Abstract
Although coil embolization is commonly perceived as a minimally invasive procedure, the associated radiation exposure cannot be disregarded. To date, no specific study has investigated radiation exposure during coil embolization. This study aimed to investigate the potential of lowering the pulse rate to decrease radiation exposure during coil embolization while maintaining patient safety. Radiation data and clinical features of 70 patients who underwent coil embolization between 2015 and 2020 were retrospectively analyzed. Since July 2017, the pulse rate was regulated from 7.5 to 4 frames per second (f/s). Statistical analyses were performed to examine the correlation between pulse rate and radiation exposure. Out of the 70 procedures, 30 were performed at the standard pulse rate (7.5 f/s), and 40 were performed at the lower pulse rate (4 f/s). In the lower-pulse-rate group, the absorbed dose to the patient (AK) was 2580.7 (±217) mGy, whereas in the standard-pulse-rate group, it was 4760 (±411.1). Both the dose-area product (DAP) and AK were substantially reduced in the low pulse rate group (p = 0.000002). There was a significant correlation between DAP and AK and pulse rate (p = 0.004, p = 0.0017, respectively). Moreover, there was no significant correlation between pulse rate and perioperative complications. Our findings suggest that using a lower pulse rate (4 f/s) can effectively reduce radiation exposure during coil embolization for cerebral aneurysms while ensuring patient safety.
Keywords: radiation exposure, cerebral aneurysms, coil embolization, interventional radiology
Introduction
Recent years have seen an increased demand for endovascular treatments for cerebral aneurysms. Although the physical burden of coil embolization is considered light, the associated radiation exposure should be considered.1-4) Radiation dose to patients should be kept “as low as reasonably achievable” (ALARA principle) and is one of the easiest ways to reduce the pulse rate, which can be adjusted by the surgeon without interrupting workflow.5) The optimal pulse rate for endovascular treatments remains controversial, and in the field of cardiology, there have been reports comparing 7.5 frame per second (f/s) and 4 f/s.6) However, in the field of neurosurgery, endovascular treatments are often performed at the default setting of 7.5 f/s without a thorough examination of how low the pulse rate can be set. Therefore, we have previously reported that this adjustment during carotid stenting significantly lowers radiation dosage while maintaining patient safety.7) Despite these findings, no studies have specifically focused on radiation exposure during coil embolization for cerebral aneurysms. Therefore, this study aimed to determine if lowering the pulse rate reduced radiation exposure during coil embolization while maintaining patient safety.
Materials and Methods
Patients
This historical control study involved acquisition of radiation measurements and clinical data from 70 consecutive patients who underwent coil embolization for cerebral aneurysms between November 2015 and August 2020. Beginning in July 2017, we changed the pulse rate from 7.5 to 4 f/s; all pulse rates were intraoperatively maintained. This investigation was conducted in compliance with our institutional review board's guidelines (approval no. 191295). Written consent for patient information and images to be published was obtained from all the participants.
Treatment
Several neurosurgeons evaluated all cerebral aneurysms requiring treatment to determine whether clipping or coil embolization was the preferred treatment modality. Patients with unruptured aneurysms received 2 weeks of dual antiplatelet therapy before surgery. All patients with ruptured aneurysms received intraoperative heparin. After general anesthesia, a 9 Fr-long sheath was inserted into the groin, and then an 8 Fr FUBUKI (Asahi Intec Corporation, Aichi, Japan) was placed into the internal carotid artery. If the simple technique was unable to be completed, embolization using a balloon (Scepter XC, Microvention, Aliso Viejo, CA, USA) or stent (Neuroform Atlas, Stryker, Fremont, California, USA) was performed. Postoperative MRI images were obtained within 48 h, and cerebral angiography was performed within 1 week.
Radiation exposure
All endovascular procedures were conducted using a floor-mounted C-arm (Siemens Artis-Zee BA Twin PURE). Data were collected from a summary sheet automatically generated by the Siemens software. The collected data were the total fluoroscopic time (FT), dose area product (DAP), and total air kerma (AK). Of note, FT-as reported in this study-was determined by adding the FTs measured from the front and lateral views. In addition, DAP was measured by a DAP meter attached to the collimator (DIAMENTOR K2S Type), while AK was calculated automatically by the Siemens software based on the DAP value assuming a focus-to-subject distance of 60 cm.
