Target Ultra and Nano coils in the endovascular treatment of small intracranial aneurysms (ULTRA Registry)

Gaurav JindalDepartment of Radiology, Division of Interventional Neuroradiology, University of Maryland Medical Center, Baltimore, Maryland;

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Ranyah AlmardawiDepartment of Radiology, Division of Interventional Neuroradiology, University of Maryland Medical Center, Baltimore, Maryland;

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Rishi GuptaDepartment of Neurosurgery, Wellstar Health System, Marietta, Georgia;

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Geoffrey P. ColbyDepartment of Neurosurgery, University of California, Los Angeles, California;

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Clemens M. SchirmerDepartment of Neurosurgery, Geisinger Health System, Danville, Pennsylvania;

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Sudhakar R. SattiDepartment of Neurointerventional Surgery, Christiana Care Medical Center, Newark, Delaware;

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Bryan PukenasDepartment of Radiology, Division of Interventional Neuroradiology, Hospital of the University of Pennsylvania, Philadelphia, Pennsylvania;

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Ferdinand K. HuiDepartment of Radiology, Division of Interventional Neuroradiology, and

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Justin CaplanDepartment of Neurosurgery, Johns Hopkins Hospital, Baltimore;

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Timothy MillerDepartment of Radiology, Division of Interventional Neuroradiology, University of Maryland Medical Center, Baltimore, Maryland;

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Jacob CherianDepartment of Neurosurgery, University of Maryland Medical Center, Baltimore; and

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Francois AldrichDepartment of Neurosurgery, University of Maryland Medical Center, Baltimore; and

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Gulam KibriaDepartment of International Health, Johns Hopkins School of Public Health, Baltimore, Maryland

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J. Marc SimardDepartment of Neurosurgery, University of Maryland Medical Center, Baltimore; and

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for the ULTRA Study Investigators
Open access

OBJECTIVE

The ULTRA Registry is a national multicenter prospective study designed to assess aneurysm occlusion rates and safety profiles of the Target Ultra and Nano coils in the treatment of small intracranial aneurysms (IAs).

METHODS

Patients with small (≤ 5 mm) ruptured and unruptured IAs were treated exclusively with Target Ultra and Nano coils. The primary endpoints were the initial rate of complete or near-complete aneurysm occlusion, aneurysm recurrence, and need for retreatment. Secondary endpoints were device- and procedure-related adverse events, hemorrhage from the coiled aneurysm at any time during follow-up, and clinical outcomes.

RESULTS

The ULTRA Registry included 100 patients with a mean ± SD age of 56 ± 11.6 years, of whom 75 were women and 48 presented after aneurysm rupture. The mean aneurysm size was (3.5 ± 0.9) × (2.8 ± 0.9) × (3.0 ± 1.0) mm, and the mean packing density was 34.4% ± 16.7%. Posttreatment complete or near-complete occlusion reported by an independent imaging core laboratory was seen in 92% of patients at baseline and in 87%, 87%, and 83% of patients at first, second, and final follow-up, respectively. At first, second, and final follow-up, 10%, 11%, and 15%, respectively, of patients were deemed to require retreatment. There were three procedural-related ischemic strokes and one intracranial hemorrhage from wire perforation of a parent artery not involved by the aneurysm. There were no coil-related adverse events, including no intraoperative aneurysm ruptures and no known aneurysm ruptures after coiling.

CONCLUSIONS

This assessment of aneurysm occlusion rates and safety profiles in ULTRA Registry study participants demonstrates excellent safety and efficacy profiles for Target Ultra and Nano coils in the treatment of small IAs.

ABBREVIATIONS

AE = adverse event; IA = intracranial aneurysm; IOR = intraoperative rupture; mRS = modified Rankin Scale; NIHSS = National Institutes of Health Stroke Scale; RR = Raymond and Roy; SAE = serious AE.

OBJECTIVE

The ULTRA Registry is a national multicenter prospective study designed to assess aneurysm occlusion rates and safety profiles of the Target Ultra and Nano coils in the treatment of small intracranial aneurysms (IAs).

METHODS

Patients with small (≤ 5 mm) ruptured and unruptured IAs were treated exclusively with Target Ultra and Nano coils. The primary endpoints were the initial rate of complete or near-complete aneurysm occlusion, aneurysm recurrence, and need for retreatment. Secondary endpoints were device- and procedure-related adverse events, hemorrhage from the coiled aneurysm at any time during follow-up, and clinical outcomes.

RESULTS

The ULTRA Registry included 100 patients with a mean ± SD age of 56 ± 11.6 years, of whom 75 were women and 48 presented after aneurysm rupture. The mean aneurysm size was (3.5 ± 0.9) × (2.8 ± 0.9) × (3.0 ± 1.0) mm, and the mean packing density was 34.4% ± 16.7%. Posttreatment complete or near-complete occlusion reported by an independent imaging core laboratory was seen in 92% of patients at baseline and in 87%, 87%, and 83% of patients at first, second, and final follow-up, respectively. At first, second, and final follow-up, 10%, 11%, and 15%, respectively, of patients were deemed to require retreatment. There were three procedural-related ischemic strokes and one intracranial hemorrhage from wire perforation of a parent artery not involved by the aneurysm. There were no coil-related adverse events, including no intraoperative aneurysm ruptures and no known aneurysm ruptures after coiling.

CONCLUSIONS

This assessment of aneurysm occlusion rates and safety profiles in ULTRA Registry study participants demonstrates excellent safety and efficacy profiles for Target Ultra and Nano coils in the treatment of small IAs.

In Brief

In the ULTRA Registry 100-patient cohort (mean aneurysm size 3.5 mm), researchers performed an investigator-initiated, multicenter US prospective study of aneurysm occlusion rates and safety profiles of Target Ultra and Nano coils for treatment of ruptured and unruptured small intracranial aneurysms, most with irregular shape and wide-neck morphology. Coils were safe and reliable, with only moderate aneurysm recurrence at follow-up, occurring mostly in ruptured aneurysms. There were no intraoperative aneurysm ruptures, coil-related complications, or crossovers from coiling to other treatment methods. This study provides additional prospective evidence that even challenging, tiny aneurysms can be safely treated via coil embolization, highlighting recent advancements in endovascular technology.

