Abstract
Background
The artery of Adamkiewicz (AKA) is vital for spinal cord blood supply. Its role in embolization procedures for bone metastases can cause serious complications. We explored its prevalence, anatomical variation, and effect on spinal embolization using N-butyl cyanoacrylate (NBCA) in patients with bone metastases.
Purpose
To understand the impact and variability of AKA in spinal embolizations in cases of bone metastases to reduce complications and improve patient outcomes.
Material and Methods
We examined data from 454 patients who underwent spinal embolization with NBCA between 2009 and 2018. The presence, anastomoses, and tumor features of AKA were assessed via pre-procedure imaging and angiography. Complications were classified per the CIRSE Classification System.
Results
AKA was found in 22.8% of patients, predominantly left-sided and originating from T8 to L1. Direct and indirect anastomoses were present in 66.6% and 33.4% of patients, respectively. Extra-compartmental invasion was linked with direct anastomosis (P = 0.004). High-grade complications were rare but included one instance of bilateral lower limb paralysis. Partial embolization was necessary in 22.8% of cases due to AKA.
Conclusion
The study underscores the need for rigorous preoperative evaluation of AKA origin and anastomoses in patients undergoing spinal embolization for bone metastases. Given the significant presence of AKA and related anastomoses, especially with renal extra-compartmental tumors, caution is advised to reduce complications and optimize patient outcomes. Further research is required for best practice guidelines involving bone metastases and AKA.
Keywords
Introduction
Spinal selective arterial embolization has emerged as an effective preoperative and palliative treatment for a variety of spinal pathologies, including vertebral hemangiomas, metastatic tumors, and aggressive benign bone tumors (1–4). The procedure aims to reduce intraoperative blood loss, alleviate pain, and improve the quality of life for patients. However, the artery of Adamkiewicz (AKA), a major spinal artery that plays a critical role in the blood supply of the spinal cord, presents a significant challenge for physicians performing embolization procedures (5–7). Anatomical variations and the presence of anastomoses between AKA and pathological vascularization of bone metastases may increase the risk of complications, including paralysis and other neurological deficits (8–10).
The AKA, also known as the great anterior radiculomedullary artery, is the largest and most significant arterial supply to the thoracolumbar spinal cord. Albert Wojciech Adamkiewicz (1850–1921), a Polish physician and pathologist, was the first to describe this critical artery, which now bears his name, in his work published in 1889. It typically arises from a segmental artery between the levels T8 and L1 and has a left-sided predominance. However, the AKA can exhibit considerable anatomical variability, making its identification during embolization procedures challenging (6,11–13). In some cases, the AKA may form anastomoses with the pathological vascularization of bone metastases, increasing the risk of serious complications if the artery is inadvertently embolized (7).
Understanding the anatomical characteristics of AKA and its anastomoses with pathological vascularization is critical for the safe and effective performance of spinal selective arterial embolization. Previous studies have reported on the incidence and location of AKA and its anastomoses in small patient cohorts (5–8). However, there is a lack of data from larger series that could provide more comprehensive information on the prevalence and distribution of these important anatomical features (9,14–16).
The aim of the present study was to present the largest series in the literature about the evaluation of AKA before embolization procedures in spinal surgery for preoperative or palliative treatments. We aim to provide valuable information on the anatomical variability of AKA and the presence of anastomoses with pathological vascularization, which can help minimize the risk of complications and improve patient outcomes during embolization procedures. Furthermore, we discuss the potential limitations of the embolization procedure in the presence of AKA and its anastomoses and propose recommendations for future research in this area.
Material and Methods
Study population and design
This retrospective study included 454 patients who underwent spinal selective arterial embolization procedures with N-butyl cyanoacrylate (NBCA) (Glubran2; GEM, Viareggio, Italy) between January 2009 and December 2018. The study population consisted of patients with spinal bone metastases from various primary tumors. The patients were treated at a single tertiary care center, and all procedures were performed by experienced interventional radiologists. The study was approved by the institutional review board (approval number: AVEC/503/2019/Oss/IOR) and the need for informed consent was waived.
