You are here

Article Text

Article menu

Download PDFPDF

Hemorrhagic stroke
Original research
A survey of intracranial aneurysm treatment practices among United States physicians
  1. Kyle M Fargen1,
  2. Hector E Soriano-Baron1,
  3. Julia T Rushing2,
  4. William Mack3,
  5. J Mocco4,
  6. Felipe Albuquerque5,
  7. Andrew F Ducruet5,
  8. Maxim Mokin6,
  9. Italo Linfante7,
  10. Stacey Q Wolfe1,
  11. John A Wilson1,
  12. Joshua A Hirsch8
  1. 1Department of Neurological Surgery, Wake Forest University, Winston-Salem, North Carolina, USA
  2. 2Wake Forest Baptist Medical Center, Wake Forest University, Winston-Salem, North Carolina, USA
  3. 3Department of Neurosurgery, University of Southern California, Los Angeles, California, USA
  4. 4Department of Neurosurgery, Mount Sinai Hospital, New York, New York, USA
  5. 5Department of Neurosurgery, Barrow Neurological Institute, Phoenix, Arizona, USA
  6. 6Departments of Neurology and Neurosurgery, University of Southern Florida, Tampa, Florida, USA
  7. 7Miami Cardiac and Vascular Institute, Baptist Neuroscience Center, Miami, Florida, USA
  8. 8Department of Interventional Neuroradiology, Massachusetts General Hospital, Boston, Massachusetts, USA
  1. Correspondence to Dr Kyle M Fargen, Department of Neurological Surgery, 1 Medical Center Blvd, Winston-Salem, NC 27157, USA; kfargen{at}wakehealth.edu

Abstract

Background Recent surveys have failed to examine cerebrovascular aneurysm treatment practices among US physicians.

Objective To survey physicians who are actively involved in the care of patients with cerebrovascular aneurysms to determine current aneurysm treatment preferences.

Methods A 25-question SurveyMonkey online survey was designed and distributed electronically to members of the Society of NeuroInterventional Surgery, Society of Vascular and Interventional Neurology, and the American Association of Neurological Surgeons/Congress of Neurological Surgeons Combined Cerebrovascular Section.

Results 211 physicians completed the survey. Most respondents recommend endovascular treatment as the first-line management strategy for most ruptured (78%) and unruptured (71%) aneurysms. Thirty-eight per cent of respondents indicate that they routinely treat all patients with subarachnoid hemorrhage regardless of grade. Most physicians use the International Study of Unruptured Intracranial Aneurysms data for counseling patients on natural history risk (80%); a small minority (11%) always or usually recommend treatment of anterior circulation aneurysms of <5 mm. Two-thirds of respondents continue to recommend clipping for most middle cerebral artery aneurysms, while most (51%) recommend flow diversion for wide-necked internal carotid artery aneurysms. Follow-up imaging schedules are highly variable. Neurosurgeons at academic institutions and those practicing longer were more likely to recommend clipping surgery for aneurysms (p<0.05).

Conclusions This survey demonstrates considerable variability in patient selection for intracranial aneurysm treatment, preferred treatment strategies, and follow-up imaging schedules among US physicians.

  • Aneurysm
  • Coil
  • Flow Diverter
  • Subarachnoid

https://doi.org/10.1136/neurintsurg-2016-012808

Statistics from Altmetric.com

    Request Permissions

    If you wish to reuse any or all of this article please use the link below which will take you to the Copyright Clearance Center’s RightsLink service. You will be able to get a quick price and instant permission to reuse the content in many different ways.

    Introduction

    Subarachnoid hemorrhage from ruptured intracranial aneurysms remains a source of considerable patient morbidity, cost, and disability. Approximately 0.8–6% of the population has intracranial aneurysms1–5 and 20–22 000 aneurysms are treated by endovascular means each year.6 Aneurysms can be associated with major morbidity and mortality when they rupture, with 30-day mortality rates ranging from 30% to 60%.7 ,8 Rupture may be further complicated by hydrocephalus, subdural or intraparenchymal hematoma, seizure, cardiomyopathy, vasospasm, and delayed ischemic events, among others. Rupture is a rare but unpredictable event.