Coil embolization of intracranial aneurysms (IAs) is a well-accepted and highly effective treatment strategy. However, endovascular treatment of small IAs has been technically difficult historically and continues to be currently. The investigators of the International Subarachnoid Aneurysm Trial (ISAT), for example, excluded small aneurysms (≤ 3 mm) from their study, given the technical challenges that these aneurysms posed at that time for endovascular therapy.1,2 The challenges presented by catheterization and then deployment of coils while maintaining catheter stability in small, confined spaces have raised questions about the feasibility, safety, and efficacy of endovascular therapy of these lesions. Many investigators have reported a high risk of intraprocedural rupture, which is higher in already ruptured aneurysms compared to unruptured aneurysms.3 Preventing coil loops from herniating into the parent artery and coil migration present additional challenges when working in such small spaces. Additional management considerations to take into account include crossover from coil embolization to surgical clipping and achieving a reliable and durable result from coil embolization. Inability to effectively coil the aneurysm during the initial procedure can result in greater follow-up imaging, retreatment, and/or target aneurysm (re)hemorrhage.

Despite these challenges, endovascular treatment of small IAs has dramatically evolved and is now considered feasible and effective.36 New devices, including improved catheter technology and soft and stable coils, have been instrumental in making this possible. Target Ultra and Nano coils represent such advancement in soft coil mechanics. Therefore, we sought to investigate the safety and efficacy of these coils in the treatment of small IAs.

Methods

Trial Design

ULTRA is an investigator-initiated, nonrandomized, prospective registry of aneurysm patient data collected from six treatment centers across the United States to assess the use of Target Ultra and Nano coils to treat ruptured or unruptured small IAs, defined as having a maximal diameter ≤ 5.0 mm.

The institutional review boards at the University of Maryland School of Medicine and all participating study sites approved the study protocol. This study was funded by Stryker Neurovascular. The funding source was not involved in study design, monitoring, data collection, statistical analyses, interpretation of results, or manuscript writing. The sponsor was informed of serious adverse events (SAEs) throughout the trial. The grant was independently managed by the principal investigator (G.J.) with his research team. The principal investigator had no contractual relationship with the sponsor beyond the study’s funding during the study. An independent imaging core laboratory (F.K.H.) reviewed all angiographic imaging. Clinical outcomes and events were independently monitored and reviewed by a data safety monitoring board. Clinical trial registration information for this study can be found at https://clinicaltrials.gov/ct2/show/NCT02657772 with the unique identifier NCT02657772.

Participants and Interventions

Patients were eligible for enrollment if they were between 18 and 80 years of age with an untreated IA (ruptured or unruptured) ≤ 5.0 mm in maximal size and deemed amenable to complete or near-complete coil embolization during the index procedure. No cases with the use of planned staged coil embolization procedures were included. Patients with ruptured aneurysms were eligible if their Hunt and Hess aneurysm grade was III or lower. An amendment to the study later permitted the enrollment of Hunt and Hess grade IV patients. Exclusion criteria included the presence of prespecified concurrent intracranial pathologies or the presence of severe comorbidities, life expectancy less than 12 months, or other concerns regarding patient follow-up. Prior to enrollment, informed consent was obtained from patients or legally authorized representatives. Consent was obtained before aneurysm treatment in 96 consecutive cases and within 7 days after treatment in the final 18 cases. The use of coil types other than Target Ultra and Nano or a flow diverter was excluded. Cases with the use of assist devices at the surgeon’s discretion, including balloons and stents, were included. A detailed listing of inclusion and exclusion criteria is provided in the study protocol.

Outcomes

The primary endpoints of the ULTRA Registry were initial rate of complete or near-complete aneurysm occlusion, aneurysm recurrence, and need for retreatment as determined by the investigator and core laboratory using the Raymond and Roy (RR) occlusion scale with RR occlusion classes 1) complete occlusion, 2) neck remnant, and 3) residual aneurysm.7 Aneurysm occlusion was also assessed using the 6-point Meyer grading scale based on the percentage of aneurysm filling assessed on DSA. In addition, primary endpoints were evaluated based on aneurysm rupture status, and aneurysm size was dichotomized at maximal sizes of > 3.8 or ≤ 3.8 mm. Secondary endpoints of the trial were device- or procedure-related adverse events (AEs), hemorrhage from the index aneurysm at any time during follow-up, and clinical outcomes.

Aneurysm and coil volumes were calculated using software from the AngioCalc website (http://www.angiocalc.com). Packing density was calculated using the following formula: packing density = (coil volume/aneurysm volume) × 100%. Aneurysm volume was calculated by assuming that the aneurysms were elliptical and using the following formula: volume = π (height × length × width)/6. The volume of the coils was determined by summing the volume of all coils used. The volume of each coil was calculated by multiplying the square of the coil diameter by the length and by π/4.

Aneurysm treatment day was considered day 0. Imaging evaluation of the treated aneurysm via either cerebral angiography or brain MRA was obtained at the follow-up visits at 6–9 months (designated as the first follow-up) and at 12–18 months (designated as the second follow-up). Initial and follow-up clinical assessments were performed at the following intervals: baseline, 1 day, 3–28 days, 6–9 months, and 12–18 months. Clinical outcomes were assessed using the modified Rankin Scale (mRS) score at baseline, 1 day, 3–28 days, 6–9 months, and 12–18 months. Good clinical outcome was defined as an mRS score ≤ 2. National Institutes of Health Stroke Scale (NIHSS) values were assessed at baseline, 1 day, and 12–18 months. AEs were designated as related to the device or procedure at the discretion of the participating sites. Serious AEs, defined as life threatening, disabling, or resulting in prolonged hospitalization or death, were designated by the treating physicians and were reported to the principal investigator, his research team, and the study sponsor.

Statistical Methods

Baseline patient demographics are presented as numbers and percentages for categorical characteristic variables or mean ± standard deviation (SD) for continuous variables. Outcomes are reported as investigator/core laboratory results. In addition, outcomes are compared according to aneurysm rupture status and aneurysm size. Chi-square/Fisher’s exact test comparisons were performed for categorical variables and Student t-test analyses for continuous variables. Data analyses were performed using Stata 14.0.

