Spinal tumor embolization with Onyx: A systematic review and meta-analysis

Abstract

Introduction

Onyx embolization has emerged as a promising technique for spinal tumor embolization due to its high devascularization rate and low incidence of complications.

Objective

Evaluate the safety and efficacy of Onyx embolization in spinal tumor procedures.

Methods

Following the PRISMA guidelines, we conducted a systematic review and meta-analysis. To be included, the articles had to report specific outcomes of Onyx embolization for spinal tumors (complications, mortality, blood loss, tumor devascularization, or reduction in tumor blush).

Results

We selected 11 out of 2941 articles, encompassing 127 patients. Among them, no major complications or persistent neurological deficits were reported, and no deaths occurred as a result of the embolization procedure. Of the 63 patients with available data, two complications were observed: one infarct leading to transient neurological deficit and one clinically silent vessel perforation related to the microcatheter. Thus, the complication rate was 1% (95% confidence interval (CI): 0% to 6%). Blood loss during surgery ranged from 100 to 1500 mL (four studies). Complete tumor blush reduction was achieved in 52% of the cases (95% CI: 16% to 88%) across 32 patients. Three studies reported a median percentage of tumor devascularization of 91% (86.1% to 97.5%).

Conclusion

Onyx embolization for spinal tumor procedures appears to be a safe technique, as evidenced by the absence of major complications or deaths. However, the determination of its efficacy remains challenging due to limited data availability and substantial heterogeneity across studies. These findings highlight the need for future research to address this knowledge gap and further validate our results.

Keywords

Onyx EVOH spine embolization neuroendovascular

Introduction

Bone metastases and primary spinal tumors can lead to significant blood loss during open surgery, particularly due to intraoperative bleeding, which is a notable concern when operating on those tumors.¹ The primary objective of surgical intervention for symptomatic metastatic lesions is to enhance quality of life, retain neurological function, establish mechanical spinal stability, and in some instances, obtain diagnostic tissue for further therapeutic measures.² In primary spinal tumors, there is a clear benefit of “en bloc” resections with free margins, a highly demanding and risky procedure. In these cases, controlling bleeding is an important part of both surgical planning and the surgical procedure.³

Given the potential complications associated with these scenarios, prior to surgery, embolization of these lesions can effectively reduce intraoperative blood loss and subsequently ease the process of surgical resection.⁴ Preoperative tumor embolization aims to achieve multiple goals, including diminishing intraoperative blood loss, managing tumor-related bleeding, and administering chemotherapy through intra-arterial routes.⁵

Since its inception in the 1970s, endovascular embolization has evolved into a crucial component within the comprehensive strategy for managing highly vascular spinal tumors.⁶ Onyx is one of the most useful tools in embolization scenarios, upon injection into the bloodstream, the substance gradually dissipates. This unique process results in the creation of a soft and pliable nonadherent mass. This mass is highly effective at achieving permanent occlusion of blood vessels, contributing to reducing the blood flow.⁷

Considering this topic and the lack of studies to establish it clearly, we aimed to perform a systematic review of the management regarding spinal tumors and spinal metastases with Onyx.

Methods

Eligibility criteria

Inclusion in this meta-analysis was restricted to studies that met all the following criteria: (1) randomized and nonrandomized studies; (2) report spinal tumor and metastasis embolization using Onyx; (3) patients who were submitted to preoperative embolization; (4) studies that report one of the interest outcomes; (5) studies reporting two or more patients. We excluded non-English papers, reviews, letters to the editor, abstracts, and commentaries from the initial assessment.

Search strategy and data extraction

We systematically searched for Onyx embolization for spinal tumors on PubMed, Cochrane, Web of Science, and Embase databases with terms associated with “onyx”, “spine tumor”, “metastasis”, “spine metastases”, “care”, “preoperative care”, “therapy”, “safety”, “efficacy”, “effectiveness”.

Nonrandomized studies compound our sample due to the lack of randomized controlled trials on this topic. The references from all included studies, previous systematic reviews, and meta-analyses were also searched manually for any additional studies. Two authors (LBO and FFA) independently extracted the data following predefined search criteria.

Statistical analysis

This systematic review and meta-analysis were performed following the Cochrane Collaboration and the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) statement guidelines. Proportion rate with 95% confidence intervals (95% CI) was used to compare outcome treatment effects. I² statistics was used to assess for heterogeneity and I² < 35% were considered significant for heterogeneity. R Studio was used to perform data analysis.

