Antithromboticmedications (ATMs), including antiplatelet therapy (APT) and oral anticoagulants (OACs), are widely used in current clinical practice for the prevention and treatment of a variety of cardiovascular diseases, deep vein thrombosis, and pulmonary thromboembolisms.1The long-term usage of these drugs, associated with an inherent risk of bleeding, raises concerns for unruptured cerebrovascular malformations (UCVMs), such as arteriovenous malformations (AVMs), cerebral cavernous malformations (CCMs), and intracranial aneurysms (IAs), in which the bleeding risk also poses a major threat.2,3
The increased risk of bleeding during neurosurgical procedures, both elective and emergent and leading to poor outcomes and deadly prognoses, is well established.4,5Although with regard to aspirin, in particular, many studies have recently drawn attention to its safety in elective neurosurgical procedures.6,7After hemorrhagic events, ATMs are suspended according to well-defined guidelines on timing and the need for ATM reversal agents.8ATM discontinuation, however, does not apply to endovascular procedures, given that it may induce thromboembolic complications.
The current literature is unclear on how to manage the following two clinical scenarios: 1) a patient on ATMs who presents with an incidental finding of a UCVM, and 2) a patient with a known UCVM who needs to be placed on ATMs for various clinical reasons. Therefore, this systematic review of the literature aimed to assemble the current evidence concerning the safety of ATM usage in patients with conservatively managed UCVMs, such as AVMs, CCMs, and IAs. The primary objective of our review was to clarify whether there is an increased risk of bleeding for patients with UCVMs on ATMs, including the incidence of hemorrhagic events and the severity of the hemorrhagic event itself. Ultimately, the goal was to provide neurosurgeons with a risk-benefit analysis of ATMs in patients with UCVMs in order to facilitate the clinical decision-making process.
开云体育世界杯赔率
Search Strategy
A systematic review of the literature according to the Preferred Reporting Items for Systematic Review and Meta-Analysis Protocols (PRISMA-P) guidelines was performed (Fig. 1). We searched two online databases—MEDLINE/PubMed and Embase—using the following free terms, keywords, or MeSH terms: "intracranial arteriovenous malformation," "intracranial cavernous haemangiomas," "cerebral cavernous malformation," "intracranial aneurysm," "anticoagulants," "haemorrhage," "intracranial bleeding," "subarachnoid haemorrhage," "antithrombotic agents/drugs," and "delayed cerebral ischemia" with AND, OR, or NOT operators. All English-language papers published over a 20-year period from January 2001 to December 2021 were considered.
PRISMA 2020 flow diagram illustrating study selection.
From the initial results page, we selected randomized and nonrandomized studies, as well as prospective and retrospective cohort studies. Due to limited data on the subject matter, we included case reports while excluding letters and editorials. Duplicates were removed. We did not request missing study data from the authors whose papers omitted such data. The titles and abstracts from the search results page were independently screened for eligibility by three review authors (A.B., P.F., and A.P.) to identify studies fulfilling the following inclusion criteria: inclusion of an adult population (> 18 years) on ATMs with a diagnosis of UCVM that reported the number of bleeding events. Studies in which ATMs were initiated after treatment (surgical or endovascular) were not considered, and only studies in which ATMs were ongoing at the time of UCVM bleeding were included. Due to the heterogeneity of UCVMs, we extrapolated and grouped data individually for each type of UCVM (AVM, CCM, and IA). Each paper’s full text was read and critically evaluated by the same three review authors. Disagreements were resolved through consensus after a thorough discussion of the conflicting article. The reference lists were also screened to identify additional relevant papers.
Outcome Definition
Two primary outcomes were reported for all UCVMs: 1) bleeding risk (number of bleeding cases/total cases), when both bleeding and nonbleeding cases were included; or 2) total number of bleeding cases, when only cases that bled were included. With respect to IAs, we noted an additional primary outcome of delayed cerebral ischemia (DCI) and secondary outcomes of morbidity, defined as major neurological deficits, and mortality. The findings of the risk of bias assessment are shown inFig. 2。9
Risk of bias assessment of the included studies.