Results

In total, 114 patients were enrolled in the ULTRA Registry between December 2013 and January 2019, and 14 patients were excluded after enrollment based on exclusion criteria, including aneurysm size > 5.0 mm, improper consent, Hunt and Hess grade V, predetermined staging of treatment, and kidney failure. Two patients were excluded due to the surgeon’s use of a coil type other than Target Ultra and Nano. After exclusion of these patients, 100 patients were included in the final cohort. There were no exclusions due to crossover from coiling to surgical clipping in prospectively enrolled patients. Follow-up imaging was obtained for 78 patients at the first follow-up (mean 5.7 months; contrast-enhanced MRA [n = 45], DSA [n = 27], and noncontrast MRA [n = 6]) and for 62 patients at the second follow-up (mean 15.7 months; DSA [n = 56], contrast-enhanced MRA [n = 5], and noncontrast MRA [n = 1]). In 82 patients, one or both imaging follow-up studies were performed, with the last imaging study designated as the final follow-up (mean 12.2 months; DSA [n = 67], contrast-enhanced MRA [n = 14], and noncontrast MRA [n = 1]). Eighteen patients had no imaging follow-up, including 4 patients who died during the study. One patient voluntarily withdrew from the study.

Baseline Characteristics

Patient demographic and clinical data, as well as aneurysm characteristics, are summarized in Table 1. The mean patient age was 56 ± 11.6 years, and 75 (75%) patients were female. The mean aneurysm size was (3.5 ± 0.9) × (2.8 ± 0.9) × (3.0 ± 1.0) mm. The mean dome/neck ratio was 1.9 ± 0.6, and 61 (61%) of aneurysms had a wide dome/neck ratio < 2. The mean coil diameter and length were 2 ± 0.9 mm and 3.6 ± 1.7 cm, respectively. A mean of 2.9 ± 1.6 coils were implanted into each aneurysm. The mean packing density was 34.4% ± 16.7%. Stent and balloon assist devices were used in 21 (21%) and 19 (19%) patients, respectively.

TABLE 1.

Baseline characteristics of patients and aneurysms in the ULTRA Registry (n = 100)

CharacteristicValue
Patient characteristics
 Sex
  Female75 (75)
  Male25 (25)
 Age, yrs56 ± 11.6
 Family history of aneurysm
  No89 (89)
  Yes11 (11)
 Comorbidities
  Hypertension65 (65)
  Hypercholesterolemia/hyperlipidemia45 (45)
  Diabetes17 (17)
  Cancer11 (11)
  Other medical conditions33 (33)
 Smoking status
  Current40 (40)
  Former25 (25)
  Never35 (35)
Aneurysm characteristics
 Rupture status
  Unruptured52 (52)
  Ruptured48 (48)
 If ruptured, H&H grade
  I10 (21.3)
  II18 (38.3)
  III19 (40.4)
 Neck size, mm2.0 ± 0.7
 Dome/neck ratio
  Mean1.9 ± 0.6
  <261 (61)
  ≥239 (39)
 Size, mm
  Height3.5 ± 0.9
  Width3.0 ± 1.0
  Depth2.8 ± 0.9
 Location
  Anterior communicating artery34 (34)
  Internal carotid artery22 (22)
  Posterior communicating artery13 (13)
  Basilar artery10 (10)
  Middle cerebral artery9 (9)
  Anterior cerebral artery9 (9)
  Vertebral artery3 (3)
 Shape
  Regular40 (40)
  Irregular57 (57)
  Daughter sac3 (3)
 Type
  Sidewall53 (53)
  Bifurcation29 (29)
  Terminal18 (18)

H&H = Hunt and Hess.

Values are presented as the number (%) of patients or mean ± SD.

Primary Endpoints

Data from the investigators and the core laboratory are reported as investigator/core laboratory (e.g., xx%/yy%). Complete or near-complete occlusion on the RR scale was seen in 97%/92% of patients at baseline after coiling and in 91%/87%, 89%/87%, and 88%/83% of patients at the first, second, and final follow-up visits, respectively. Major recurrence (defined by an increase on the RR scale from 1 to 3 or 2 to 3, or 3 with progression on the Meyer scale) was seen in 9%/13% of patients at first follow-up, 11%/11% at second follow-up, and 12%/16% of patients on final follow-up. Per investigator/core laboratory assessment at first, second, and final follow-ups, 13%/14%, 18%/21%, and 21%/23% of patients showed any degree of recurrence, respectively, and 10%/10%, 10%/11%, and 15%/15% of patients were deemed to require retreatment. These results are summarized in Table 2. A total of 9 patients, all of whom had an aneurysm rupture at initial presentation and all of whom were deemed to need retreatment, underwent retreatment during the study with either flow diversion (n = 4), coil embolization (n = 4), or surgical clipping (n = 1). Seven patients underwent retreatment after the first follow-up and exited the study upon retreatment without obtaining a second follow-up.

TABLE 2.

Primary and secondary outcomes

Investigator/Core Labp Value
Overall (n = 100)Ruptured (n = 48)Unruptured (n = 52)
Occlusion
  Initial97%/92%100%/96%94%/88%0.14/0.16
  1st FU91%/87%84%/72%96%/98%0.096/0.001
  2nd FU89%/87%83%/79%92%/92%0.25/0.14
  Final FU88%/83%82%/71%92%/92%0.18/0.012
Packing density34.4% ± 16.7%36.1% ± 17.5%32.7% ± 15.8%0.19
Meyer scale score increase
  1st FU18%/10%31%/22%9%/2%0.011/0.007
  2nd FU23%/16%29%/29%18%/8%0.32/0.037
  Final FU22%/18%29%/32%17%/8%0.17/0.006
Any recurrence
  1st FU13%/14%25%/31%4%/2%0.01/<0.001
  2nd FU18%/21%25%/38%13%/10%0.2/0.011
  Final FU21%/23%32%/41%12%/10%0.029/0.001
Major recurrence
  1st FU9%/13%16%/28%4%/2%0.096/0.001
  2nd FU11%/11%17%/17%8%/8%0.25/0.25
  Final FU12%/16%18%/26%8%/8%0.18/0.027
Retreatment need
  1st FU10%/10%22%/22%2%/2%0.007/0.008
  2nd FU10%/11%21%/21%3%/5%0.028/0.072
  Final FU15%/15%29%/26%4%/6%0.001/0.011
AEs
  082.0% (82)83.3% (40)80.8% (42)0.479
  19.0% (9)6.3% (3)11.5% (6)
  25.0% (5)6.3% (3)3.8% (2)
  31.0% (1)0.0% (0)1.9% (1)
  41.0% (1)0.0% (0)1.9% (1)
  52.0% (2)4.2% (2)0.0% (0)
SAEs
  083.0% (83)70.8% (34)94.2% (49)0.005
  113.0% (13)22.9% (11)3.8% (2)
  23.0% (3)4.2% (2)1.9% (1)
  31.0% (1)2.1% (1)0.0% (0)
ICH1%2%0%
IOR0%0%0%
Coil-related complication0%0%0%
mRS score
  Baseline1.1 ± 1.41.8 ± 1.70.5 ± 0.7<0.001
  2nd FU0.6 ± 0.80.8 ± 10.4 ± 0.60.10
NIHSS
  Baseline1.7 ± 43.2 ± 5.30.4 ± 1.1<0.001
  2nd FU0.3 ± 1.20.3 ± 1.30.3 ± 1.10.97
Final mRS score
  0–292% (80)82% (32)100% (48)0.003
  31% (1)3% (1)0% (0)
  42% (2)5% (2)0% (0)
  50% (0)0% (0)0% (0)
  65% (4)10% (4)0% (0)