Results

Study selection

We found 2941 articles, 837 in PubMed, 1506 in Embase, 13 in Cochrane databases, and 585 in Web of Science. A total of nonduplicate citations were screened, and after a thorough review, 2175 articles were excluded per title or abstract screen, and 52 articles were selected after reading the abstract for a full-text review. Next, 41 articles were excluded after full-text screen and data extraction. Finally, 11 studies were included in the final analysis, comprising 127 patients. The search is described in Figure 1.

Baseline characteristics of included studies

The meta-analysis analyzed data from 11 studies comprising a total of 127 patients were included in the analysis. Of the 11 studies included, 6 were retrospective, 2 were prospective, and 3 were case reports. The average age of the patients at diagnosis was 44.69 years, as reported in 8 studies. The distribution of patients by sex showed no significant difference, with 38 males and 14 females reported among 7 studies.

Table 1 provides an overview of the key patient characteristics observed, including the mean age of the patients, follow up, sex, and lesion.

Table 1.

Characteristics of the studies, in terms of number of patients, length of follow up, age, sex, and type/topography of lesions.

Study (year)	Number of patients	Follow up (months)	Age (years)	Sex (M :F)	Lesions	Levels
Ashour (2012)⁸	17	6	12,8 (Pediatric)	16 : 1	Aneurysmal bone cyst (3); sacral giant cell tumor (1) NA (13)	NA
Awad (2015)⁴	29	NA	NA	NA	NA	NA
Clarençon (2013) ⁹	2	14,5 (11–18)	45,5 (36–55)	0 : 2	Hypervascular spinal metastases of the posterior arch that were in proximity to the ASA (2)	C (1) T (1)
Elhammady (2010) ¹⁰	9	NA	43,7 (9–68)	7 : 2	C1–2 hemangioblastoma; cervicomedullary hemangioblastoma; T7–10 RCC metastasis; L2 body chondrosarcoma; T-12 vertebral hemangioma; L2 ABC; L3 RCC metastasis; C3–4 intramedullary RCC metastasis; C2 ABC	C (5) T (2) L (3)
Ghobrial (2013) ²	16	3	60,4 (42–80)	10 : 6	Carcinoma, indet.; thyroid CA (2); renal cell CA (10); plasmacytoma; hemangioblastoma; nonsmall cell lung cancer	NA
Gore (2008)¹¹	4	NA	45, 75 (38–60)	2 : 2	Giant cell; renal cell CA; follicular thyroid; hemangioblastoma	C (1) T (1) L (2)
Grandhi (2015)⁷	5	NA	51,4 (13–77)	NA	Plasma cell myeloma; renal cell carcinoma (2); multiple myeloma; osteosarcoma	C (2) T (2) L (1)
Hurley (2008)¹²	2	0	35 (29–41)	1 : 1	Aggressive vertebral hemangiomas	T (1) L (1)
Ladner (2014)¹	11	0	NA	NA	Peripheral nerve sheath tumor; hemangioma (2); RCC met (4); nonsmall cell lung cancer met; pheochromocytoma met; thyroid met; ABC	T (9) L (1) S (1)
Rangel-Castilla (2012)⁶	30	NA	NA	NA	Giant cell tumor of bone (5); renal carcinoma (10); Ewing sarcoma (3); osteoblastoma; osteosarcoma (2); poor differentiated carcinoma; thyroid carcinoma (5); hepatic carcinoma; hemangioma (2); multiple myeloma; hemangioblastoma	C (10) T (14) L (6)
Sedora-Roman (2013)⁵	2	0	63 (52–74)	2 : 0	Vertebral hemangioma (1); renal cell carcinoma vertebral body metastatic lesion (1)	T (1) L (1)

ABC: aneurysmal bone cyst; ASA: anterior spinal artery; C: cervical; C + number: cervical vertebrae; CA: carcinoma; L: lumbar; L + number: lumbar vertebrae; NA: not available; RCC: renal cell carcinoma; S: sacral; T: thoracic; T + number: thoracic vertebrae. .