Clinical outcomes
To determine the safety of coil embolization under low pulse rate fluoroscopy, we collected clinical data on perioperative complications, such as the rate of complete occlusion achieved, 90-day postoperative morbidity, the incidence of procedure-associated intraoperative perforations, symptomatic infarctions, and hemorrhage. Additional data such as the number of coils used during procedures, the coil deviation rate, and rate of retreatment within 1 year were collected. We collected neurological examinations, postoperative MRI scans, and angiography reports. The total procedural duration was obtained from the medical records. Neurological signs consistent with the imaging findings were classified as “symptomatic infarction.”
Statistics
We evaluated between-group differences in radiation exposure-as measured by DAP and AK-FT, and total procedure time using pulse rates of 4 f/s and 7.5 f/s. Furthermore, Student's t-test was used to evaluate potential between-group differences in age, maximum aneurysm diameter, dome/neck ratio, and height/neck ratio.
The chi-squared test was used to evaluate the correlation between pulse rate and categorical variables such as laterality of approach, preoperative-modified Rankin Scale (mRS) score, rate of subarachnoid hemorrhage (SAH), World Federation of Neurological Surgeons grade, sex, rate of stent assistance, rate of balloon assistance, aneurysm location, and concomitant conditions such as heart disease, diabetes mellitus, hypertension (HT), and dyslipidemia (DL).
Using multiple regression, we applied a stepwise algorithm to select significant predictive predictors of DAP and AK (among pulse rate, FT, and the other variables mentioned above). A similar procedure was used to assess the combination of significant predictors of FT.
The chi-squared test was used to evaluate the correlation between pulse rate and perioperative problems, such as the complete occlusion success rate, 90-day postoperative morbidity, the incidence of symptomatic perioperative infarctions, incidence of hemorrhage, coil deviation rate, and rate of retreatment within 1 year.
All statistical analyses were performed using the Statistical Package for the Social Sciences, version 22.0 (SPSS Inc., Armonk, NY). Two-tailed p-values < 0.05 were considered statistically significant.
Results
Table 1 shows patient and procedural characteristics. Forty and 30 patients underwent coil embolization using a pulse rate of 4 f/s and 7.5 f/s, respectively.
Table 1.
Characteristics of patients in each group
| Characteristics | 4 f/s (N = 40) | 7.5 f/s (N = 30) | p-value | |
|---|---|---|---|---|
| Age, mean (SD) | 67.2 (2.4) | 68.7 (2.6) | 0.317 | |
| Male, n (%) | 11 (27.5) | 11 (36.7) | 0.414 | |
| Preoperative mRS, median (range) | 0 (0-4) | 0 (0-4) | 0.347 | |
| SAH, n (%) | 16 (40.0) | 16 (53.3) | 0.335 | |
| WFNS grade, median (range) | 4 (1-5) | 5 (1-5) | 0.780 | |
| Left approach, n (%) | 24 (60.0) | 13 (43.3) | 0.810 | |
| Retreatment case, n (%) | 5 (12.5) | 2 (6.7) | 0.690 | |
| Max diameter (mm) | 6.8 (1.3) | 6.3 (0.5) | 0.277 | |
| Dome/neck ratio | 2.1 (0.1) | 2.3 (0.2) | 0.132 | |
| Height/neck ratio | 1.8 (0.1) | 2.3 (0.2) | 0.009 | |
