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Abstract
Background/purpose Carotid body paragangliomas are rare hypervascular lesions which may benefit from preoperative devascularization to reduce intraoperative blood loss. The optimal method for devascularization of these tumors is not known. Our purpose was to evaluate the extent of angiographic devascularization and intraoperative blood loss using only ethylene vinyl alcohol copolymer (EVOH) for percutaneous glomus tumor embolization.
Methods A consecutive series of seven paragangliomas located at the carotid bifurcation were treated with percutaneous embolization with EVOH as the sole embolic agent.
Results Complete devascularization of seven paragangliomas was achieved in all cases percutaneously with only EVOH. There were no complications. The average intraoperative blood loss was 55 ml (range 15–80 ml).
Conclusions Our preliminary experience suggests that EVOH may offer a higher degree of devascularization when compared with other embolic agents. This may facilitate easier surgical resection with lower blood loss. EVOH seems to be safe when percutaneously injected as the sole embolic agent.
- Carotid body paragangliomas
- devascularization
- ethylene vinyl alcohol copolymer
- neck
- Onyx
- technique
- tumor
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Introduction
Paragangliomas, also known as glomus tumors, are rare neoplasms arising from chemoreceptor organs in blood vessels or nerves in the head and neck area.1–3 Though benign, these tumors can be locally destructive, necessitating resection.4 Given the hypervascular nature of these tumors, direct surgical resection may result in a substantial amount of bleeding.5 Therefore, transarterial particulate embolization of these lesions is often performed for curative, preoperative or palliative management. When performed preoperatively, this procedure shortens the surgical time, reduces intraoperative blood loss and reduces morbidity and mortality.6–8 However, complete devascularization of these lesions by this approach is often limited by vessel tortuosity, atherosclerotic disease, vasospasm and tiny arterial feeders. Currently, there are limited data on the use of ethylene vinyl alcohol copolymer (EVOH) (Onyx; ev3, Irvine, California, USA) for embolization of paragangliomas. We report our experience with using EVOH as the sole agent for direct percutaneous embolization of paragangliomas at the carotid bifurcation.
Materials and methods
The institutional review board at the University of Michigan, Ann Arbor, approved this study. We retrospectively reviewed the medical records for the last 20 months to obtain a consecutive series of seven carotid body paragangliomas in which EVOH was used as the sole agent for direct percutaneous embolization. Neurointerventional imaging studies, diagnostic imaging studies and reports, operative reports and medical notes from these cases were reviewed. All procedures were performed under general anesthesia with monitoring of the patients' electroencephalogram, brainstem evoked potentials and somatosensory evoked potentials.
Standard percutaneous transfemoral arterial access was established. Non-ionic contrast iodixanol (Visipaque 270; GE Healthcare, Princeton, New Jersey, USA) was used to perform diagnostic cerebral angiography. The internal carotid, external carotid and common carotid arteries were injected and angiograms obtained to identify the arterial supply and hypervascularity of the lesion. The results from the diagnostic angiograms were used to assess the feasibility of direct percutaneous embolization, to delineate the targeted neovasculature of the lesion, to evaluate for dangerous vascular collaterals to the intracranial circulation and to determine the appropriate projection required to monitor the embolization.
Lesions were punctured with a 20-gauge needle utilizing ultrasound, fluoroscopy, biplanar transarterial roadmap and bony landmarks. After puncture, the needle position was considered correct when blood reflux from the needle was slow but continuous. A gentle hand injection of iodixanol was performed to obtain a biplanar parenchymogram, which was utilized to confirm placement of the needle within the lesion, to assess the neovascular compartment of the lesion being filled by the needle position and to determine the venous drainage pattern and opacification of possible arterial feeding pedicles. Biplanar angiography was also performed to confirm that the needle was not placed through a large arterial feeder or the internal or common carotid artery. Embolization of the tumor was performed using 8% EVOH (Onyx 34). The dead space of the needle was initially primed with dimethyl sulfoxide (DMSO) and EVOH was slowly injected with a 1 ml luer lock DMSO-compatible syringe and connecting tube under continuous negative roadmap. A tap technique, which consisted of making small taps at the end of the leur lock syringe with the operator's thumb to inject at a rate of ∼0.1–0.2 ml/min, was used to ensure optimal control. Embolization was stopped for ∼2 min if non-target embolization was noted to occur. This was done to let the Onyx cast solidify. The process was repeated until EVOH penetrated the desired segment of the tumor. This technique was repeated as many times as necessary to achieve optimal devascularization of the tumor.
