hours after preoperative direct intralesional embolization with 20 mL Onyx (ethylene-vinyl alcohol copolymer; Micro Therapeutics, Irvine, Calif), the patient showed symptoms of Horner syndrome and deficits of the hypoglossal and glossopharyngeal nerves. Intraoperative examination 12 hours after Onyx embolization revealed a massive swelling of the hypoglossal and glossopharyngeal nerves. The patient's tongue motility and glossopharyngeal function improved after surgery, but Horner syndrome was still present. Owing to the delayed occurrence of these adverse effects, the optimal time of surgical intervention after Onyx embolization should be discussed and perhaps expedited. Paragangliomas of the carotid body are rare, highly vascularized tumors of neural crest origin.1Bishop G.B. Urist M.M. Gammal T. Peters G.E. Maddox W.A. Paragangliomas of the neck.Arch Surg. 1992; 127: 1441-1445Crossref PubMed Scopus (52) Google Scholar They are usually benign but locally destructive tumors presenting at any age.2Sprong D.H. Kirby F.G. Familial carotid body tumors: a report of nine cases in eleven siblings.Ann West Med Surg. 1949; 3: 241-242PubMed Google Scholar In 1743, von Haller described the carotid body for the first time.3Milewski C. Morphology and clinical aspects of paragangliomas in the area of head-neck.HNO. 1993; 41: 526-531PubMed Google Scholar The carotid body is located at the common carotid artery bifurcation and is typically fed mainly from the external carotid artery.4Davidovic L.B. Djukic V.B. Vasic D.M. Sindjelic R.P. Duvnjak S.N. Diagnosis and treatment of carotid body paraganglioma: 21 years of experience at a clinical centre of Serbia.World J Surg Oncol. 2005; 3: 10Crossref PubMed Scopus (68) Google Scholar Carotid body tumors usually present as slow-growing neck masses. Shamblin et al5Shamblin W.R. ReMine W.H. Sheps S.G. Carotid body tumor (chemodectoma): clinicopathologic analysis of ninety cases.Am J Surg. 1971; 122: 732-739Abstract Full Text PDF PubMed Google Scholar introduced a system to classify these tumors according to tumor size and the degree of involvement of the internal carotid artery. Tumors that do not compress or involve both carotid vessels are classified as Shamblin I, tumors that compress the carotid vessels are Shamblin II, and those that involve the carotid vessels are Shamblin III.5Shamblin W.R. ReMine W.H. Sheps S.G. Carotid body tumor (chemodectoma): clinicopathologic analysis of ninety cases.Am J Surg. 1971; 122: 732-739Abstract Full Text PDF PubMed Google Scholar Surgery is the only curative treatment for carotid body tumors; however, radiotherapy may be indicated in cases of giant or recurrent carotid body tumors or in malignant tumors with metastases to the regional lymph nodes.6Evenson L.J. Mendenhall W.M. Parsons J.T. Cassisi N.J. Radiotherapy in the management of chemodectomas of the carotid body and glomus vagale.Head Neck. 1998; 20: 609-613Crossref PubMed Scopus (57) Google Scholar, 7Mayer R. Fruhwirth J. Beham A. Groell R. Poschauko J. Hackl A. radiotherapy as adjunct to surgery for malignant carotid body paragangliomas presenting with lymph node metastases.Strahlenther Onkol. 2000; 176: 356-360Crossref PubMed Scopus (18) Google Scholar Surgical treatment is always associated with the risk of damage to major vascular structures and to cranial nerves. Preoperative embolization seems to reduce blood loss, facilitate surgical resection, and reduce operating time and morbidity. Embolization is often performed with particulate agents by using the transarterial route since transarterial embolization was introduced by Schick et al8Schick P.M. Hieshima G.B. White R.A. Fiaschetti F.L. Mehringer C.M. Grinnell V.S. et al.Arterial catheter embolization followed by surgery for large chemodectoma.Surgery. 1980; 87: 459-464PubMed Google Scholar in 1980. The disadvantage of transarterial embolization of paragangliomas is that devascularization often is incomplete due to the frequent presence of very small feeding branches that cannot be directly catheterized. Direct intralesional embolization with liquid agents often is superior in the degree of devascularization achieved. The first direct intralesional embolization of a paraganglioma was described in 1994.9Casasco A. Herbreteau D. Houdart E. George B. Tran Ba Huy P. Deffresne D. et al.Devascularization of craniofacial tumors by percutaneous tumor puncture.Am J Neuroradiol. 1994; 15: 1233-1239PubMed Google Scholar Since then, several liquid agents, such as N-butyl-2-cyanoacrylate, lipiodol, ethanol, and Onyx (ethylene-vinyl alcohol copolymer; Micro Therapeutics, Irvine, Calif), have been used for preoperative direct embolization of paragangliomas.10Horowitz M. Whisnant R.E. Jungreis C. Snyderman C. Levy E.I. Kassam A. Temporary balloon occlusion and ethanol injection for preoperative embolization of carotid-body tumor.Ear Nose Throat J. 2002; 81: 536-538PubMed Google Scholar, 11Harman M. Etlik O. Unal O. Direct percutaneous embolization of a carotid body tumor with n-butyl cyanoacrylate: an alternative method to endovascular embolization.Acta Radiol. 2004; 45: 646-648Crossref PubMed Scopus (21) Google Scholar Special risks of direct embolization are migration of glue into the intracranial circulation, chemical toxicity, and hemorrhage after direct puncture.12Derdeyn C.P. Neely J.G. Direct puncture embolization for paragangliomas: promising results but preliminary data.AJNR Am J Neuroradiol. 