    The most often cited natural history studies of aneurysms are from the International Study of Unruptured Intracranial Aneurysm trial (ISUIA),9 ,10 but these studies suggest a natural history of small aneurysms that is distinctly different from that seen in clinical practice. For instance, anterior circulation aneurysms measuring <7 mm have a negligible annual risk of rupture based on ISUIA findings. Yet, in a study of almost 1000 patients presenting with ruptured aneurysms, Weir et al11 showed that 70% of ruptured aneurysms were <10 mm in size. Furthermore, Carter et al12 have suggested that the sizes of ruptured aneurysms differ based on location and are smaller on more distal arteries than those arising from a more proximal location. A 2014 study of international experts in the field showcased the lack of consensus on aneurysm treatment due to the uncertainty associated with their natural history.13 The underlying conclusion of that group was that an international collaboration was necessary for further research.

    To date there is a relative lack of guidelines to assist in the selection of patients for endovascular or microsurgical treatment of ruptured or unruptured cerebral aneurysms based on natural history, location, morphological features of the aneurysm, and patient characteristics such as age. The uncertainty about natural history, the considerable morbidity and mortality associated with rupture, and innate practice preferences in the three different specialties that treat cerebral aneurysms have led to highly disparate treatment practices. No recent studies have attempted to define modern clinical practice to quantify and understand the variability in aneurysm treatment preferences or practice patterns. We sought to survey members of the three major US professional societies that treat cerebral aneurysms to better understand how and why physicians are treating patients in the USA.

    Methods

    Institutional review board approval was obtained before starting the study. A 25-question SurveyMonkey online survey was designed to examine aneurysm treatment practices (tables 1⇓⇓–4 and figure 1). Approval was obtained from the Society of NeuroInterventional Surgery (SNIS), Society of Vascular and Interventional Neurology (SVIN), and the American Association of Neurological Surgeons/Congress of Neurological Surgeons Combined Cerebrovascular Section (CV section) to distribute emails to their respective members soliciting survey completion. In addition, a copy of the email was posted on the SNIS Connect website for SNIS members and advertised in registration packets at the 2016 SNIS annual meeting in Boston, Massachusetts, USA. Communications contained a link to the survey that could be easily accessed with a single click. No compensation was offered to participants. All responses were anonymous. SurveyMonkey records the IP address, therefore limiting respondents to a single response. Reminder emails were sent periodically during the study period, which lasted 4 weeks (July–August 2016).

    View this table:
    Table 1

    Characteristics of respondents (survey questions 1–5)

    View this table:
    Table 2

    Survey questions and responses (survey questions 6–13)

    View this table:
    Table 3

    Survey questions and answers addressing treatment preferences based on aneurysm location in the majority of cases (survey questions 17–22)

    View this table:
    Table 4

    Survey questions and answers dealing with follow-up schedules after treatment of aneurysms (survey questions 23–25)

    Figure 1
    Figure 1

    Survey questions and answers dealing with candidacy for treatment based on age for patients with newly diagnosed unruptured aneurysms (survey questions 14–16). A response of 65 indicates that physicians no longer perform or recommend that treatment beyond the age of 65.

    Statistical analysis

    Questionnaire items were examined by the factors of interest: specialty, years of independent practice, practice setting, and number of aneurysms per year, using χ2 tests; when a global p value was <0.05 for an item, pairwise testing (using χ2) was performed to further explain the association. For questions related to age at which a surgical technique was no longer performed, responses were dichotomized to at or above the median versus below the median; χ2 tests were performed on these dichotomized values. AGE of respondent was compared for these factors using the Wilcoxon signed rank test. All tests were considered significant at α<0.05.

    Results

    A total of 211 individual survey responses were obtained and included in this analysis. The full list of questions and respondent answers is shown in tables 1⇑⇑–4 and figure 1. Note that some survey questions had missing responses and therefore total responses for each question may be less than 211.

    Respondent characteristics

    Respondent characteristics are shown in table 1. The majority of respondents were neurosurgeons (116; 55%). Further, the majority of respondents had been trained in endovascular techniques (171; 81%), had >5 years of personal independent practice (129; 61%), worked at academic centers (123; 58%), and treated more than 25 aneurysms a year personally (142; 67%).