FU = follow-up; ICH = intracranial hemorrhage.

Values are presented as the percentage (number) of patients or mean ± SD unless otherwise indicated. Data from the investigation and the core laboratory are reported as investigator/core laboratory (e.g., xx%/yy%).

Subgroup Analyses

According to reporting by both the investigators and core laboratory, ruptured aneurysms were more likely to demonstrate recurrence and require retreatment at both the first and final follow-ups. Ruptured versus unruptured aneurysm recurrence rates were 25%/31% versus 4%/2% (p = 0.01/< 0.001) and 32%/41% versus 12%/10% (p = 0.029/0.001), respectively, and retreatment need was 22%/22% versus 2%/2% (p = 0.007/0.008) and 29%/26% versus 4%/6% (p = 0.001/0.011), respectively. These results are summarized in Table 2.

Numerically greater rates of recurrence and need for retreatment occurred in patients with relatively smaller aneurysms, i.e., those ≤ 3.8 mm in maximal diameter, particularly at the final follow-up. However, per investigator and core laboratory reporting this finding did not reach statistical significance in terms of rates of aneurysm occlusion, recurrence, or need for retreatment at first and final follow-ups when maximal aneurysm sizes > 3.8 versus ≤ 3.8 mm were compared. For these aneurysms, occlusion rates at first follow-up were 90%/88% versus 92%/86% (p = 0.59/0.53) and at final follow-up were 91%/88% versus 85%/77% (p = 0.31/0.17); rates for any recurrence at first follow-up were 12%/12% versus 14%/17% (p = 0.53/0.51) and at final follow-up were 14%/19% versus 28%/28% (p = 0.11/0.3); retreatment need rates at first follow-up were 7%/7% versus 14%/14% (p = 0.27/0.26) and at final follow-up were 9%/9% versus 20%/20% (p = 0.13/0.15).

Secondary Endpoints and AEs

During the study, 4 patients died from complications of initial subarachnoid hemorrhage presentation. There were no known deaths from unknown causes. The mean mRS scores at baseline, first follow-up, and second follow-up were 1.1 ± 1.4, 0.6 ± 0.8, and 0.6 ± 0.8, respectively. The mean NIHSS scores at baseline and second follow-up were 1.7 ± 4 and 0.3 ± 1.2, respectively. Good clinical outcome, defined as mRS scores 0–2, was seen in 92% of patients at last follow-up. These results are summarized in Table 2.

The investigators recorded 36 AEs in 18 patients and 22 SAEs in 17 patients. AEs and SAEs are listed in Supplemental Table 1. The number of AEs per patient ranged from 0 to 5. There were 7 procedure-related AEs: ischemic stroke (n = 3), intracranial hemorrhage from wire perforation of the anterior cerebral artery distant from and not involved by the aneurysm (n = 1), cellulitis (n = 1), groin hematoma (n = 1), and lip numbness (n = 1). The single microwire device–related AE resulted in 1 intracranial hemorrhage from an artery distant from the target aneurysm in a patient who presented with subarachnoid hemorrhage and later died of respiratory failure. There were no coil-related AEs, including no instances of coil breakage or intraoperative aneurysm rupture due to coiling. There were no deaths attributed to the coiling procedure. There were no known aneurysm ruptures after coiling.

Discussion

Technological advancements have propelled the endovascular treatment of IAs, including small IAs in many cases, to the forefront of management options for these lesions. The advent of safer and more trackable sheaths, catheters, and microcatheters and softer and smaller coils has substantially improved the ability of neurointerventional surgeons to treat small IAs, and coil embolization of these lesions is accepted as an effective minimally invasive treatment strategy. In this study, we found that endovascular therapy is feasible, safe, and effective in treating small IAs with the use of only Target Ultra and Nano coils. Although small IAs remain potentially challenging lesions to treat by coil embolization, our results highlight the safety and reliability of current endovascular techniques, including these coils.

There were no cases of crossover from coiling to clipping in our study, which is in contrast to reports of older studies of the treatment of small IAs. In the Barrow Ruptured Aneurysm Trial (BRAT), 25 of 40 patients with small ruptured IAs who were randomized to coiling crossed over to clipping,8 whereas none of the patients with small ruptured IAs who were assigned to clipping crossed over to coiling. In another series of small ruptured IAs (≤ 3 mm), endovascular treatment failed in 9.9% of cases.9 These failure rates underscore the historical technical challenges posed by small IAs.

There were no cases of intraoperative rupture (IOR) in our study. This feared and potentially devastating complication is regarded as the primary limitation of coil embolization of small IAs. However, IOR is encountered less frequently in the most recent studies investigating coil embolization of small IAs. Patients with small IAs are more likely to experience IOR than those with larger IAs,1012 and IORs occur more often with ruptured than with unruptured IAs. Two older studies (2009 and 2010, respectively) demonstrated 10.1%4 and 16.7%3 rates of IOR during coil embolization of small ruptured IAs. Two recent studies demonstrated IOR in 13% and 9% of small ruptured IAs,13,14 while another group more recently reported IOR in only 3.7% of small ruptured IAs.15 Two prior series evaluating Target Ultra and Nano coils in the treatment of small IAs demonstrated IOR in only 2% and 0% of cases;16,17 80% of aneurysms were unruptured in those reports. These and other studies are summarized in Table 3.18,19

TABLE 3.