The technical success of the embolization procedures was determined by the degree of residual parenchymal staining of the tumors on biplanar angiography. The extent of tumor devascularization was recorded as poor (0–30%), moderate (30–70%), subtotal (70–99%) and total (100%) and reviewed by the three authors (J.G., N.C. and A.P.).
Illustrative cases
Case 1
A 39-year-old woman presented with a history of bilateral carotid body paragangliomas discovered on imaging studies to investigate bilateral neck masses (figure 1A). Initially, the left mass was resected without incidence. The right mass measured 1.6×1.5×2.3 cm and was noted to be hypervascular on angiogram (figure 1B). After a lateral parenchymogram was obtained (figure 1C), Onyx 34 was injected through the needle into the tumor to obliterate the vasculature (figure 1D). The estimated blood loss during surgical resection was noted to be 20 ml.
Patient No. 1 in table 1. (A) Axial CT of neck with contrast showing bilateral carotid body tumors. (B) Lateral right common carotid artery angiogram demonstrating a hypervascular mass splaying the carotid bifurcation. (C) Lateral parenchymogram demonstrating direct needle placement into the tumor with contrast injection showing the neovascularity of the tumor. (D) Lateral right common carotid artery angiogram after the injection of ethylene vinyl alcohol copolymer showing complete devascularization of tumor.
Case 2
A 58-year-old man presented with a history of right tinnitus and a sensation of aural fullness. Palpation of the neck revealed palpable masses bilaterally and MRI revealed bilateral carotid body tumors (figure 2A). The right-sided mass measured 1.8×2×3.1 cm and hypervascularity was demonstrated on angiogram (figure 2B). After a lateral parenchymogram was obtained, direct percutaneous embolization of the tumor was performed using 4.2 ml of EVOH (figure 2C,D). The tumor was successfully removed surgically with an estimated blood loss of 80 ml.
Patient No. 3 in table 1. (A) Coronal MRI T2 weighted image showing bilateral carotid body tumors. (B) Right common carotid artery angiogram showing a hypervascular mass at the carotid bifurcation. (C) Right common carotid artery angiogram after the injection of ethylene vinyl alcohol copolymer showing complete devascularization of the mass. (D) Lateral spot fluoroscopic image showing the ethylene vinyl alcohol copolymer cast within the tumor.
Results
A total of seven patients with carotid body paragangliomas were treated with direct percutaneous embolization with only EVOH (table 1). There were four men and three women with a mean age of 47 years (range 18–69 years). Complete devascularization of all seven paragangliomas was achieved using a direct percutaneous embolization technique with EVOH as the sole agent. An average of 3.4 needles (range 2–6) were placed into each tumor under ultrasound, fluoroscopy, biplanar transarterial roadmap and bony landmarks. The mean duration of the total Onyx injection time was 23 min (range 15–35 min). An average of 8.7 ml (range 4.2–18.0 ml) of EVOH was injected into each tumor. Total (100%) devascularization was achieved in each case as assessed by angiography and reviewed by three of the authors (J.G., N.C. and A.P.). Surgical resection was performed 24 h after the embolization.
Results summary of carotid body paragangliomas devascularized using direct percutaneous injection with EVOH as the sole embolic agent
Three Ear Nose and Throat surgeons reported the effectiveness of preoperative devascularization as excellent in all seven cases based on personal communication and procedure records. One surgeon commented that he lost more blood from the skin incision than from removal of the tumor. Another commented that the surgical resection was one of the easiest he had encountered in his 15-year career. The average intraoperative blood loss was 55 ml (range 15–80 ml). They reported encountering minimal or no bleeding from the tumor bed intraoperatively, which greatly improved resection time, blood loss and visualization of the lesion margins. Because EVOH contains tantalum, it was particularly helpful at demarcating the pathologic margins of the tumor for the surgeon.
Minimal non-target embolization was seen in all seven cases. This was usually into the small arteries surrounding the tumor or into the adjacent soft tissue plane. This occurred near the end of the procedure when the tumor was nearly filled with Onyx. When this did occur we waited 2 min to let the Onyx further solidify before restarting the injection. If Onyx infiltrated the soft tissue plane the injection was stopped and the needle repositioned. No patient experienced non-target embolization into the intracranial circulation. There were no major or minor clinical complications from the direct percutaneous embolization technique.