    Ruptured aneurysms

    Table 2 displays questions and respondent answers for ruptured intracranial aneurysms. The vast majority of respondents recommend an endovascular-first approach for the majority of ruptured aneurysms (164; 78%) compared with a very small minority recommending a clip-first approach (6; 3%). More than one-third of respondents indicate that they routinely treat all patients with subarachnoid hemorrhage regardless of Hunt and Hess grade (79; 38%).

    Unruptured aneurysms

    When selecting patients for candidacy for treatment of unruptured aneurysms, the vast majority of respondents reported using ISUIA data (170; 80%) as a standalone or in conjunction with other natural history studies to counsel patients about the risk of conservative management. Twenty-six respondents (12%) indicated they used other natural history studies than those provided or do not use natural history studies when counseling patients.

    Table 2 displays questions and respondent answers for unruptured intracranial aneurysms. The vast majority of respondents recommend an endovascular-first approach for the majority of unruptured aneurysms (147; 71%) compared with a very small minority recommending a clip-first approach (6; 3%). Only 11% of respondents reported always or usually treating anterior circulation aneurysms of <5 mm in those without a personal or family history of ruptured aneurysms; this percentage increased to 42% in patients with a family history of a ruptured cerebral aneurysm and 76% in those with a personal history.

    Treatment strategy preference depends on the location of the aneurysm (table 3). Most wide-necked internal carotid artery aneurysms are treated with flow diversion (51%), while a plurality of anterior communicating, posterior communicating, and vertebral-posterior inferior cerebellar artery aneurysms are treated preferentially with primary coiling (47%, 47%, and 55%, respectively). The majority of respondents indicate preferentially recommending stent-assisted coiling (42%) or primary coiling (37%) for basilar terminus aneurysms. The preferred treatment strategy for middle cerebral artery (MCA) bifurcation aneurysms remains surgical clipping among the majority (67%).

    Analysis of practices (questions 6–13) based on respondent characteristics

    Physicians at academic hospitals were more likely to treat ruptured and unruptured aneurysms via an open surgical approach than those at other centers (p=0.001 and p=0.05, respectively). Neurosurgeons without endovascular training were most likely to recommend surgical clipping for both ruptured and unruptured aneurysms, followed by neurosurgeons with endovascular training, and finally, radiologists and neurologists were least likely to recommend surgical clipping (p<0.001). Additionally, those physicians practicing longer were more likely to recommend clipping for ruptured aneurysms than those practicing for a shorter length of time (p=0.04). Answers to questions 6 through 13 otherwise did not differ based on the number of aneurysms treated, type of practice, specialty, or years of practice (p>0.05).

    Age

    Treatment preferences based on age are shown in figure 1. The highest percentage of respondents indicated that they stop performing or recommending surgical clipping to patients with unruptured aneurysms once patients reach 70–75 years of age. For endovascular coiling, the highest percentage stop treating aneurysms at ages 80–85. Similarly, 80–85 is also the age range at which the highest percentage of respondents stop performing scheduled follow-up with serial imaging.

    The age at which respondents generally stop recommending surgical clipping or serial imaging did not differ based on specialty, aneurysm treatment volume, years of practice, or practice setting. However, neurosurgeons were more likely to recommend endovascular treatment of aneurysms in older individuals than radiologists or neurologists (p=0.02).

    Follow-up imaging after treatment

    Preferred follow-up post-treatment imaging schedules are shown in table 4. There is wide variation in preferred practices. In follow-up after coiling, 20% of respondents who perform coiling (n=193) obtain no catheter angiograms, while 38% obtain one, 31% obtain two, and 11% obtain at least three. After flow diversion (181 respondents), 7% obtain no catheter angiograms, 48% obtain one, 38% obtain two, and 7% obtain at least three. In contrast, after clipping surgery (148 respondents), 49% of surgeons do not obtain catheter angiograms, 45% obtain one, and only 7% obtain two or more.

    Discussion

    This survey of US physicians who perform surgical or endovascular treatment of cerebral aneurysms is the first recent survey of its kind to evaluate and quantify general aneurysm practice patterns in the USA. The results are notable for the high degree of respondent variability in determining candidacy for treatment, treatment strategy preferences, and post-treatment follow-up schedules. Survey results therefore suggest that a focus on developing evidence-based consensus recommendations involving members of all three of the major societies might be useful in standardizing practice patterns in the USA.