Risk of intraoperative aneurysm rupture during coiling by aneurysm size

Authors & YearAneurysm Size, mm
≤3≤4<5>3 or 4
Nguyen et al., 20081011.7% (60)2.3% (622)
van Rooij et al., 200947.7% (196)3.3% (1099)
Brinjikji et al., 201038.3% (493)
Schuette et al., 20111213.5% (74)2.9% (273)
Chung et al., 2013198.3% (108)
Mitchell et al., 2013118.7% (683)3.9% (683)
Starke et al., 2013153.7% (91)
Stetler et al., 2015181.2% (85)
Yamaki et al., 2016147% (1105)
Jindal et al., 2016162% (50)*
Kim et al., 2018170% (45)*
Zhao et al., 20191316% (46)
ULTRA Registry0% (100)*

Values are presented as the percentage of aneurysms (total number of aneurysms evaluated).

Evaluated only Target Ultra and Nano coils.

Favorable clinical outcomes in our study were seen in 82% and 100% of patients with ruptured and unruptured aneurysms, respectively, at the last follow-up. There were 7 (7%) procedure-related AEs reported, including 3 cases of procedure-related ischemic strokes and 1 microwire arterial perforation. In one study on small ruptured IAs, there was a 9.8% (n = 8) procedure-related complication rate, including 3 ischemic events and 3 intraprocedural ruptures with permanent morbidity in 3 patients.9 In another study of 97 patients with small ruptured IAs, procedural complications occurred in 7.2% of patients, including intraprocedural ruptures in 4.1%20 and favorable outcomes in 80.3% of patients. A meta-analysis of outcomes of endovascular therapy in small ruptured IAs demonstrated morbidity of 4%.3 Another meta-analysis of coiling very small IAs demonstrated an intraoperative ischemic stroke risk of 4% across 1105 patients.14

Recurrence and retreatment rates are other limitations of coil embolization of IAs. Generally, across IAs of all sizes, postcoiling aneurysm recurrence and retreatment rate ranges of 15%–34% and 10%–20%, respectively, have been reported2125 in some older series, whereas more recently reported studies have demonstrated improvements in rates of recurrence and retreatment of 4%–21% and 3%–8%, respectively.2628 In regard to small IAs, retreatment of both ruptured and unruptured aneurysms has been shown to be 5.4% in one meta-analysis,3 while another demonstrated a ≥ 6-month retreatment rate of 7%.14 In the present study, according to core laboratory reporting, the rates of major recurrence (16%) and retreatment need (15%) at last follow-up were higher than some of the rates reported in these very recent reports. However, these prior studies were retrospective meta-analyses as opposed to the current prospective registry. Recurrence and retreatment in the current registry were primarily seen in ruptured aneurysms. Recanalization and retreatment rates are relatively high for ruptured aneurysms28 and higher for very small ruptured aneurysms in particular,9 findings that reflect a greater propensity for ruptured aneurysms to recur,2830 as well as the difficulty involved in deploying coils into small confined spaces with an already weakened aneurysm wall. Our results likely also reflect a propensity for Target Ultra and Nano coils toward some degree of compaction, as the coil design is deliberately geared toward a high degree of softness. However, rates of major recurrence and any increase in the Meyer scale in the current study (16% and 18%, respectively) were numerically lower than those for the bare platinum coiling cohort of another recent study (20.7% and 27%). This finding is probably related at least in part to a higher mean packing density of 34% in the current study compared to 24.7% in the other study.26 Notably, nearly all aneurysms in that study had a narrow neck with a regular shape, and most were unruptured. In contrast, most aneurysms in our study had a wide neck and irregular shape, while nearly half presented after rupture. These factors add complexity to and difficulty in obtaining aneurysm occlusion at baseline and maintaining it at follow-up. Two additional studies evaluating Target Ultrasoft and Nano coils in small IAs demonstrated lower rates of recurrence and retreatment of 10% or less. However, these studies were of retrospective design and/or nearly exclusively evaluated unruptured aneurysms.12,13 It is noteworthy that, with appropriate imaging follow-up, small recurrences after coiling have not resulted in worse outcomes due to significant rebleeding or morbidity of repeat endovascular therapy.28,31 Subtotal coiling of an IA in the acute stage with subacute second-stage aneurysm obliteration via stent-assisted coiling, flow diverter reconstruction, or microsurgical clipping has become a more commonly utilized treatment strategy in certain settings.31,32

It should be stated that multiple studies have shown that the likelihood of rupture of small unruptured IAs without treatment is low.1,2,33 Nevertheless, subarachnoid hemorrhage from small and very small IAs is not uncommon in neurovascular clinical practice,34,35 and nearly half of IAs in the ULTRA Registry presented after rupture. Current predictive scoring systems for unruptured aneurysms may also underestimate future rupture risk in some patients.36 Indications for treatment of small, unruptured IAs include patient or family history of subarachnoid hemorrhage. In addition, patient- and aneurysm-related factors play a role in decision making, including patient age and management preference and aneurysm size, morphology, and location, in addition to the feasibility of and risk profile associated with treatment.

Coil sizing in the current study was determined by the individual provider treating the aneurysm. In the authors’ experience with these coils, sizing can require a coil one-half millimeter smaller in diameter than the target diameter desired. These decisions vary by aneurysm morphology as well as presence of assist devices.

Study Limitations

This study has limitations. While the strength of this study is its diligent prospective design, the power of the study is relatively small, and, as such, meaningful comparisons between the ruptured and unruptured cohorts are challenging to make definitively. Long-term clinical and imaging follow-up is lacking, although the majority of aneurysm retreatments occur in the early follow-up period.37 Follow-up imaging is missing on 18 patients, including 4 patients who died soon after rupture from complications of subarachnoid hemorrhage presentation. A minority of patients were enrolled after coil embolization, which can introduce selection bias into the study. Stents were used in 21 patients; such assist devices can help achieve optimal aneurysm occlusion at baseline and follow-up. Indications for treatment of unruptured aneurysms and data on total patients screened were not collected in this study; documentation of these data in future studies on small IAs would be useful.