Procedures characteristics

Most studies used Onyx 18, with Onyx 34 also being used in some cases. The volume of Onyx used ranged from 0.44 to 5.5 mL on average. Additionally, eight studies reported that the average use of coils was approximately two. Among these studies, five did not use n-butyl cyanoacrylate (N-BCA), while another study used four N-BCA. The distribution of spinal levels was examined in 8 studies, revealing a varied pattern: 28.7% at the cervical level, 47% at thoracic levels, 22.7% at lumbar levels, and a singular case (1.6%) at the sacral level. The range of pedicles embolized fluctuated between 1 and 5, with a median of 2.6 pedicles embolized per procedure. Notably, the identification of the Adamkiewicz artery before the procedure was documented in only 2 studies,^1,12 and in 30% of the cases, no such identification was reported. More information about the different lesions presented by the patients in their respective studies will be provided in Table 2. Table 2 presents a summary of the main Onyx volume, Onyx type, coil, N-BCA, as well as mortality.

Table 2.

Details of the embolization procedure and morbidity/mortality.

Study	Onyx volume	Onyx type	Coil	N-BCA	Average number of pedicles embolized (range)	Adamkiewicz artery identification	Blood loss during surgery
Ashour⁸	NA	NA	2	4	NA	NA	NA
Awad⁴	NA	NA	NA	NA	NA	NA	NA
Clarençon⁹	5.5 mL (5–6)	Onyx 18 (2)	1	0	NA	NA	NA
Elhammady¹⁰	NA	Onyx 18 (NA); Onyx 34 (NA)	NA	NA	NA	NA	NA
Ghobrial²	1.86 mL	Onyx 18 (15); Onyx 34 (2)	1	0	1.8 (1–4)	NA	750 cm³
Gore¹¹	NA	NA	1	1	4.5 (4–5)	NA	NA
Grandhi⁷	NA	Onyx 18 (5)	2	NA	2.6 (2–4)	NA	NA
Hurley¹²	0.5–4.5 mL	Onyx 18 (2); Onyx 34	1	0	2 (1–3)	1/2	800 mL (1500 −100)
Ladner¹	NA	Onyx 34 (7); Onyx 18 (5)	5	0	2.8 (1–4)	7/11	1410 ± 430 mL
Rangel-Castilla⁶	NA	Onyx 18 (NA); Onyx 34 (NA)	NA	NA	NA	NA	NA
Sedora-Roman⁵	0.44 mL (0.24–0.64)	Onyx 18 (2)	0	0	1 (1)	NA	200 cm³ (100–300 cm³)

Compl.: complications; N-BCA: n-butyl cyanoacrylate; NA: not available.

Complications

The total complications rate in the majority of the studies included in this analysis was low, with only two complications seen in nine studies. The pooled analysis, using a random-effects model, yielded an overall total complication rate of 1% (95% CI 0% to 6%). Figure 2 illustrates the distribution of these total complications, showing a high level of consistency across the studies. It is also important to note that there was a low level of heterogeneity among the studies, with an I² value of 0%.

The rate of major complications of the studies included in this analysis was low. All studies did not report major complications. The collective analysis, employing a random-effects model, produced an overall major complication rate of 0% (95% CI 0% to 3%). Figure 3 depicts the distribution of these significant complications, demonstrating a strong level of consistency among the studies. Nonetheless, it's crucial to highlight that there existed minimal heterogeneity among the studies, as evidenced by an I² value of 0%.

The hemorrhagic complication rate in the majority of the studies included in this analysis was low, with only one case reported, and the pooled analysis, using a random-effects model, yielded an overall complication rate of 1% (95% CI 0% to 6%). Figure 4 depicts the spread of these significant complications, indicating a consistent pattern across the studies. And, importantly, the studies were quite uniform, with an I² value of 0%.

The occurrence of ischemic complications in most of the studies included in this analysis was infrequent, just one study reported an ischemic complication. The combined analysis, utilizing a random-effects model, generated an overall major complication rate of 1% (95% CI 0% to 6%). Figure 5 portrays the distribution of these significant complications, revealing a strong level of uniformity among the studies. Furthermore, it's noteworthy that there existed a limited amount of heterogeneity among the studies, with an I² value of 0%.

Mortality

The mortality rate in the collective analysis showed no one case, employing a random-effects model, produced an overall major complication rate of 0% (95% CI 0% to 3%). Figure 6 depicts the distribution of these mortality cases resulting from the embolization procedure. There was a low level of heterogeneity among the studies, with an I² value of 0%.

Tumor devascularization

The total tumor devascularization rate was reported in 5 studies and showed a rate, using a random-effects model, of 52% (95% CI 16% to 88%). Figure 7 illustrates the distribution of these patients with tumor devascularization, showing a low level of consistency across the studies. There was a high level of heterogeneity among the studies, with an I² value of 90%.