2004; 25: 1453-1454PubMed Google Scholar However, to our knowledge, no study to date has compared the risks of transarterial and direct embolization in carotid body tumors and no severe complications have been described after Onyx embolization of a carotid body tumor. Most authors have, however, described total or near total devascularization of paragangliomas after Onyx embolization that facilitated the surgical intervention.13Ozyer U. Harman A. Yildirim E. Aytekin C. Akay T.H. Boyvat F. Devascularization of head and neck paragangliomas by direct percutaneous embolization.Cardiovasc Intervent Radiol. 2010; ([E-pub ahead of print: doi: 10.1007/s00270-010-9803-4])Google Scholar The aim of the present study was to describe the advantages and potential adverse effects of preoperative direct intralesional embolization of a carotid body tumor using the nonadhesive, nonacrylic liquid polymer agent, Onyx. A 20-year-old woman presented with a swelling of the right side of the neck of 1-year duration. The clinical examination was unremarkable except for the swelling. Magnetic resonance imaging revealed a well-defined heterogenous mass at the region of the carotid bifurcation that exhibited intense contrast enhancement after intravenous administration of gadolinium (Fig 1). A strong vascularity of the tumor and a separation of the internal and external carotid artery with a posterior displacement of the internal carotid artery were evident on the angiography (Fig 2). Moreover, it showed a tumor blush pathognomic for paragangliomas (Fig 3,A). The diagnosis was a 7- × 3- × 4-cm right-sided carotid body tumor of Shamblin class III, reaching from the carotid bifurcation to the skull base, with a conical extension into the jugular foramen.Fig 2Magnetic resonance imaging angiography of the carotid body tumor revealed a separation of the internal and external carotid artery, with a posterior displacement of the internal carotid artery.View Large Image Figure ViewerDownload Hi-res image Download (PPT)Fig 3A, Angiography showed the pathognomic tumor blush. B, Final angiography after Onyx embolization revealed complete devascularization of the tumor.View Large Image Figure ViewerDownload Hi-res image Download (PPT) After diagnostic imaging, preoperative direct intralesional embolization with Onyx was performed under general anesthesia. A 6F vascular sheath was placed in the right common femoral artery and a 6F catheter was navigated into the common carotid artery. A 4- × 30-mm balloon was placed into the right internal carotid artery. A needle was then placed into the paraganglioma under roadmap guidance. Embolization was performed using 20 mL of Onyx until complete devascularization of the paraganglioma was achieved (Fig 3, B). Three hours later, the patient described right-sided oral paraesthesia. Ten hours after the intervention, the patient showed symptoms of Horner syndrome and deficits of the hypoglossal and glossopharyngeal nerves, which became evident by a tongue motility disturbance, enoral paraesthesia, and a ptosis and miosis of the right eye. The patient underwent planned surgery under general anesthesia 12 hours after embolization. The tumor was carefully dissected from the common, external, and internal carotid arteries, with preservation of the hypoglossal, glossopharyngeal, and vagal nerves. Intraoperative examination revealed a massive swelling of the hypoglossal (Fig 4) and glossopharyngeal nerves after Onyx embolization. There were no signs of ischemia of the nerves. Intraoperative bleeding was minimal, however, and the Onyx cast delineated the boundaries of the tumor, thus facilitating its removal. The common carotid, internal, and external carotid arteries were left intact. The patient's tongue motility and glossopharyngeal function improved within the next 7 days, but Horner syndrome was still present 1 year after the intervention. Carotid body tumors are rare tumors arising from extra-adrenal chromaffin cells; however, they are the most common paragangliomas in the head and neck.14Singh D. Pinjala R.K. Reddy R.C. Satya Vani P.V. Management for carotid body paragangliomas.Interact Cardiovasc Thorac Surg. 2006; 5: 692-695Crossref PubMed Scopus (23) Google Scholar They are typically movable from side to side but not vertically downward. Because of their location, tumor enlargement often causes symptoms of dysphagia, odynophagia, and hoarseness. Computed tomography and magnetic resonance imaging are the methods of choice for diagnosis and staging. Angiography combined with embolization is predominantly used adjunctively before surgical resection, but can also be used for diagnostic purposes when the diagnosis is unclear. Because of the unpredictable malignant potential, complete resection of the carotid body tumor is always recommended. Its special anatomic position imposes great difficulty during surgery, whereby resection is technically difficult, especially in Shamblin III tumors. Therefore preoperative embolization is essential to reduce major surgical complications. Embolization reduces morbidity and mortality and shortens the time of surgery by reducing intraoperative bleeding. This was demonstrated by Vogel et al,15Vogel T.R. Mousa A.Y. Dombrovskiy V.Y. Haser P.B. Graham A.M. Carotid body tumor surgery: management and outcomes in the nation.Vasc Endovascular Surg. 2009; 43: 457-461Crossref PubMed Scopus (38) Google Scholar who evaluated 2117 patients with carotid body tumors and found significantly fewer complications and decreased blood product requirements when resection was combined with preoperative embolization. Small paragangliomas are usually easier to resect; however, no study to date has evaluated the benefits and risks of embolization according to tumor size. Embolization is usually performed through transarterial access using microparticles. Transarterial embolization does not lead to complete devascularization, however, because not all of the small feeding branches are accessible to selective microcatheterization and most embolic material remains proximal in the arterial tree. In addition, the veins draining the tumor remain patent. Direct intralesional embolization is a therapeutic alternative that was initially presented by the Lariboisière group.9Casasco A. Herbreteau D. Houdart E. George B. Tran Ba Huy P. Deffresne D. et al.Devascularization of craniofacial tumors by percutaneous tumor puncture.Am J Neuroradiol. 1994; 15: 1233-1239PubMed Google Scholar It always allows an access to the tumor and a higher degree of devascularization by occlusion of the intratumoral vessels as well as the arterial feeders and draining veins. It therefore has an important role in the embolization of large hypervascularized tumors, especially if the feeding arteries are not selectively accessible with a microcatheter, which is more frequent after previous embolization with coils or previous surgery. Direct puncture embolization has mainly been described with acrylic glue. There is growing experience in recent years with the use of Onyx, a nonadhesive liquid embolic agent, in the treatment of vascular malformations16Pierot I. Januel A.C. Herbreteau D. Barreau X. Drouineau J. Berge J. et al.Endovascular treatment of brain arteriovenous malformations using Onyx : preliminary results of a prospective multicenter study.Intervent Neuroradiol. 2005; 11: 159-164PubMed Google Scholar and in percutaneous embolization of hypervascularized tumors.17Quadros R.S. Gallas S. Delcourt C. Dehoux E. Scherperel B. Pierot L. Preoperative embolization of a cervicodorsal paraganglioma by direct percutaneous injection of onyx and endovascular delivery of particles.Am J Neuroradiol. 2006; 27: 1907-1909PubMed Google Scholar Onyx is an ethylene vinyl alcohol polymer dissolved in the organic solvent dimethyl sulfoxide (DMSO). Onyx precipitates on contact with water or blood as a result of rapid diffusion of the DMSO solvent. Animal studies have shown DMSO itself tends to be angiotoxic and neurotoxic.18Bakar B. Oruckaptan H.H. Hazer B.D. Saatci I. Atilla P. Kilic K. et al.Evaluation of the toxicity of onyx compared with n-butyl 2-cyanoacrylate in the subarachnoid space of a rabbit model: an experimental research.Neuroradiology. 2010; 52: 125-134Crossref PubMed Scopus (23) Google Scholar In the present case, we chose to use Onyx because in our experience it enables a more extensive filling with fewer punctures compared with acrylic glue. Onyx can be injected as slowly as necessary for precise delivery, and the injection can even be stopped to check the degree of embolization and be restarted later. Because it is less adhesive and polymerizes slowly, it seems to have advantages compared with NCBA. We were able to fill the entire carotid body tumor with Onyx, which led to a devascularization of the tumor and prevented significant blood loss during surgery. To our knowledge, the presented complication has not been described after Onyx embolization of a paraganglioma. In general, patients must be informed of two of its characteristics before Onyx embolization: it produces a garlic-like taste and breath odor during the first postembolization day, and emission of sparks may occur when Onyx-embolized tissue is surgically resected with monopolar electrocautery devices because of the tantalum powder content.19Katsanos K. Sabharwal T. Ahmad F. Dourado R. Adam A. Onyx embolization of sporadic angiomyolipoma.Cardiovasc Intervent Radiol. 2009; 32: 1291-1295Crossref PubMed Scopus (19) Google Scholar To prevent the risk of migration of Onyx into the internal carotid artery, a balloon was placed into the internal carotid artery during embolization. However, enoral paraesthesia, Horner syndrome, and deficits of the hypoglossal and glossopharyngeal nerves appeared with a delay of between 3 and 10 hours after Onyx embolization, which we believe was not due to direct toxicity of DMSO but to mechanical compression caused by swelling of the paraganglioma after embolization or inflammation after Onyx embolization. Although there was no evidence of nerve ischemia, ischemia, followed by reperfusion, can cause the same symptoms. Horner syndrome still remains after 1 year, although the other symptoms disappeared the first days after surgery. Preoperative direct intralesional embolization with Onyx facilitates the resection of extensive carotid body tumors because devascularization minimizes intraoperative bleeding and the Onyx cast leads to delineation against the surrounding normal tissue. However, the presented case also demonstrates potential adverse effects associated with direct intralesional Onyx injection. Owing to the delayed occurrence of these adverse effects, the optimal time of surgical intervention should be discussed and perhaps should be initiated directly after Onyx embolization.