    The considerable advancements in endovascular devices and techniques over the past two decades have largely driven a paradigm shift from a mainstay of open CV techniques to an endovascular-first management approach at many centers. This shift has been fueled by a number of trials that have suggested equivalency of coiling and clipping, beginning with the International Subarachnoid Aneurysm Trial in 200216 and most recently with the Barrow Ruptured Aneurysm Trial extended results published in 2015.17 A more recent meta-analysis of randomized and non-randomized trials, including 85 studies, showed significantly lower mortality and higher rates of independency with coiling than with clipping.18 Our survey captures this shift, with 78% and 71% of respondents recommending endovascular treatment as first-line management for most ruptured and unruptured aneurysms, respectively. Primary coiling is reportedly the preferred technique for most anterior communicating, posterior communicating, and vertebral-posterior inferior cerebellar artery aneurysms as well as many basilar apex aneurysms. Flow diverter stents, such as the Pipeline embolization device (Medtronic-Covidien, Minneapolis, Minnesota, USA), have further revolutionized the treatment of wide-necked proximal internal carotid artery aneurysms, making aneurysm catheterization unnecessary. The increasing popularity of flow diversion is confirmed with this survey as most physicians now recommend flow diversion for most unruptured wide-necked internal carotid artery aneurysms. The endovascular-first approach shift is not all encompassing, however, as over two-thirds of respondents continue to recommend microsurgical clipping as the preferred treatment for MCA bifurcation aneurysms. Although a small number of recent series support the safety of coiling for MCA aneurysms,19 ,20 there are no randomized controlled trials specifically comparing coiling versus clipping at this location, and the most rigorous analyses to date suggest the continued superiority of clipping.21 ,22

    This survey demonstrates considerable variability among physicians in selecting patients for treatment. One specific interesting finding is the disparate treatment of patients with poor-grade subarachnoid hemorrhage. Nearly 40% of respondents indicate that they perform either clipping or coiling on all ruptured patients, regardless of Hunt and Hess14 or World Federation of Neurological Surgeons15 grade, while over half do not perform an aneurysm securing procedure on grade 5 patients unless they improve. A recent systematic analysis of the literature suggests that favorable outcomes occur in only about 30% of high-grade patients, with mortality approximating 60%.23 Some authors strongly recommend performing coiling or clipping to avoid rebleeding early and aggressively in all patients, as good outcomes are possible even in poor-grade patients.24 A prospective registry is currently evaluating poor-grade patients,25 and it is clear that further prospective evidence is needed to help standardize treatment recommendations in this patient subgroup.

    Another important finding is in the selection for treatment of patients with small, unruptured anterior circulation aneurysms. Although several natural history studies can be used for patient counseling,9 ,10 ,26–29 the most robust risk prediction analysis to date is the PHASES score, which pooled data from six prospective cohort studies (including ISUIA) to generate risk profiles based on location, size, age, race, history of rupture, and hypertension.30 Interestingly, only one-quarter of US physicians reported using PHASES for patient counseling, while the vast majority reported using ISUIA data (80%) in this manner. It is therefore expected that very few respondents reported always or usually treating anterior circulation aneurysms of <5 mm in patients without family or personal rupture history (11%), as ISUIA predicts a very low rupture risk in this population. This number is in stark contrast to a recent international survey by Alshafai and colleagues, where the majority of neurosurgeons supported unruptured aneurysm treatment regardless of aneurysm size. In Alshafai's survey, only 40% reported that they would manage a 4 mm MCA or anterior communicating artery aneurysm conservatively.31

    The fact that US physicians are predominantly relying on ISUIA for patient counseling and selection for treatment is important. The limitations of natural history studies as they pertain to cerebral aneurysms are well-described.32 ,33 Most importantly, many of the ruptured aneurysms seen in clinical practice are small,11 which is counter to the supposed risk profile of these aneurysms based on ISUIA. There is increasing evidence supporting the role of other morphological or hemodynamic characteristics in determining rupture risk, such as the size ratio, which may be a particularly important explanatory predictor for rupture of small aneurysms such as those on the anterior communicating artery.34–36 A recent case–control analysis from a subset of the original ISUIA dataset has demonstrated a significant relationship between perpendicular height and size ratio with rupture (unpublished data). As the vast majority of US physicians continue to rely on ISUIA as the predominant natural history study, updating the ISUIA risk assessment based on these other factors is needed.