Preprocedural evaluation and embolization procedure
Before the embolization procedure, all patients underwent diagnostic selective catheter angiography of the metameric arteries of the affected level, including one level above (cranial) and one level below (caudal) the lesion to evaluate the pathological vascularization, identify the presence of AKA, and assess significant anatomical anomalies and anastomoses. (Fig. 1). Preprocedural diagnostic imaging evaluation, including computed tomography (CT) or magnetic resonance imaging (MRI), was performed to evaluate tumor histology and determine the presence of extra-compartmental tumor invasion (exceeding the bone edges).
Graphic representation of the possible origin of AKA (the green area of the vessels represents the embolized area if the embolic material is injected from the tip of the arrow). (a) Direct origin from the intercostal or lumbar artery; (b) origin from the contralateral intercostal or lumbar artery and vascularized through anastomotic circles; (c) origin from the homolateral or (d) contralateral intercostal or lumbar artery from an adjacent level (inferior or superior) through anastomotic circles. AKA, artery of Adamkiewicz.
The angiographic technique consisted of a standardized selective procedure performed under local anesthesia using the Seldinger technique through common femoral artery transarterial catheterization. Diagnostic digital subtraction angiography was carried out to map the vascularization and identify pathological tumor vessels. After the diagnostic phase, selective and superselective arteriography was performed to visualize the tumoral feeding vessels and the AKA. The embolization procedure was then carried out using NBCA mixed with lipiodol, injected under fluoroscopic guidance.
Data collection and analysis
Data on patient demographics, tumor histology, presence and location of AKA, type and extent of anastomoses, embolization technique (complete or partial), and early and late complications were collected and analyzed. The completeness of embolization was defined as complete (all levels embolized) or partial (only some levels embolized due to the presence of AKA or anastomoses). Complications were classified according to the CIRSE Quality Assurance Document and Standards for Classification of Complications: The CIRSE Classification System (17).
A statistical analysis was performed using appropriate descriptive statistics, including means, ranges, frequencies, and percentages. Comparisons between groups were made using chi-square or Fisher's exact tests for categorical variables, as appropriate. A P value <0.05 was considered statistically significant.
Results
Patient characteristics and angiographic findings
A total of 454 patients (202 men, 252 women; mean age = 58.7 years; age range = 28–82 years) were included in this study. Diagnostic angiography was successfully performed in all patients, without any complications during the common femoral artery access procedure. The presence of AKA was identified in 103/454 (22.8%) patients. The AKA was more frequently observed on the left side (71/103 cases, 69%) than on the right side (32/103 cases, 31%). In terms of origin, AKA arose from a thoracic vessel in 65/103 (62.8%) cases and from a lumbar vessel in 38/103 (37.2%) cases. Fig. 2 provides detailed information on the emergence of the AKA.
A 60-year-old woman with vertebral metastasis in L4 from kidney cancer. (a) Unsubtracted and (b) digitally subtracted anteroposterior angiography of the left 4th lumbar artery with AKA (arrowhead) originating at the same level homolateral (asterisk) and (c) lateral view (arrowhead). AKA, artery of Adamkiewicz.
Visualization of AKA and anastomoses
Direct visualization of AKA was achieved in 69/103 (66.6%) cases, while indirect visualization through anastomotic circulation was observed in 34/103 (33.4%) cases. Anastomoses were found to be transverse, connecting with a contralateral intercostal or lumbar artery, in 10/34 (30%) cases, and longitudinal, connecting with an immediately adjacent intercostal or lumbar artery, in 24/34 (70%) cases. Single, double, and triple anastomoses were visualized in 18/34 (53%) cases, 9/34 (27%) cases, and 7/34 (20%) cases, respectively.
Tumor histology and vascularization
Table 1 summarizes and correlates histological data with vascularization patterns. Direct anastomosis was found to be significantly more common in renal cell tumors with extra compartmental invasion (P = 0.004). The AKA emerged at the level known in the literature (T8 to L1) in 59/103 (57.2%) patients. However, in 41% of the cases, the AKA originated higher than T8 or lower than L1.