Discussion

The use of preoperative embolization has gained significant attention as a valuable adjunct in the management of spinal metastases, particularly for hypervascular tumors.^13–17 The primary goal of preoperative embolization is to reduce intraoperative blood loss, decrease operating time, and facilitate surgical resection.^18,19 Different embolic agents and techniques have been employed to achieve this goal. Notably, the application of Onyx embolization has emerged as a promising approach to enhance the effectiveness of preoperative embolization for spinal metastases. In that context, the present study conducted a systematic review and meta-analysis to assess the safety and efficacy of Onyx embolization for preoperative treatment of spinal tumors. The analysis included a total of 11 studies encompassing 127 patients who underwent preoperative Onyx embolization for spinal tumors. The findings indicate that Onyx embolization appears to be a safe technique, with no major complications or deaths reported as a result of the embolization procedure. Other than that, the overall complication rate associated with Onyx embolization was low, while a significant total tumor devascularization, with a rate of 52%, was also attested, which suggests a favorable profile for this procedure.

Even before angiography existed, Dawbarn was already exploring transarterial embolization for head and neck tumors, which is seen in his reports in 1904.²⁰ Nowadays, after decades of technological advance and intricate research, there are better microcatheter technology and a multitude of options in terms of embolic agents, which are divided into three categories: mechanical devices, for example, balloons and coils; particles, for example, polyvinyl alcohol (PVA), Gelfoam, and Embospheres; or liquid agents, for example, Onyx, N-BCA, and dehydrated ethanol.^11,21 The retrospective analysis by Vetter et al.²² of 38 patients with cervical spine tumors, of which 36 underwent embolization using either coils, PVA, or the both combined, with a mean intraoperative blood loss of 2.4 L for 36 patients, significantly higher than our result which ranged from 100 to 1500 mL. Similarly, Kato et al.²³ also investigated intraoperative blood loss, this time comparing an embolization group of 28 patients that used PVA, gelatin sponge, or coils, with a no embolization group of 28 patients for spinal metastasis, they average blood loss for the intervention group was 520 mL, which is closer to our results, while the average blood loss for the control group was 1128 mL (p < 0.05), showing once again the relevance of the preoperative embolization. Another expressively good result was attested by Tampieri et al.²⁴ case reports of 2 patients with large hemangioblastomas embolization with a particle-type agent, with one being cerebellar and the other being intramedullary (at T4)—both lesions were fully resected with a blood loss of 50 to 150 mL.

Other articles looked into the efficacy of liquid embolic agents. Kim et al.²⁵ reported 35 consecutive patients with central nervous system tumors that underwent preoperative embolization with N-BCA, of which only one had a normal artery inadvertently occluded by the embolization as a complication, resulting in a rate of 3%, close to our 1% finding. In their article, the mean percent of tumor embolized was 68%, significantly lower than our results, but they assert that it did not significantly correlate with blood loss. Still in the liquid agent category, Onyx 18 was being explored in 2001 by Gobin et al.²⁶ for embolization of head and neck hypervascular lesions of 18 patients, recording an average intraoperative blood loss of 354 mL for 14 patients. In a small case series by Shi et al.,²⁷ Onyx 18 was used to embolize meningiomas for delayed surgical resection, one of their cases did not need blood transfusion, other case had only minimum blood loss, while the remaining required 400 mL of blood transfusion.

Prior systematic reviews also investigated preoperative spinal tumor embolization and its impact on intraoperative blood loss, but it is important to note that these analyses did not encompass the application of Onyx as an embolic agent.^28–30 As so, comparing the results of this study with earlier meta-analyses sheds light on the evolving landscape of preoperative embolization techniques for spinal tumors, specially. Gao et al.²⁸ conducted a systematic review and meta-analysis that focused on the effectiveness of preoperative embolization in patients with spinal metastases. Their analysis included a mix of hypervascular and nonhypervascular tumors, and they found that preoperative embolization was effective in improving intraoperative blood loss, transfusion requirement, and operative time for hypervascular tumors. However, for nonhypervascular tumors and mixed, the evidence was limited, as it showed not statistically relevant results for these subgroups. They only included studies with control groups, which were usually sham intervention or just no intervention, but none of these studies used Onyx as an embolic agent; instead, different embolization materials were used.