    Most respondents indicated that they stop recommending surgical clipping at age 70–75, while most stop recommending endovascular treatment at 80–85 and most stop following up patients with unruptured aneurysms with serial imaging at 80–85 years. These preferences are slightly older than the data from a Nationwide Inpatient Sample database study, which suggested that the risk of treatment complication surpasses the natural history risk of rupture for unruptured aneurysms at age 61–70 for clipping and 71–80 for coiling.37 Further, age preferences were highly variable and influenced by specialty, with neurosurgeons more likely to recommend treatment of older individuals than radiologists or neurologists. Interestingly, 9% and 15% reported no upper limit of age for clipping or endovascular treatment, respectively.

    Another interesting finding is the high degree of variability seen in follow-up imaging schedules. In follow-up after coiling, 20%, 38%, 31%, and 11% of respondents who perform coiling obtain no angiogram, or one, two, and at least three catheter angiograms, respectively. These numbers differ after flow diversion, where 48% and 38% obtain one and two catheter angiograms, respectively; and after clipping, where roughly half do not obtain catheter angiograms and just under half obtain one follow-up catheter angiogram. Only 18%, 6%, and 35% of respondents exclusively use non-invasive imaging after coiling, flow diversion, or clipping, respectively, even though there are several studies suggesting non-inferiority of CT angiography or magnetic resonance angiography in detecting recanalization.38–40 A recent survey of institutional practices also demonstrated significant heterogeneity in imaging follow-up protocols, with wide variability in cost.41 Follow-up imaging may therefore be a practical area of focus where consensus recommendations can be formulated and adopted to help standardize national practices.

    This study has several important limitations. First, this survey was designed to study general treatment practices with questions specifically formulated to capture the most common strategies among physicians. Each aneurysm has specific and unique considerations, such as shape, location, rupture status, and individual patient factors that influence treatment strategy. This survey was not designed to collect data on physician treatment biases based on these important nuances. Accordingly, failure to separate treatment preferences at specific locations based on certain anatomical characteristics, such as the presence of a wide neck, may limit interpretation of the results. Second, the majority of respondents were neurosurgeons, with relative under-representation of SVIN. Multiple attempts were made to obtain responses from all three organizations to maximize the response rate. The over-representation of neurosurgeon respondents may bias the results. Further, statistical analysis comparing specialty-specific practices might, therefore, have been underpowered. Third, as a survey, this study is subject to the inherent limitations of survey methodology, including recall and selection bias. Prospective multicenter databases, such as the NeuroVascular Quality Initiative or the NeuroPoint Alliance Neurovascular Quality Outcomes Database, may be integral in providing robust scientific data to further support these findings.

    Conclusions

    This national survey of 211 US physician members of SNIS, SVIN and the CV section demonstrates considerable variability in aneurysm treatment practices for patient selection for treatment, preferred treatment strategies, and follow-up imaging schedules. Most physicians rely on ISUIA for patient counseling and most recommend an endovascular-first approach for both ruptured and unruptured aneurysms, although two-thirds continue to recommend surgical clipping for the majority of MCA bifurcation aneurysms. The high degree of variability in certain aneurysm management preferences, such as post-treatment imaging schedules, suggests that multidisciplinary consensus recommendations could be of benefit in standardizing national practices.