Conclusions

This analysis of the ULTRA Registry patient data demonstrates excellent safety and efficacy profiles of Target Ultra and Nano coils in treating ruptured and unruptured small IAs. There were no coil-related complications. The excellent safety profile demonstrated here is comparable to those reported in other retrospective studies evaluating these coils. The core laboratory–adjudicated aneurysm recurrence and retreatment rates were similar to those documented in prior similar reports.

Disclosures

This registry was funded by Stryker Neurovascular. The sponsor had no role in data collection, data management, data analysis, nor manuscript preparation. Dr. Jindal reports receiving clinical or research support for the study described (includes equipment or material) from, being a consultant for, and receiving support for travel and food from Stryker Neurovascular and receiving clinical or research support for the study described from MicroVention. Drs. Gupta and Satti each report being a consultant for Stryker Neurovascular. Dr. Colby reports being a consultant for Stryker Neurovascular and MicroVention. Dr. Caplan reports being a consultant for Medtronic, receiving clinical or research support for the study described (includes equipment or material) from Stryker, and receiving support of non–study-related clinical or research effort overseen by the author from MicroVention, Balt, and Stryker. Dr. Miller reports receiving clinical or research support for the study described (includes equipment or material) from Stryker and being a site investigator and receiving salary support from MicroVention-Terumo, Vesalio, Stryker, and Northwestern University for the completed Hydrogel Endovascular Aneurysm Treatment Trial (HEAT), a multicenter study investigating the safety and efficacy of using hydrogel-coated coils for the treatment of intracranial aneurysms.

Author Contributions

Conception and design: Jindal. Acquisition of data: Jindal, Almardawi, Gupta, Colby, Schirmer, Satti, Pukenas, Hui, Miller. Analysis and interpretation of data: Jindal, Almardawi, Hui, Kibria. Drafting the article: Jindal. Critically revising the article: Jindal, Gupta, Colby, Schirmer, Satti, Hui, Caplan, Cherian, Kibria, Simard. Reviewed submitted version of manuscript: Jindal, Colby, Schirmer, Satti, Pukenas, Hui, Caplan, Cherian, Aldrich, Simard. Approved the final version of the manuscript on behalf of all authors: Jindal. Statistical analysis: Jindal, Almardawi, Kibria. Administrative/technical/material support: Jindal, Almardawi. Study supervision: Jindal, Almardawi, Gupta, Colby, Schirmer, Satti, Pukenas, Caplan. Study principal investigator: Jindal. Study coordinator, data and safety monitoring, site visits: Almardawi.

Supplemental Information

Online-Only Content

Supplemental material is available with the online version of the article.

References

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    Molyneux AJ, Kerr RSC, Yu LM, et al. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet. 2005;366(9488):809817.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Molyneux A, Kerr R, Stratton I, et al. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet. 2002;360(9342):12671274.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Brinjikji W, Lanzino G, Cloft HJ, Rabinstein A, Kallmes DF. Endovascular treatment of very small (3 mm or smaller) intracranial aneurysms: report of a consecutive series and a meta-analysis. Stroke. 2010;41(1):116121.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4

    van Rooij WJ, Keeren GJ, Peluso JPP, Sluzewski M. Clinical and angiographic results of coiling of 196 very small (< or = 3 mm) intracranial aneurysms. AJNR Am J Neuroradiol. 2009;30(4):835839.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Pierot L, Barbe C, Spelle L. Endovascular treatment of very small unruptured aneurysms: rate of procedural complications, clinical outcome, and anatomical results. Stroke. 2010;41(12):28552859.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Iskandar A, Nepper-Rasmussen J. Endovascular treatment of very small intracranial aneurysms. Interv Neuroradiol. 2011;17(3):299305.

  • 7

    Roy D, Milot G, Raymond J. Endovascular treatment of unruptured aneurysms. Stroke. 2001;32(9):19982004.

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    Catapano JS, Nguyen CL, Frisoli FA, et al. Small intracranial aneurysms in the Barrow Ruptured Aneurysm Trial (BRAT). Acta Neurochir (Wien). 2021;163(1):123129.

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    Chalouhi N, Penn DL, Tjoumakaris S, et al. Treatment of small ruptured intracranial aneurysms: comparison of surgical and endovascular options. J Am Heart Assoc. 2012;1(4):e002865.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Nguyen TN, Raymond J, Guilbert F, et al. Association of endovascular therapy of very small ruptured aneurysms with higher rates of procedure-related rupture. J Neurosurg. 2008;108(6):10881092.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Mitchell PJ, Muthusamy S, Dowling R, Yan B. Does small aneurysm size predict intraoperative rupture during coiling in ruptured and unruptured aneurysms?. J Stroke Cerebrovasc Dis. 2013;22(8):12981303.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Schuette AJ, Hui FK, Spiotta AM, et al. Endovascular therapy of very small aneurysms of the anterior communicating artery: five-fold increased incidence of rupture. Neurosurgery. 2011;68(3):731737.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Zhao B, Xing H, Fan L, et al. Endovascular coiling versus surgical clipping of very small ruptured anterior communicating artery aneurysms. World Neurosurg. 2019;126:e1246e1250.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Yamaki VN, Brinjikji W, Murad MH, Lanzino G. Endovascular treatment of very small intracranial aneurysms: meta-analysis. AJNR Am J Neuroradiol. 2016;37(5):862867.

  • 15

    Starke RM, Chalouhi N, Ali MS, et al. Endovascular treatment of very small ruptured intracranial aneurysms: complications, occlusion rates and prediction of outcome. J Neurointerv Surg. 2013;5(suppl 3):iii66iii71.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Jindal G, Miller T, Iyohe M, Shivashankar R, Prasad V, Gandhi D. Small intracranial aneurysm treatment using Target (®) Ultrasoft (™) coils. J Vasc Interv Neurol. 2016;9(1):4651.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Kim SM, Lee HG, Choi BS, et al. Recurrence of small cerebral aneurysms (< 4 mm) treated endovascularly using Target® Nano™ coils. J Cerebrovasc Endovasc Neurosurg. 2018;20(2):106111.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Stetler WRJ Jr, Wilson TJ, Al-Holou WN, et al. Conventional endovascular treatment of small intracranial aneurysms is not associated with additional risks compared with treatment of larger aneurysms. J Neurointerv Surg. 2015;7(4):262265.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19

    Chung KHC, Herwadkar A, Laitt R, Patel HC. Rate and clinical impact of intra-procedural complications during coil embolisation of ruptured small (3 mm or less) cerebral aneurysms. Clin Neurol Neurosurg. 2013;115(8):13561361.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Ioannidis I, Lalloo S, Corkill R, Kuker W, Byrne JV. Endovascular treatment of very small intracranial aneurysms. J Neurosurg. 2010;112(3):551556.