| Stent assist, n (%) | 16 (40.0) | 3 (10.0) | 0.027 | |
| Balloon assist, n (%) | 6 (15.0) | 6 (20.0) | 0.834 | |
| Location of aneurysm | 0.599 | |||
| Internal carotid artery, n (%) | 19 (47.5) | 13 (43.3) | ||
| Anterior cerebral artery, n (%) | 11 (27.5) | 8 (26.7) | ||
| Basilar artery, n (%) | 5 (12.5) | 7 (23.3) | ||
| Vertebral artery, n (%) | 3 (7.5) | 2 (6.7) | ||
| Middle cerebral artery, n (%) | 2 (5.0) | 0 (0) | ||
| Heart disease, n (%) | 5 (12.5) | 4 (13.3) | 0.918 | |
| Diabetes mellitus, n (%) | 6 (15.0) | 5 (16.7) | 0.850 | |
| Hypertension, n (%) | 24 (60.0) | 12 (40.0) | 0.098 | |
| Dyslipidemia, n (%) | 16 (40.0) | 8 (26.7) | 0.245 | |
| Other medical history, n (%) | 19 (47.5) | 14 (46.7) | 0.945 | |
SAH, subarachnoid hemorrhage; WFNS, World Federation of Neurosurgical Societies
Factors affecting radiation exposure
In the 4 f/s group, the mean DAP (±standard error; SE) was 15,965 (±1,046) μGym2, and the mean AK was 2580.7 (±217) mGy. In the 7.5 f/s group, the mean DAP (±SE) was 23,572 (±2,136) μGym2, and the mean AK was 4,760 (±411.1) mGy. Pulse rates of 4 and 7.5 f/s produced significant differences in DAP (p = 0.00017) and AK (p = 0.000002; Fig. 1). On multivariate analysis, pulse rate, FT, and SAH were significantly correlated with DAP; in contrast, only pulse rate was significantly correlated with AK (p = 0.004, p = 0.029, p = 0.019, p = 0.017, respectively). There were no significant correlations between DAP, AK, and the other variables (Table 2).
Fig. 1.
Comparison of the mean (±standard error; SE) of DAP and AK between the two group. In the 4 f/s group, DAP was 15,965 (±1,046) μGym2 and AK was 2580.7 (±217) mGy. In the 7.5 f/s group, DAP was 23,572 (±2,136) μGym2 and AK was 4,760 (±411.1) mGy. Pulse rates of 4 and 7.5 f/s produced significant differences in DAP (p = 0.00017) and AK (p = 0.000002).
Table 2.
The results of multivariate analysis to investigate the factor affecting DAP. Pulse rate, FT, and SAH were significantly correlated with DAP
| Univariate analysis | Multivariate analysis | 95% CI | ||||||
|---|---|---|---|---|---|---|---|---|
| p-value | B | β | p-value | Lower limit | Upper limit | |||
| DAP variable | ||||||||
| Pulse rate (4 f/s:low) | <0.001 | −6797.932 | −0.341 | 0.004 | −11311.677 | −2284.187 | ||
| Fluoroscopy time (min) | <0.001 | 150.973 | 0.402 | 0.029 | 15.968 | 285.978 | ||
| The number of AP imaging | <0.001 | −6.93 | −0.007 | 0.981 | −591.776 | 577.917 | ||
| The number of LR imaging | <0.001 | 408.832 | 0.35 | 0.251 | −300.047 | 1117.711 | ||
| The number of 3D imaging | 0.135 | 103.074 | 0.214 | 0.078 | −12.17 | 218.318 | ||
| Age (years) | 0.158 | 0.816 | 0.001 | 0.992 | −166.772 | 168.405 | ||
| Sex (male) | 0.047 | 1042.983 | 0.049 | 0.65 | −3563.225 | 5649.19 | ||
| mRS (preoperative) | 0.041 | −131.509 | −0.012 | 0.913 | −2543.735 | 2280.717 | ||
| SAH (present) | 0.489 | −9276.592 | −0.468 | 0.019 | −16917.223 | −1635.962 | ||
| WFNS grade | 0.207 | 1520.57 | 0.298 | 0.071 | −137.051 | 3178.191 | ||
| Approach side (left) | 0.214 | −335.177 | −0.017 | 0.867 | −4337.176 | 3666.821 | ||
| Retreatment case (present) | 0.447 | 4039.321 | 0.123 | 0.353 | −4645.829 | 12724.47 | ||