    References

    1. ↵
      1. Chason JL,
      2. Hindman WM
      . Berry aneurysms of the circle of Willis; results of a planned autopsy study. Neurology 1958;8:41–4.
      OpenUrl
    2. ↵
      1. de la Monte SM,
      2. Moore GW,
      3. Monk MA, et al
      . Risk factors for the development and rupture of intracranial berry aneurysms. Am J Med 1985;78(6 Pt 1):957–64.
      OpenUrlCrossRefPubMed
    3. ↵
      1. Horikoshi T,
      2. Akiyama I,
      3. Yamagata Z, et al
      . Retrospective analysis of the prevalence of asymptomatic cerebral aneurysm in 4518 patients undergoing magnetic resonance angiography--when does cerebral aneurysm develop? Neurol Med Chir (Tokyo) 2002;42:105–12; discussion 113.
      OpenUrlCrossRefPubMed
    4. ↵
      1. Agarwal N,
      2. Gala NB,
      3. Choudhry OJ, et al
      . Prevalence of asymptomatic incidental aneurysms: a review of 2,685 computed tomographic angiograms. World Neurosurg 2014;82:1086–90. doi:10.1016/j.wneu.2013.01.082
      OpenUrlPubMed
    5. ↵
      1. Winn HR,
      2. Jane JA Sr.,
      3. Taylor J, et al
      . Prevalence of asymptomatic incidental aneurysms: review of 4568 arteriograms. J Neurosurg 2002;96:43–9. doi:10.3171/jns.2002.96.1.0043
      OpenUrlCrossRefPubMedWeb of Science
    6. ↵
      1. Fiorella D,
      2. Hirsch JA,
      3. Woo HH, et al
      . Should neurointerventional fellowship training be suspended indefinitely? J Neurointerv Surg 2012;4:315–18. doi:10.1136/neurintsurg-2012-010471
      OpenUrlFREE Full Text
    7. ↵
      1. Sacco RL,
      2. Wolf PA,
      3. Bharucha NE, et al
      . Subarachnoid and intracerebral hemorrhage: natural history, prognosis, and precursive factors in the Framingham Study. Neurology 1984;34:847–54.
      OpenUrlCrossRefPubMed
    8. ↵
      1. Sekhar LN,
      2. Heros RC
      . Origin, growth, and rupture of saccular aneurysms: a review. Neurosurgery 1981;8:248–60.
      OpenUrlCrossRefPubMedWeb of Science
    9. ↵
      Unruptured intracranial aneurysms--risk of rupture and risks of surgical intervention. International Study of Unruptured Intracranial Aneurysms Investigators. N Engl J Med 1998;339:1725–33.
      OpenUrlCrossRefPubMedWeb of Science
    10. ↵
      1. Wiebers DO,
      2. Whisnant JP,
      3. Huston J III., et al
      . Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet 2003;362:103–10.
      OpenUrlCrossRefPubMedWeb of Science
    11. ↵
      1. Weir B,
      2. Disney L,
      3. Karrison T
      . Sizes of ruptured and unruptured aneurysms in relation to their sites and the ages of patients. J Neurosurg 2002;96:64–70. doi:10.3171/jns.2002.96.1.0064
      OpenUrlCrossRefPubMedWeb of Science
    12. ↵
      1. Carter BS,
      2. Sheth S,
      3. Chang E, et al
      . Epidemiology of the size distribution of intracranial bifurcation aneurysms: smaller size of distal aneurysms and increasing size of unruptured aneurysms with age. Neurosurgery 2006;58:217–23; discussion 217–223. doi:10.1227/01.NEU.0000194639.37803.F8
      OpenUrlCrossRefPubMedWeb of Science
    13. ↵
      1. Etminan N,
      2. Beseoglu K,
      3. Barrow DL, et al
      . Multidisciplinary consensus on assessment of unruptured intracranial aneurysms: proposal of an international research group. Stroke 2014;45:1523–30. doi:10.1161/STROKEAHA.114.004519
      OpenUrlAbstract/FREE Full Text
    14. ↵
      1. Hunt WE,
      2. Hess RM
      . Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg 1968;28:14–20. doi:10.3171/jns.1968.28.1.0014
      OpenUrlCrossRefPubMedWeb of Science
    15. ↵
      1. Teasdale GM,
      2. Drake CG,
      3. Hunt W, et al
      . A universal subarachnoid hemorrhage scale: report of a committee of the World Federation of Neurosurgical Societies. J Neurol Neurosurg Psychiatr 1988;51:1457.
      OpenUrlFREE Full Text
    16. ↵
      1. Molyneux A,