  • 21

    Crobeddu E, Lanzino G, Kallmes DF, Cloft HJ. Review of 2 decades of aneurysm-recurrence literature, part 1: reducing recurrence after endovascular coiling. AJNR Am J Neuroradiol. 2013;34(2):266270.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Crobeddu E, Lanzino G, Kallmes DF, Cloft HJ. Review of 2 decades of aneurysm-recurrence literature, part 2: managing recurrence after endovascular coiling. AJNR Am J Neuroradiol. 2013;34(3):481485.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    White PM, Lewis SC, Gholkar A, et al. Hydrogel-coated coils versus bare platinum coils for the endovascular treatment of intracranial aneurysms (HELPS): a randomised controlled trial. Lancet. 2011;377(9778):16551662.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24

    McDougall CG, Johnston SC, Gholkar A, et al. Bioactive versus bare platinum coils in the treatment of intracranial aneurysms: the MAPS (Matrix and Platinum Science) trial. AJNR Am J Neuroradiol. 2014;35(5):935942.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Riina HA, Barker FG. Editorial. The relevance of the BRAT and the management of ruptured brain aneurysms. J Neurosurg. 2019;132(3):760761.

  • 26

    Bendok BR, Abi-Aad KR, Ward JD, et al. The Hydrogel Endovascular Aneurysm Treatment Trial (HEAT): a randomized controlled trial of the second-generation hydrogel coil. Neurosurgery. 2020;86(5):615624.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27

    Taschner CA, Chapot R, Costalat V, et al. Second-generation hydrogel coils for the endovascular treatment of intracranial aneurysms: a randomized controlled trial. Stroke. 2018;49(3):667674.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Funakoshi Y, Imamura H, Tani S, et al. Predictors of cerebral aneurysm rupture after coil embolization: single-center experience with recanalized aneurysms. AJNR Am J Neuroradiol. 2020;41(5):828835.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Piotin M, Blanc R, Spelle L, et al. Stent-assisted coiling of intracranial aneurysms: clinical and angiographic results in 216 consecutive aneurysms. Stroke. 2010;41(1):110115.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Raymond J, Guilbert F, Weill A, et al. Long-term angiographic recurrences after selective endovascular treatment of aneurysms with detachable coils. Stroke. 2003;34(6):13981403.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Howard BM, Frerich JM, Madaelil TP, et al. ‘Plug and pipe’ strategy for treatment of ruptured intracranial aneurysms. J Neurointerv Surg. 2019;11(1):4348.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Brinjikji W, Piano M, Fang S, et al. Treatment of ruptured complex and large/giant ruptured cerebral aneurysms by acute coiling followed by staged flow diversion. J Neurosurg. 2016;125(1):120127.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Morita A, Kirino T, Hashi K, et al. The natural course of unruptured cerebral aneurysms in a Japanese cohort. N Engl J Med. 2012;366(26):24742482.

  • 34

    Bender MT, Wendt H, Monarch T, et al. Small aneurysms account for the majority and increasing percentage of aneurysmal subarachnoid hemorrhage: a 25-year, single institution study. Neurosurgery. 2018;83(4):692699.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Waqas M, Chin F, Rajabzadeh-Oghaz H, et al. Size of ruptured intracranial aneurysms: a systematic review and meta-analysis. Acta Neurochir (Wien). 2020;162(6):13531362.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Feghali J, Gami A, Xu R, et al. Application of unruptured aneurysm scoring systems to a cohort of ruptured aneurysms: are we underestimating rupture risk?. Neurosurg Rev. 2021;44(6):34873498.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    McDougall CG, Johnston SC, Hetts SW, et al. Five-year results of randomized bioactive versus bare metal coils in the treatment of intracranial aneurysms: the Matrix and Platinum Science (MAPS). Trial. J Neurointerv Surg. 2021;13(10):930934.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

Supplementary Materials

  • Collapse
  • Expand

Figure from Ramos et al. (pp 95–103).

  • 1

    Molyneux AJ, Kerr RSC, Yu LM, et al. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet. 2005;366(9488):809817.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Molyneux A, Kerr R, Stratton I, et al. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet. 2002;360(9342):12671274.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Brinjikji W, Lanzino G, Cloft HJ, Rabinstein A, Kallmes DF. Endovascular treatment of very small (3 mm or smaller) intracranial aneurysms: report of a consecutive series and a meta-analysis. Stroke. 2010;41(1):116121.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4

    van Rooij WJ, Keeren GJ, Peluso JPP, Sluzewski M. Clinical and angiographic results of coiling of 196 very small (< or = 3 mm) intracranial aneurysms. AJNR Am J Neuroradiol. 2009;30(4):835839.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Pierot L, Barbe C, Spelle L. Endovascular treatment of very small unruptured aneurysms: rate of procedural complications, clinical outcome, and anatomical results. Stroke. 2010;41(12):28552859.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Iskandar A, Nepper-Rasmussen J. Endovascular treatment of very small intracranial aneurysms. Interv Neuroradiol. 2011;17(3):299305.

  • 7

    Roy D, Milot G, Raymond J. Endovascular treatment of unruptured aneurysms. Stroke. 2001;32(9):19982004.

  • 8

    Catapano JS, Nguyen CL, Frisoli FA, et al. Small intracranial aneurysms in the Barrow Ruptured Aneurysm Trial (BRAT). Acta Neurochir (Wien). 2021;163(1):123129.