| Max diameter (mm) | 0.209 | 76.24 | 0.021 | 0.899 | −1131.064 | 1283.544 | ||
| Dome/neck ratio | 0.175 | 2580.227 | 0.215 | 0.185 | −1283.307 | 6443.762 | ||
| Height/neck ratio | 0.398 | −716.061 | −0.061 | 0.69 | −4312.278 | 2880.157 | ||
| Bleb (present) | 0.32 | −3357.273 | −0.168 | 0.151 | −7987.131 | 1272.585 | ||
| Location of aneurysm | 0.247 | −142.26 | −0.014 | 0.897 | −228.998 | 2054.478 | ||
| Heart disease (present) | 0.01 | 2669.481 | 0.091 | 0.367 | −3241.748 | 8580.71 | ||
| Diabetes mellitus (present) | 0.368 | −171.186 | −0.006 | 0.953 | −6040.534 | 5698.162 | ||
| Hypertension (present) | 0.222 | 3235.623 | 0.164 | 0.196 | −1729.254 | 8200.5 | ||
| Dyslipidemia (present) | 0.099 | −1776.745 | −0.085 | 0.522 | −7336.375 | 3782.884 | ||
| Other medical history (present) | 0.098 | 3506.123 | 0.177 | 0.097 | −665.209 | 7677.455 | ||
| Stent assist (present) | 0.312 | −4379.206 | −0.186 | 0.274 | −12355.411 | 3596.998 | ||
| Balloon assist (present) | 0.223 | −2341.723 | −0.089 | 0.414 | −8073.909 | 3390.463 | ||
| The number of coils | 0.001 | −67.013 | −0.035 | 0.849 | −774.942 | 640.917 | ||
| Operator | 0.157 | 1384.88 | 0.096 | 0.433 | −2146.699 | 4916.46 | ||
| Complete obliteration (present) | 0.208 | −3501.335 | −0.175 | 0.111 | −7843.159 | 840.49 | ||
Factors affecting FT
We found no significant between-group differences in FT or total procedure times (p = 0.10 and p = 0.07, respectively). In the 4 f/s group, the mean (±SE) total FT was 57.4 (±3.9) min and the mean total procedure time was 210.6 (±8.4) min. In the 7.5 f/s group, the mean total FT was 65.5 (±5.2) min and the mean total procedure time was 235 (±11.9) min. Multivariate analysis revealed that the number of 3D imaging, age, retreatment case, max diameter of aneurysms, stent assist, and operator significantly correlated with FT (p = 0.036, p = 0.005, p = 0.049, p = 0.037, p = 0.015, p = 0.014, respectively; Table 3). There were no significant correlations between FT and the other variables (Table 3).
Table 3.
The results of multivariate analysis to investigate the factor affecting AK. Only pulse rate was significantly correlated with AK
| Univariate analysis | Multivariate analysis | 95% CI | ||||||
|---|---|---|---|---|---|---|---|---|
| p-value | B | β | p-value | Lower limit | Upper limit | |||
| AK variable | ||||||||
| Pulse rate (4 f/s: low) | <0.001 | −1284.24 | −0.306 | 0.017 | −2325.79 | −242.68 | ||
| Fluoroscopy time (min) | <0.001 | 22.05 | 0.279 | 0.161 | −9.11 | 53.20 | ||
| The number of AP imaging | <0.001 | 62.37 | 0.287 | 0.356 | −72.584 | 197.325 | ||
| The number of LR imaging | <0.001 | 3.91 | 0.016 | 0.962 | −159.66 | 167.49 | ||
| The number of 3D imaging | 0.200 | −6.19 | −0.061 | 0.641 | −32.78 | 20.41 | ||
| Age (years) | 0.012 | 26.33 | 0.161 | 0.177 | −12.35 | 65.00 | ||
| Sex (male) | 0.074 | 221.96 | 0.050 | 0.676 | −840.94 | 1284.85 | ||
| mRS (−preoperative) | 0.125 | 35.81 | 0.016 | 0.897 | −520.82 | 592.43 | ||
| SAH (present) | 0.133 | 855.23 | 0.205 | 0.333 | −907.86 | 2618.32 | ||
| WFNS grade | 0.210 | −246.15 | −0.230 | 0.201 | −628.65 | 136.35 | ||
| Approach side (left) | 0.440 | 194.07 | 0.046 | 0.674 | −729.40 | 1117.54 | ||
| Retreatment case (present) | 0.409 | −197.02 | −0.028 | 0.844 | −2201.13 | 1807.10 | ||