      2. Kerr R,
      3. 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;360:1267–74.
      OpenUrlCrossRefPubMedWeb of Science
    17. ↵
      1. Spetzler RF,
      2. McDougall CG,
      3. Zabramski JM, et al
      . The Barrow Ruptured Aneurysm Trial: 6-year results. J Neurosurg 2015;123:609–17. doi:10.3171/2014.9.JNS141749
      OpenUrlCrossRefPubMed
    18. ↵
      1. Falk Delgado A,
      2. Andersson T,
      3. Falk Delgado A
      . Clinical outcome after surgical clipping or endovascular coiling for cerebral aneurysms: a pragmatic meta-analysis of randomized and non-randomized trials with short- and long-term follow-up. J Neurointerv Surg Published Online First: 6 Apr 2016. doi:10.1136/neurintsurg-2016-012292 doi:10.1136/neurintsurg-2016-012292
    19. ↵
      1. Wang CC,
      2. Wen WL,
      3. Feng ZZ, et al
      . Endovascular treatment of 48 early branch aneurysms of the middle cerebral artery. World Neurosurg 2016;94:131–6. doi:10.1016/j.wneu.2016.06.117
      OpenUrl
    20. ↵
      1. Zhao X,
      2. Li Z,
      3. Fang X, et al
      . Treatment of ruptured middle cerebral artery aneurysms by endovascular approach: a single-center experience. Int J Neurosci 2016:1–6. [Epub ahead of print]
    21. ↵
      1. Smith TR,
      2. Cote DJ,
      3. Dasenbrock HH, et al
      . Comparison of the efficacy and safety of endovascular coiling versus microsurgical clipping for unruptured middle cerebral artery aneurysms: a systematic review and meta-analysis. World Neurosurg 2015;84:942–53.
      OpenUrl
    22. ↵
      1. Blackburn SL,
      2. Abdelazim AM,
      3. Cutler AB, et al
      . Endovascular and surgical treatment of unruptured MCA aneurysms: meta-analysis and review of the literature. Stroke Res Treat 2014;2014:348147.
      OpenUrlPubMed
    23. ↵
      1. de Oliveira Manoel AL,
      2. Mansur A,
      3. Silva GS, et al
      . Functional outcome after poor-grade subarachnoid hemorrhage: a single-center study and systematic literature review. Neurocrit Care 2016;25:338–50.
      OpenUrl
    24. ↵
      1. Schuss P,
      2. Hadjiathanasiou A,
      3. Borger V, et al
      . Poor-grade aneurysmal subarachnoid hemorrhage: factors influencing functional outcome--a single-center series. World Neurosurg 2016;85:125–9.
      OpenUrl
    25. ↵
      1. Zhao B,
      2. Tan X,
      3. Yang H, et al
      . A Multicenter prospective study of poor-grade aneurysmal subarachnoid hemorrhage (AMPAS): observational registry study. BMC Neurol 2014;14:86.
      OpenUrl
    26. ↵
      1. Juvela S,
      2. Poussa K,
      3. Lehto H, et al
      . Natural history of unruptured intracranial aneurysms: a long-term follow-up study. Stroke 2013;44:2414–21.
      OpenUrlAbstract/FREE Full Text
    27. ↵
      1. Sonobe M,
      2. Yamazaki T,
      3. Yonekura M, et al
      . Small unruptured intracranial aneurysm verification study: SUAVe study, Japan. Stroke 2010;41:1969–77. doi:10.1161/STROKEAHA.110.585059
      OpenUrlAbstract/FREE Full Text
    28. ↵
      1. Ishibashi T,
      2. Murayama Y,
      3. Urashima M, et al
      . Unruptured intracranial aneurysms: incidence of rupture and risk factors. Stroke 2009;40:313–6. doi:10.1161/STROKEAHA.108.521674
      OpenUrlAbstract/FREE Full Text
    29. ↵
      1. Morita A,
      2. Kirino T,
      3. Hashi K, et al
      . UCAS Japan Investigators. The natural course of unruptured cerebral aneurysms in a Japanese cohort. N Engl J Med 2012;366:2474–82. doi:10.1056/NEJMoa1113260
      OpenUrlCrossRefPubMedWeb of Science
    30. ↵
      1. Greving JP,
      2. Wermer MJ,
      3. Brown RD Jr., et al
      . Development of the PHASES score for prediction of risk of rupture of intracranial aneurysms: a pooled analysis of six prospective cohort studies. Lancet Neurol 2014;13:59–66. doi:10.1016/S1474-4422(13)70263-1