Histological data, tumor invasion, and AKA.
AKA, artery of Adamkiewicz.
Embolization outcomes and complications
Only 1 (0.9%) case with a low risk of embolic agent reflux was embolized among patients with AKA, without any complications. Early complications were encountered in a few cases: 1 (0.2%) patient experienced complete bilateral lower limb paralysis (grade 5 according to the CIRSE classification system); 18 (4%) patients experienced leg paraesthesia (grade 2 complication) that resolved completely within one month; and 1 (0.2%) patient experienced the rupture of the third lumbar artery, which was managed successfully with immediate embolization and occlusion of the artery. A total of 278/454 (81.2%) patients experienced grade 1 complications (post-embolization syndrome).
Among the 454 patients, 14 (3%) did not have any pathological vascularization and were not submitted to embolization. In 337/454 (74.2%) patients, the AKA was not found, and all of them underwent successful complete embolization. Partial embolization was performed in 103/454 (22.8%) patients (Figs. 3 and 4).
A 67-year-old woman with vertebral metastasis in T12 and L1 from kidney cancer. (a) Digitally subtracted and (b) unsubtracted anteroposterior angiography of the left 1st lumbar artery demonstrating a hypervascular area in the region occupied by the metastatic lesion and AKA (arrowhead) originating from T12 (asterisk) through anastomotic circulation between the left 1st lumbar artery and the homolateral 12th intercostal artery. AKA, artery of Adamkiewicz.
Level of the emergence of the AKA for each patient. AKA, artery of Adamkiewicz.
Discussion
To the best of our knowledge, this study represents the largest series in the literature on AKA evaluation before embolization procedures in spinal surgery for preoperative or palliative treatments. Our findings support the existing literature regarding the predominance of the left side for the origin of AKA (69%) and its location between T8 and L1 in 59% of cases (16,19). However, our study also highlights the anatomical variability of AKA origin, with some rare origins such as the T1, T2, and L4 levels.
The presence of anastomoses between the AKA and pathological vascularization was significantly more likely in highly vascularized tumors, such as renal cell carcinoma, and when extra-compartmental invasion was present. These factors should be carefully considered during embolization procedures to minimize the risk of complications. Our findings align with previous literature on anatomical AKA characterization, as well as CT and MRI anatomical descriptions of spinal cord vasculature (19–21). Understanding the various types of anastomoses, including transverse and longitudinal connections, is crucial for preventing serious complications in patients undergoing embolization.
Matsuda et al. (15) reported a significantly higher incidence of temporary or permanent paraplegia in patients undergoing thoracic endovascular aneurysm repair with the closure of the intercostal-lumbar artery that supplies AKA. Some authors have suggested using evoked electrical potentials (EPM) to monitor and prevent complications during embolization of the AKA (22). Combining EPM with spinal angiography and temporary arterial occlusion may help guide decisions regarding the safety of permanent radicular artery occlusion, including the AKA. However, this study comprises a small group of patients, and thus its conclusions should be treated with caution until larger studies reinforce these observations.
Our experience is primarily based on using glue as the embolizing material, but we believe that other permanent embolizing materials may also cause serious harm to the patient if used in the presence of AKA. When performing spinal embolization for preoperative or palliative indications, the presence of AKA can limit the potential for complete embolization, possibly leading to reduced therapeutic efficacy (e.g. minimal reduction of bleeding or pain). The efficacy of this approach should be confirmed with a well-designed scientific trial.
In our series, we encountered a single high-grade complication (complete bilateral lower limb paralysis) due to an aberrant vascular anastomosis between AKA and pathological feeding vessels that was not clearly evident during the preliminary diagnostic angiographic evaluation.
In conclusion, while NBCA embolization is recommended as a palliative treatment for bone metastases, the presence of AKA should prompt serious consideration of stopping the procedure, particularly in cases of renal extra-compartmental tumors. The anatomical variability of AKA and the potential anastomoses with pathological vascularization of bone metastases pose a high risk of serious complications.
Footnotes
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.