| Max diameter (mm) | 0.108 | 4.54 | 0.006 | 0.974 | −274.05 | 283.13 | ||
| Dome/neck ratio | 0.325 | −10.22 | −0.004 | 0.982 | −901.74 | 881.30 | ||
| Height/neck ratio | 0.191 | 242.27 | 0.098 | 0.559 | −587.57 | 1072.10 | ||
| Bleb (present) | 0.259 | −716.05 | −0.170 | 0.183 | −1784.40 | 352.30 | ||
| Location of aneurysm | 0.292 | −100.68 | −0.046 | 0.691 | −607.58 | 406.23 | ||
| Heart disease (present) | 0.062 | 786.01 | 0.127 | 0.251 | −578.02 | 2150.04 | ||
| Diabetes mellitus (present) | 0.289 | −354.60 | −0.062 | 0.600 | −1708.97 | 999.76 | ||
| Hypertension (present) | 0.278 | 62.39 | 0.015 | 0.913 | −1083.27 | 1208.05 | ||
| Dyslipidemia (present) | 0.098 | −487.36 | −0.111 | 0.448 | −1770.26 | 795.53 | ||
| Other medical history (present) | 0.234 | 17.45 | 0.004 | 0.971 | −945.10 | 979.99 | ||
| Stent assist (present) | 0.448 | 132.06 | 0.027 | 0.886 | −1708.47 | 1972.58 | ||
| Balloon assist (present) | 0.480 | −189.82 | −0.034 | 0.774 | −1512.54 | 1132.89 | ||
| The number of coils | <0.001 | 43.45 | 0.108 | 0.594 | −119.91 | 206.81 | ||
| Operator | 0.134 | 32.26 | 0.011 | 0.937 | −782.66 | 847.18 | ||
| Complete obliteration (present) | 0.358 | 102.98 | 0.024 | 0.837 | −898.91 | 1104.86 | ||
Perioperative complications
Overall procedural complications occurred in 4 of 70 patients (5.71%). There were no significant between-group differences for any clinical outcome, including perioperative complication rates, for pulse rates of 4 and 7.5 f/s (Table 4). There were no procedural complications leading to death.
Table 4.
Comparison of perioperative complications between the two groups using a pulse rate of 4 f/s and 7.5 f/s. There was no significant difference in the perioperative complication rates between the two groups
| Clinical outcome | 4 f/s (N = 40) | 7.5 f/s (N = 30) | p-value |
|---|---|---|---|
| Complete occlusion, n (%) | 25 (62.5) | 19 (63.3) | 0.484 |
| 90-day morbidity, n (%) | 1 (2.5) | 2 (6.6) | 0.394 |
| Intraoperative perforation, n (%) | 0 (0) | 0 (0) | - |
| Perioperative infarction, n (%) | 2 (5.0) | 2 (6.6) | 0.766 |
| The number of coils, mean (SD) | 7.9 (0.9) | 8.5 (1.1) | 0.111 |
| Coil deviation, n (%) | 1 (2.5) | 2 (6.6) | 0.394 |
| Retreatment within 1 year, n (%) | 1 (2.5) | 2 (6.6) | 0.394 |
Discussion
With the recent development of devices, coiling is an increasingly popular treatment for cerebral aneurysms. However, at the same time, there is a growing concern over radiation exposure associated with endovascular treatments. As if to reflect the heightened concern about radiation exposure, recent instruments have been equipped with digital zoom functions to avoid increasing the magnification rate and low-dose high-equality imaging technology. Although this radiation exposure is multifactorial, the operator can adjust the fluoroscopic pulse rate.7) To our knowledge, this study is the first to examine the clinical effects of a 4 f/s pulse rate on radiation exposure and patient safety during coil embolization. Our results suggest that using 4 f/s pulse rate during the entire coil embolization procedure can significantly reduce radiation exposure while maintaining patient safety.