Furthermore, in a previous paper by Gong et al.,²⁹ a similar systematic review and meta-analysis was presented, this time focusing on the preoperative embolization of hypervascular tumor and its determination method. Their analysis demonstrated that embolization was effective in reducing blood loss only for tumors angiographically identified as hypervascular, highlighting the importance of accurately identifying the vascular nature of the tumor for successful embolization outcomes, while tumors that were classified as hypervascular only by consensus—which was done by considering the histological findings of renal cell carcinoma (RCC), hepatocellular cancer, and thyroid cancer as hypervascular—did not show a statistically relevant result, and that was also attested for both angiographically and by consensus groups combined. This finding resonates with the current study's observation that Onyx embolization can provide effective tumor blush reduction, potentially leading to decreased intraoperative bleeding. Gong et al. study, as a comparative meta-analysis, only included clinical trials with control groups as well, consisting of sham intervention or no procedure, and no included trial used Onyx as an embolic agent either.

In contrast with the others meta-analysis, the systematic review by Luksanapruksa et al.³⁰ mentioned Onyx while referring to one of our included studies as a way to illustrate the promising results of evolving technologies in spinal tumor embolization in reducing intraoperative blood loss.¹ However, as all of their studies were already included in both of the aforementioned reviews, it was not included in their article selection any paper that used Onyx as an embolization material, but they innovated with an analysis discerned by the histological finding. Their analysis favored embolization for mixed tumor histology, while, for RCC and for mixed and RCC combined, their results were not statistically relevant.

This comment regarding Onyx embolization by Luksanapruksa et al.³⁰ highlights the importance of our systematic review for establishing more impactful evidence for the use of this promising embolic agent, especially by being the first to do so. Thereupon, in the context of earlier research, the current study provides valuable insights into the role of Onyx embolization as a preoperative technique for spinal tumor treatment. The use of Onyx as an embolic agent has gained traction in recent years, and its application for spinal tumors is supported by evidence of effective tumor devascularization and reduced intraoperative blood loss. The analysis of the included studies revealed that Onyx embolization resulted in a median percentage of tumor devascularization of 91%, which was revealed using data available in three different articles.^1,2,7 These findings suggest that Onyx embolization can play a significant role in preparing patients for safer and potentially more efficient surgical procedures, which perhaps makes it the future for preoperative spinal tumor embolization. Other than that, embolization with liquid agents has also been presented as a stand-alone treatment for spinal aneurysmal bone cyst, as seen in the case report by Doss et al., where after a N-BCA and a subsequent Onyx 18 embolization, the patient had become completely asymptomatic.³¹ In addition to its application in spinal tumors, Onyx has demonstrated utility in diverse contexts, including arteriovenous malformations, arteriovenous fistulas, and intracranial tumors.^32–34 A recent systematic review and meta-analysis specifically investigated the use of the Onyx agent in the pre-embolization of intracranial meningioma resection. The review's findings emphasized not only low complication rates but also the successful achievement of preoperative devascularization, highlighting the potential advantages of incorporating Onyx in the management of vascularized intracranial tumors.³⁵

Finally, the pre-embolization technique in spinal procedures has advanced not only regards embolic agents as shown previously, but simulation technologies. Zhu et al. have presented a promising software solution for addressing spinal dural arteriovenous fistula. Their study not only marks a significant step forward but also sheds light on the future possibilities in the realm of preparation techniques. With the advent of advanced tools like virtual injection software, pre-embolization techniques can be executed with enhanced safety and efficacy, with more in-depth exploration of pedicles targeted for embolization, which can contribute substantially to advancing our understanding and refining interventional neurovascular procedures in spinal tumors.³⁶

Limitations

It is important to acknowledge the limitations of the current study. The analysis is based on a relatively small number of studies and patients, indicating a need for further research with larger sample sizes to validate the findings and assess long-term outcomes. Additionally, the heterogeneity among the included studies in terms of tumor types, patient populations, and methodologies underscores the challenges in drawing definitive conclusions.

Moreover, it is important to note the lack of randomized controlled trials or even observational case-control studies in this topic. Therefore, even though the current systematic review compromises all useful scientific literature regarding spinal tumor embolization found in the selected databases, it does not achieve a high level of evidence.

Hence, as studies comparing specifically Onyx with other embolization agents, or even with no embolization are still lacking, they are still needed for stronger conclusions in this topic. Future research with larger and more standardized studies will be instrumental in establishing the true impact of Onyx embolization in improving outcomes for patients undergoing surgical procedures for spinal tumors.