Discussion
Carotid body paragangliomas, though generally benign, require treatment, as they can be locally destructive. Surgical excision is challenging as these tumors are usually hypervascular and can result in high intraoperative blood loss. While preoperative transarterial embolization has been shown to be beneficial, the extent of devascularization can be limited due to atherosclerosis, arteriovenous shunting, vasospasm and tiny arterial feeders. A combined approach utilizing direct percutaneous and intra-arterial particulate embolization has been shown to overcome this limitation to some extent. There are several studies in the literature showing the safety and efficacy of direct percutaneous liquid embolic material (traditionally acrylic glue) combined with endovascular particulate embolization in devascularization of several types of hypervascular head and neck lesion. In one of the larger case series Chaloupka et al,9 in 24 cases of hypervascular head and neck tumors demonstrated total or near-total devascularization with a combination of direct percutaneous injection of glue and transarterial embolization in 83% of the cases with no serious complications.
Percutaneous embolization alone with modified acrylic glue has also been shown to be equally effective in achieving a high degree of tumor devascularization. Abud et al10 demonstrate that direct percutaneous embolization could be performed in head and neck paragangliomas utilizing modified acrylic glue with a high degree of effectiveness and technical success. In this series, seven of the 10 patients needed three or fewer punctures. We needed three or fewer punctures in four of the seven patients treated.
The tumor penetration of the modified acrylic glue via the percutaneous needle has some limitations. The instant polymerization on contact with blood and the adhesive nature of the modified acrylic glue prevents uniform and controlled penetration of the tumor vasculature. Furthermore, theoretically, given the instant polymerization, multiple needles may be needed to access different aspects of the lesion to ensure near-total devascularization. This can be challenging in a large tumor. Based on our experience with direct percutaneous injection of both acrylic glue and Onyx into tumors we have noticed a decrease in the number of needles placed with the use of Onyx.
A relatively new liquid embolic material (EVOH) has been successfully utilized for endovascular embolization of cerebral arteriovenous malformation and arteriovenous fistulae. It has gained favor as the preferred liquid embolic agent for endovascular embolization due to its properties of cohesive polymerization on contact with blood with a non-polymerized inner core (promoting ‘lava-like flow’) that can then be directed into the tumor vasculature in an antegrade fashion. Hence, it is not surprising to find case series in the literature demonstrating its use as an alternative to modified acrylic glue in combination with particulate endovascular embolization of carotid body tumors. Quadros et al11 reported a single case of a cervicodorsal paraganglioma successfully treated by direct percutaneous injection of EVOH combined with endovascular delivery of particles. We have also recently described our preliminary experience with 15 hypervascular tumors of the head and neck that underwent direct percutaneous embolization utilizing EVOH in conjunction with intra-arterial embolization of particulate material.12
More recently, there have been case reports in the literature of complete devascularization of carotid body tumors utilizing only percutaneous embolization with EVOH. Elhammady et al13 reported the first case of a carotid body tumor effectively devascularized by direct percutaneous embolization with EVOH only. In addition, in a larger case series Wanke et al14 have also reported complete devascularization of six carotid paragangliomas in four patients utilizing direct percutaneous embolization of EVOH as the sole embolic agent. At the time of preparation of this article, our series of seven patients is the largest to date.
Wanke et al14 in their series, advocate routinely inflating a balloon in the origin of the internal carotid artery (ICA) to prevent non-target embolization. Although small, in our series we did not encounter non-target embolization without the use of the balloon in the ICA. We thought that the balloon might increase the complexity of the case and subject the patient to the possibility of additional risk. Given that some of our injections were performed spanning several minutes, sustained inflation of the balloon over long periods of time would have been required in the ICA, thereby subjecting the patient to additional risk of dissection or thromboembolic events. Given the lava-like flow and very slow controlled injection rate of EVOH, we thought that this was unnecessary.
We hypothesize that EVOH has some physical characteristics that make it a safe and effective embolic agent for more uniform and controlled percutaneous tumor penetration. EVOH is a liquid embolic agent consisting of EVOH dissolved in various concentrations of DMSO with tantalum powder. When the polymer initially contacts an aqueous medium it precipitates within the peripheral portion of the blood vessel, with the inner central portion remaining in a liquid state (allowing lava-like flow). Theoretically, this may allow a longer more controlled injection with better penetration of the vascular bed, when compared with other liquid embolic agents such as acrylic glue that polymerize immediately on contact with blood. Additionally, the characteristics of the material allow the operator the ability to stop the injection and then restart it to prevent non-target embolization with EVOH. The operator can perform angiography during the embolization to ensure progressive tumor devascularization. Large tumors can be potentially completely devascularized from a single percutaneous needle position.