The deleterious effects of radiation exposure are deterministic and stochastic. Deterministic effects have a threshold dose and are characterized by the dose-related increase in severity and can be evaluated by AK.8-12) Stochastic effects have no threshold dose and linearly correlate with the amount of exposure and are evaluated using DAP.4,8,12) We were able to reduce AK effects by 54.2% in patients undergoing coil embolization by comparing pulse rates of 4 f/s and 7.5 f/s. Focusing on the average AK value, reducing the pulse rate to 4 f/s allowed us to stay below 3 Gy, which is the threshold of the deterministic effects such as transient erythema and hair loss. Since 5 Gy is the threshold for more severe skin symptoms, it can be considered useful in avoiding these deterministic effects as well. DAP effects were also reduced by 32.3% using 4 f/s. Reducing DAP directly correlates with lowering the risk of stochastic effects such as cancer and genetic abnormalities, depending on the degree of reduction. Thus, use of a low pulse rate (4 f/s) significantly reduced the risk of both deterministic and stochastic effects following coil embolization.
A recent report examined the safety of the “ultralow” pulse rate of 4 f/s during cardiovascular treatments.13) In the previous study, we report the safety of carotid artery stenting using 4 f/s.7) Similarly, we set 4 f/s as a threshold rate to ensure visibility for the coil embolization procedure (Supplement.1). This change did not produce additional complications or prolong the FT. Compared to large scale clinical studies, the procedural complication rate was comparable: Henkes et al. found a thromboembolic complication rate of 4.7% in 1,034 patients.14) Ross et al. reported that the rate of thromboembolic stroke was 6% in a series of 118 patients.15) Rooij reported that the rate of thromboembolic complications was 4.7% in 681 consecutive patients.16) In this study, thromboembolic findings were seen in 5.0% in 40 patients using 4 f/s. In addition, there was no mortality. It seems that reducing the pulse rate to 4 f/s did not significantly affect visibility, although this change did slightly decrease the “smoothness” of the device's motion. The statistical analysis results were also consistent with our clinical experience and support the validity of our results.
First, longer FTs associated with increasing age may reflect the impact of arterial stiffness on device operability. Second, naturally, larger masses likely require more procedures and longer FT. Moreover, using stents reduces the number of rewinding coils used for embolization, thus reducing FT.
This study had some limitations. First, several factors related to radiation exposure are difficult to quantify. For example, how to use fluoroscopy and how to maintain the distance between the patient and the flat panel detector depend on the operator. This study used data generated by multiple operators for the multivariate analyses; however, this may be insufficient for evaluation. Second, selection bias is likely present as this was a single center study, and clipping was the preferred treatment for some patients, especially in cases of wide-neck aneurysms. Therefore, further studies are needed to determine treatment outcomes in patients at higher risk during coiling procedures. Third, while all procedures were performed by specialists certified by the Society for Neuroendovascular Therapy under the supervision of the corresponding author, operator-specific factors-including skill-could affect treatment outcomes, complications, FT, or procedure time. This limitation is particularly relevant to the 4 f/s procedures performed in the latter half of this historical control study. Fourth, in this facility, all endovascular treatments in the latter half were uniformly conducted at 4 f/s, so all operators had adapted to this imaging speed. However, operators who were accustomed to treating at 7.5 f/s might feel a loss of smoothness when handling devices at 4 f/s at the same speed, potentially requiring a period to adjust. Finally, flow diverters, which are widely used, will likely require future validation because the technique considerably differs from that of embolization.
Conflicts of Interest Disclosure
The authors received no financial support for the research, authorship, and/or publication of this article.
Supplementary Material
Acknowledgments
T.S. and S.T. conceptualized and designed the study. All authors collected the data. T.S. analyzed the data. T.S. wrote the manuscript. S.T. and H.K. critically revised the manuscript. This work was supported by The Grant-in-aid for Community Health and Medical Care from the Osaka University Medical School Alumni.
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