      OpenUrlCrossRefPubMed
    31. ↵
      1. Alshafai N,
      2. Falenchuk O,
      3. Cusimano MD
      . Practises and controversies in the management of asymptomatic aneurysms: results of an international survey. Br J Neurosurg 2015;29:758–64. doi:10.3109/02688697.2015.1096906
      OpenUrl
    32. ↵
      1. Raymond J,
      2. Roy D,
      3. Weill A, et al
      . Unruptured intracranial aneurysms and the Trial on Endovascular Aneurysm Management (TEAM): the principles behind the protocol. J Vasc Interv Neurol 2008;1:22–6.
      OpenUrlPubMed
    33. ↵
      1. Darsaut T,
      2. Fahed R,
      3. Raymond J
      . PHASES and the natural history of unruptured aneurysms: science or pseudoscience? J Neurointerv Surg Published Online First: 10 Feb 2016. doi:10.1136/neurintsurg-2016-012295
    34. ↵
      1. Xu T,
      2. Lin B,
      3. Liu S, et al
      . Larger size ratio associated with the rupture of very small (≤3 mm) anterior communicating artery aneurysms. J Neurointerv Surg Published Online First: 23 Mar 2016. doi:10.1136/neurintsurg-2016-012294
    35. ↵
      1. Kang H,
      2. Ji W,
      3. Qian Z, et al
      . Aneurysm characteristics associated with the rupture risk of intracranial aneurysms: a self-controlled study. PLoS ONE 2015;10:e0142330. doi:10.1371/journal.pone.0142330
      OpenUrl
    36. ↵
      1. Rahman M,
      2. Smietana J,
      3. Hauck E, et al
      . Size ratio correlates with intracranial aneurysm rupture status: a prospective study. Stroke 2010;41:916–20. doi:10.1161/STROKEAHA.109.574244
      OpenUrlAbstract/FREE Full Text
    37. ↵
      1. Lawson MF,
      2. Neal DW,
      3. Mocco J, et al
      . Rationale for treating unruptured intracranial aneurysms: actuarial analysis of natural history risk versus treatment risk for coiling or clipping based on 14,050 patients in the Nationwide Inpatient Sample database. World Neurosurg 2013;79:472–8. doi:10.1016/j.wneu.2012.01.038
      OpenUrlCrossRefPubMedWeb of Science
    38. ↵
      1. Okahara M,
      2. Kiyosue H,
      3. Yamashita M, et al
      . Diagnostic accuracy of magnetic resonance angiography for cerebral aneurysms in correlation with 3D-digital subtraction angiographic images: a study of 133 aneurysms. Stroke 2002;33:1803–8.
      OpenUrlAbstract/FREE Full Text
    39. ↵
      1. Pierot L,
      2. Portefaix C,
      3. Boulin A, et al
      . Follow-up of coiled intracranial aneurysms: comparison of 3D time-of-flight and contrast-enhanced magnetic resonance angiography at 3T in a large, prospective series. Eur Radiol 2012;22:2255–63. doi:10.1007/s00330-012-2466-6
      OpenUrlCrossRefPubMed
    40. ↵
      1. Wang H,
      2. Li W,
      3. He H, et al
      . 320-Detector row CT angiography for detection and evaluation of intracranial aneurysms: comparison with conventional digital subtraction angiography. Clin Radiol 2013;68:e15–20. doi:10.1016/j.crad.2012.09.001
      OpenUrlCrossRefPubMed
    41. ↵
      1. Gupta R,
      2. Griessenauer CJ,
      3. Adeeb N, et al
      . Evaluating imaging follow-up strategies and costs of unruptured intracranial aneurysms treated with endovascular techniques: a survey of academic neurovascular centers in the United States. World Neurosurg 2016;94:360–7. doi:10.1016/j.wneu.2016.07.030
      OpenUrl

    Footnotes

    • Contributors Study conception and design (JAH, KMF). Societal support and data collection (KMF, WM, JM, FA, AFD, MM, IL, JAH, JAW, SQW). Statistics (KMF, JTR). Manuscript composition (KMF, HES-B). All authors reviewed the manuscript, provided critical review, and provided final approval of the manuscript to be published.

    • Competing interests None declared.

    • Ethics approval Wake Forest institutional review board.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Data sharing statement There are no additional data.