The development of high-quality biplanar fluoroscopy has markedly improved the visualization of liquid adhesives during their injection, and it has increased the safety and efficacy of direct percutaneous techniques. Nevertheless, potentially dangerous external carotid artery (ECA–ICA and ECA–vertebral artery) anastomoses should always be considered and meticulously looked out for during intralesional injection, to prevent adverse events due to non-target EVOH migration.
Surgery of a carotid body tumor after an intralesional injection of EVOH appears to differ from that after transarterial embolization. Resection is facilitated because intraoperative bleeding is decreased and also because the tumor is transformed into a spongy avascular mass that is well delineated against the surrounding normal tissue by the tantalum within the EVOH. These advantages allow en bloc removal of the tumor.
We feel the radiation time to devascularize a tumor via a direct percutaneous approach is less than with particulate material. Our room time can be up to 3½ h, with >60 min fluoroscopy time utilizing particulate material, depending on how many arterial feeders supply the tumor. In our seven cases with direct percutaneous injection of EVOH, fluoroscopy time was on average 23 min with the longest duration being 35 min. The long fluoroscopy times reported with the intra-arterial injection of EVOH do not hold true for the percutaneous approach. With the direct percutaneous approach there is no need to spend considerable time forming the arterial plug, and stopping and starting multiple times to make the EVOH penetrate the desired vascular territory. We have also noticed a decrease in the amount of blood loss during surgical resection from this direct percutaneous approach. This technique therefore could possibly decrease the patient's risk of radiation-induced cancer, the surgical morbidity of the tumor resection and the risk of blood-borne disease from a transfusion.
The cost of utilizing EVOH to devascularize a tumor is high. On average a total of nine vials of EVOH was need to devascularize a tumor. Each vial of EVOH is US$2100; the total cost is roughly $18 900. If the tumor were embolized with particulate material it would require a guide catheter, two microwires, two microcatheters and roughly three vials of particles and ∼10–15 pushable/detachable coils. The total cost estimate is $4300 with pushable coils and $16 700 with detachable coils. If we save 1½ h of room time in the fluoroscopy suite ($3000) and 1½ h in the operating theater ($6000), and require no blood transfusions, the costs are about two times greater with Onyx than with pushable coils.
There are several limitations to our study. The relatively small number of patients makes generalization to a larger cohort of patients very difficult. All tumors were embolized with only EVOH, therefore a direct comparison between particulate material and modified acrylic glue cannot be made about which agent is most effective. Moreover, surgical time, blood transfusion requirements and a cost-effectiveness comparison cannot be made between this technique and using particulate material and acrylic glue.
There is a limited amount of data in the literature regarding the use of EVOH as sole agent in direct percutaneous embolization of carotid body paragangliomas. Our study, while consisting of a small cohort, offers additional data on the effectiveness and safety of such a procedure. Future studies should directly compare percutaneous embolization with only EVOH to traditional intra-arterial particulate embolization in the pre-operative devascularization of carotid body paragangliomas.
Conclusion
Direct percutaneous intratumoral embolization with EVOH as the sole approach for presurgical tumor devascularization is safe and feasible. Our preliminary experience suggests that EVOH may offer a higher degree of devascularization when compared with other embolic agents. This may facilitate a less challenging surgical resection with less intraoperative blood loss.
Key messages
Carotid body paraganglioma is a rare hypervascular lesion that may benefit from preoperative devascularization to reduce intraoperative blood loss.
Preoperative transarterial embolization of a carotid body paraganglioma has been shown to be beneficial in reducing intraoperative blood loss; however, the extent of devascularization with this technique can be limited.
Complete preoperative devascularization of a carotid body paraganglioma was achieved in all cases percutaneously with only EVOH.
The average intraoperative blood loss was 55 ml with no complications.
Percutaneous embolization with EVOH may offer a higher degree of devascularization when compared with other embolic agents.
References
Footnotes
Competing interests None.
Patient consent Obtained.
Ethics approval This study was conducted with the approval of the IRB retrospective study.
Provenance and peer review Not commissioned; externally peer reviewed.