  • 9

    Chalouhi N, Penn DL, Tjoumakaris S, et al. Treatment of small ruptured intracranial aneurysms: comparison of surgical and endovascular options. J Am Heart Assoc. 2012;1(4):e002865.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Nguyen TN, Raymond J, Guilbert F, et al. Association of endovascular therapy of very small ruptured aneurysms with higher rates of procedure-related rupture. J Neurosurg. 2008;108(6):10881092.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Mitchell PJ, Muthusamy S, Dowling R, Yan B. Does small aneurysm size predict intraoperative rupture during coiling in ruptured and unruptured aneurysms?. J Stroke Cerebrovasc Dis. 2013;22(8):12981303.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Schuette AJ, Hui FK, Spiotta AM, et al. Endovascular therapy of very small aneurysms of the anterior communicating artery: five-fold increased incidence of rupture. Neurosurgery. 2011;68(3):731737.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Zhao B, Xing H, Fan L, et al. Endovascular coiling versus surgical clipping of very small ruptured anterior communicating artery aneurysms. World Neurosurg. 2019;126:e1246e1250.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Yamaki VN, Brinjikji W, Murad MH, Lanzino G. Endovascular treatment of very small intracranial aneurysms: meta-analysis. AJNR Am J Neuroradiol. 2016;37(5):862867.

  • 15

    Starke RM, Chalouhi N, Ali MS, et al. Endovascular treatment of very small ruptured intracranial aneurysms: complications, occlusion rates and prediction of outcome. J Neurointerv Surg. 2013;5(suppl 3):iii66iii71.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Jindal G, Miller T, Iyohe M, Shivashankar R, Prasad V, Gandhi D. Small intracranial aneurysm treatment using Target (®) Ultrasoft (™) coils. J Vasc Interv Neurol. 2016;9(1):4651.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Kim SM, Lee HG, Choi BS, et al. Recurrence of small cerebral aneurysms (< 4 mm) treated endovascularly using Target® Nano™ coils. J Cerebrovasc Endovasc Neurosurg. 2018;20(2):106111.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Stetler WRJ Jr, Wilson TJ, Al-Holou WN, et al. Conventional endovascular treatment of small intracranial aneurysms is not associated with additional risks compared with treatment of larger aneurysms. J Neurointerv Surg. 2015;7(4):262265.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19

    Chung KHC, Herwadkar A, Laitt R, Patel HC. Rate and clinical impact of intra-procedural complications during coil embolisation of ruptured small (3 mm or less) cerebral aneurysms. Clin Neurol Neurosurg. 2013;115(8):13561361.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Ioannidis I, Lalloo S, Corkill R, Kuker W, Byrne JV. Endovascular treatment of very small intracranial aneurysms. J Neurosurg. 2010;112(3):551556.

  • 21

    Crobeddu E, Lanzino G, Kallmes DF, Cloft HJ. Review of 2 decades of aneurysm-recurrence literature, part 1: reducing recurrence after endovascular coiling. AJNR Am J Neuroradiol. 2013;34(2):266270.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Crobeddu E, Lanzino G, Kallmes DF, Cloft HJ. Review of 2 decades of aneurysm-recurrence literature, part 2: managing recurrence after endovascular coiling. AJNR Am J Neuroradiol. 2013;34(3):481485.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    White PM, Lewis SC, Gholkar A, et al. Hydrogel-coated coils versus bare platinum coils for the endovascular treatment of intracranial aneurysms (HELPS): a randomised controlled trial. Lancet. 2011;377(9778):16551662.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24

    McDougall CG, Johnston SC, Gholkar A, et al. Bioactive versus bare platinum coils in the treatment of intracranial aneurysms: the MAPS (Matrix and Platinum Science) trial. AJNR Am J Neuroradiol. 2014;35(5):935942.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Riina HA, Barker FG. Editorial. The relevance of the BRAT and the management of ruptured brain aneurysms. J Neurosurg. 2019;132(3):760761.

  • 26

    Bendok BR, Abi-Aad KR, Ward JD, et al. The Hydrogel Endovascular Aneurysm Treatment Trial (HEAT): a randomized controlled trial of the second-generation hydrogel coil. Neurosurgery. 2020;86(5):615624.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27

    Taschner CA, Chapot R, Costalat V, et al. Second-generation hydrogel coils for the endovascular treatment of intracranial aneurysms: a randomized controlled trial. Stroke. 2018;49(3):667674.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Funakoshi Y, Imamura H, Tani S, et al. Predictors of cerebral aneurysm rupture after coil embolization: single-center experience with recanalized aneurysms. AJNR Am J Neuroradiol. 2020;41(5):828835.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Piotin M, Blanc R, Spelle L, et al. Stent-assisted coiling of intracranial aneurysms: clinical and angiographic results in 216 consecutive aneurysms. Stroke. 2010;41(1):110115.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Raymond J, Guilbert F, Weill A, et al. Long-term angiographic recurrences after selective endovascular treatment of aneurysms with detachable coils. Stroke. 2003;34(6):13981403.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Howard BM, Frerich JM, Madaelil TP, et al. ‘Plug and pipe’ strategy for treatment of ruptured intracranial aneurysms. J Neurointerv Surg. 2019;11(1):4348.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Brinjikji W, Piano M, Fang S, et al. Treatment of ruptured complex and large/giant ruptured cerebral aneurysms by acute coiling followed by staged flow diversion. J Neurosurg. 2016;125(1):120127.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Morita A, Kirino T, Hashi K, et al. The natural course of unruptured cerebral aneurysms in a Japanese cohort. N Engl J Med. 2012;366(26):24742482.

  • 34

    Bender MT, Wendt H, Monarch T, et al. Small aneurysms account for the majority and increasing percentage of aneurysmal subarachnoid hemorrhage: a 25-year, single institution study. Neurosurgery. 2018;83(4):692699.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Waqas M, Chin F, Rajabzadeh-Oghaz H, et al. Size of ruptured intracranial aneurysms: a systematic review and meta-analysis. Acta Neurochir (Wien). 2020;162(6):13531362.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Feghali J, Gami A, Xu R, et al. Application of unruptured aneurysm scoring systems to a cohort of ruptured aneurysms: are we underestimating rupture risk?. Neurosurg Rev. 2021;44(6):34873498.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    McDougall CG, Johnston SC, Hetts SW, et al. Five-year results of randomized bioactive versus bare metal coils in the treatment of intracranial aneurysms: the Matrix and Platinum Science (MAPS). Trial. J Neurointerv Surg. 2021;13(10):930934.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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