Conclusion

This systematic review and meta-analysis focused on assessing the safety and effectiveness of Onyx embolization for preoperative treatment of spinal tumors. The study's findings reveal promising outcomes, with Onyx embolization demonstrating effective tumor devascularization and low intraoperative blood loss. With a total of 127 patients, our analysis suggests that Onyx embolization is a safe procedure, showing no major complications or deaths directly linked to the embolization process.

In conclusion, our study underscores Onyx embolization potential as a safe and effective approach for preoperative spinal tumor treatment. Nevertheless, the present review insists on the necessity for more rigorous research, including randomized controlled trials and comparative studies, to establish Onyx embolization's precise role and benefits in enhancing patient outcomes during spinal tumor surgeries. As embolization techniques continue to advance, Onyx holds promise as an essential tool, requiring continued exploration to fully comprehend its impact on patient care.

Footnotes

Authors’ contribution

The authors confirm contribution to the paper as follows: study conception and design were by SB, RB, and DGQ. Data collection, analysis and interpretation of results and draft manuscript preparation were by LBO, FFA, MPS, GMS, LBP, SB, and LVA. All authors reviewed the results and approved the final version of the manuscript.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article

ORCID iDs

Leonardo de Barros Oliveira

Livia V de Abreu

References

Ladner

Lakomkin

, et al. Minimizing bleeding complications in spinal tumor surgery with preoperative Onyx embolization via dual-lumen balloon catheter. J Neurointerv Surg 2016; 8: 210–215.

Ghobrial

Chalouhi

Harrop

, et al. Preoperative spinal tumor embolization: an institutional experience with Onyx. Clin Neurol Neurosurg 2013; 115: 2457–2463.

Boriani

. Resection in the spine: a procedure of surgical oncology. J Spine Surg 2018; 4: 668–676.

Awad

A-W

Almefty

Ducruet

, et al. The efficacy and risks of preoperative embolization of spinal tumors. J Neurointerv Surg 2016; 8: 859–864.

Sedora-Roman

Gross

Reddy

, et al. Intra-arterial Onyx embolization of vertebral body lesions. J Cerebrovasc Endovasc Neurosurg 2013; 15: 320–325.

Rangel-Castilla

Shah

Klucznik

, et al. Preoperative Onyx embolization of hypervascular head, neck, and spinal tumors: experience with 100 consecutive cases from a single tertiary center. J Neurointerv Surg 2014; 6: 51–56.

Grandhi

Hunnicutt

Harrison

, et al.

Comparing angiographic devascularization with histologic penetration after preoperative tumor embolization with Onyx: what indicates an effective procedure?

J Neurol Surg A Cent Eur Neurosurg 2015; 76: 309–317.

Ashour

Aziz-Sultan

Soltanolkotabi

, et al. Safety and efficacy of Onyx embolization for pediatric cranial and spinal vascular lesions and tumors. Neurosurgery 2012; 71: 773–784.

Clarençon

Di Maria

Cormier

, et al. Onyx injection by direct puncture for the treatment of hypervascular spinal metastases close to the anterior spinal artery: initial experience. J Neurosurg Spine 2013; 18: 606–610.

10.

Elhammady

Wolfe

Ashour

, et al.

Safety and efficacy of vascular tumor embolization using Onyx: is angiographic devascularization sufficient?

J Neurosurg 2010; 112: 1039–1045.

11.

Gore

Theodore

Brasiliense

, et al. The utility of Onyx for preoperative embolization of cranial and spinal tumors. Neurosurgery 2008; 62: 1204–1211; discussion 1211–1212.

12.

Hurley

Gross

Surdell

, et al. Preoperative Onyx embolization of aggressive vertebral hemangiomas. AJNR Am J Neuroradiol 2008; 29: 1095–1097.

13.

Robial

Charles

Y-P

Bogorin

, et al.

Is preoperative embolization a prerequisite for spinal metastases surgical management?

Orthop Traumatol Surg Res 2012; 98: 536–542.

14.

Prabhu

Bilsky

Jambhekar

, et al. Results of preoperative embolization for metastatic spinal neoplasms. J Neurosurg 2003; 98: 156–164.

15.

Olerud

Jónsson

Jr Löfberg

, et al. Embolization of spinal metastases reduces peroperative blood loss. 21 Patients operated on for renal cell carcinoma. Acta Orthop Scand 1993; 64: 9–12.

16.

Manke

Bretschneider

Lenhart

, et al. Spinal metastases from renal cell carcinoma: effect of preoperative particle embolization on intraoperative blood loss. AJNR Am J Neuroradiol 2001; 22: 997–1003.

17.

Guzman

Dubach-Schwizer

Heini

, et al. Preoperative transarterial embolization of vertebral metastases. Eur Spine J 2005; 14: 263–268.

18.

Duffis

Gandhi

Prestigiacomo

, et al. Head, neck, and brain tumor embolization guidelines. J Neurointerv Surg 2012; 4: 251–255.

19.

Gupta

Thomas

Horowitz

. Intracranial head and neck tumors: endovascular considerations, present and future. Neurosurgery 2006; 59: S251–S260; discussion S3–S13.

20.

Dawbarn

RHM

. The starvation operation for malignancy in the external carotid area. Its failures and successes. JAMA 1904; XLIII: 792.

21.

Deshmukh

Fiorella

McDougall

, et al. Preoperative embolization of central nervous system tumors. Neurosurg Clin N Am 2005; 16: 411–432, xi.

22.

Vetter

Strecker

Ackermann

, et al. Preoperative embolization of cervical spine tumors. Cardiovasc Intervent Radiol 1997; 20: 343–347.

23.

Kato

Murakami

Minami

, et al. Preoperative embolization significantly decreases intraoperative blood loss during palliative surgery for spinal metastasis. Orthopedics 2012; 35: e1389–e1395.

24.

Tampieri

Leblanc

TerBrugge

. Preoperative embolization of brain and spinal hemangioblastomas. Neurosurgery 1993; 33: 502–505; discussion 505.

25.

Kim

Albuquerque

Aziz-Sultan

, et al. Low morbidity associated with the use of NBCa liquid adhesive for preoperative transarterial embolization of central nervous system tumors. Neurosurgery 2006; 59: 98–104.

26.

Gobin

Murayama

Milanese

, et al. Head and neck hypervascular lesions: embolization with ethylene vinyl alcohol copolymer–laboratory evaluation in swine and clinical evaluation in humans. Radiology 2001; 221: 309–317.

27.

Shi

Z-S

Feng

Jiang

X-B

, et al. Therapeutic embolization of meningiomas with Onyx for delayed surgical resection. Surg Neurol 2008; 70: 478–481.

28.

Gao

Z-Y

Zhang

, et al. Effectiveness of preoperative embolization in patients with spinal metastases: a systematic review and meta-analysis. World Neurosurg 2021; 152: e745–e757.

29.

Gong

Wang

Liu

, et al. Only tumors angiographically identified as hypervascular exhibit lower intraoperative blood loss upon selective preoperative embolization of spinal metastases: systematic review and meta-analysis. Front Oncol 2020; 10: 597476.

30.

Luksanapruksa

Buchowski

Tongsai

, et al. Systematic review and meta-analysis of effectiveness of preoperative embolization in surgery for metastatic spine disease. J Neurointerv Surg 2018; 10: 596–601.

31.

Doss

Weaver

Didier

, et al. Serial endovascular embolization as stand-alone treatment of a sacral aneurysmal bone cyst. J Neurosurg Spine 2014; 20: 234–238.

32.

Khattar

Meyer

Ding

, et al. Microsurgical resection of a ruptured right peri-ventricular brain arteriovenous malformation with preoperative embolization. Interv Neuroradiol 2023: 15910199231154707.

33.

Lanzino

D'Urso

Kallmes

et al. Onyx embolization of extradural spinal arteriovenous malformations with intradural venous drainage. Neurosurgery 2012; 70: 329–333.

34.

Amuluru

Denardo

Scott

, et al. Technical video: Onyx-18 embolization of spinal epidural arteriovenous fistula using the scepter-Mini balloon catheter. Interv Neuroradiol 2022: 15910199221138633.

35.

Batista

Andreão

Palavani

, et al. Enhancing meningioma resection: a comprehensive study on the safety and effectiveness of Onyx™ presurgical embolization. Neurosurg Rev 2023; 46: 299.

36.

Zhu

Bracard

Trousset

, et al. Virtual injection software for endovascular management of spinal dural arteriovenous fistula. Interv Neuroradiol 2023: 15910199231193469.