Considering the heterogeneity of the pathologies addressed in this review, both theResultsandDiscussionhave been divided into sections according to the specific underlying pathology: AVMs, CCMs, or IAs. Although there are significant differences between the mechanisms of action of APT and OACs, as well as between AVMs and CCMs in the literature, our results discussed these two therapies used in combination as ATMs. Meanwhile, for IAs, there were sufficient data to discuss APTs and OACs separately.
Results
The initial search resulted in a total of 660 papers. After the exclusion of duplicates, 126 papers published before 2001, and 36 non–English-language papers, the titles and abstracts of 425 studies were evaluated. An additional 156 studies were excluded, yielding 269 studies for full-text evaluation. Of these 269 papers, 254 were excluded as they did not fulfill the inclusion criteria (Fig. 1). In the end, 2 papers about AVMs,10,114 about CCMs,12–15and 9 about IAs16–24were included in the systematic review.
Arteriovenous Malformation
As far as AVMs are concerned, only 2 retrospective studies met the inclusion criteria (Table 1). In a 2018 retrospective study of 77 patients with an AVM, Sturiale et al.10found that 10 of them were receiving long-term ATMs at the time of diagnosis. Not only did the authors find no significant difference in the rates of hemorrhagic onset between the ATM group and the non-ATM group (40% vs 55% hemorrhage rate, respectively), but also they discovered that none of the patients who continued taking ATMs after AVM diagnosis had hemorrhagic events over time. The other study, conducted by Edwards et al.,11focused on hereditary hemorrhagic telangiectasia (HHT), which is a genetic disease often characterized by the presence of brain AVMs. Even though they showed that ATMs had a relatively safe drug profile in most of the patients with HHT, a solid comparison with sporadic brain AVMs cannot be made given the differing characteristics of HHT and AVM (e.g., bleeding rate, dimensions).25
Summary of the included studies on AVM
| Authors & Year | Type of Study | No. of Patients | No. of Patients on ATM | Type of ATM | Hemorrhage Rate w/o ATM (%) | Hemorrhage Rate w/ ATM (%) | Follow-Up Time | Conclusions |
|---|---|---|---|---|---|---|---|---|
| Sturiale et al., 201810 | Retrospective cohort | 77 | 10 | ACT, APT | 55 | 40 | 4 yrs | No association btwn ATM & AVM bleeding |
| Edwards et al., 201211 | Retrospective cohort | 31 | 4 | ACT, APT | 0 | 0 | Not available | No association btwn ATM & AVM bleeding |
ACT = anticoagulant therapy.
Cerebral Cavernous Malformation
With respect to CCMs, the literature search yielded 4 cohort studies.12–15,26These studies affirmed the absence of a correlation between ATM usage and increased risk of CCM bleeding, with a hemorrhage rate of 0%–2% in the ATM group and 2.5%–12.0% in the non-ATM group over an average 5-year follow-up period (Table 2). The 4 recent studies—1 prospective and 3 retrospective—are methodologically valid with reasonably long follow-up periods and large case series. The distinction between APT and OACs is not discussed within our article because there were no significant differences between the two therapies in any study. Of note, in the study by Zuurbier et al.,12which was associated with the meta-analysis, a protective factor of ATMs was suggested in regard to CCM intracranial bleeding.
Summary of the included studies on CCM
| Authors & Year | Type of Study | No. of Patients | No. of Patients on ATM (%) | Median Follow-Up (yrs) | Annual Hemorrhage Rate w/o ATM | Annual Hemorrhage Rate w/ ATM | Conclusions |
|---|---|---|---|---|---|---|---|
| Zuurbier et al., 201912 | Retrospective cohort & metanalysis | 300 | 61 (20.3) | 7.4 | 12 | 2 | 协会btwn ATM和CCM hemorrhag的风险降低e |
| Bervini et al., 201913 | Retrospective cohort | 408 (492) | 91 (22.3) | 3.9 | 2.5 | 0.7 | No association btwn ATM & CCM bleeding |
| Flemming et al., 201315 | Retrospective cohort | 292 | 40 | Not available | Not available | 0.41 | No association btwn ATM & CCM bleeding |
| Schneble et al., 201214 | Prospective cohort | 87 (738) | 16 (18) | 3.9 | Not available | 0 | No association btwn ATM & CCM bleeding |
Aneurysms
Nine IA studies met the inclusion criteria: 1 prospective cohort study23and 8 retrospective cohort studies.16–22,24,27,28Of these, 6 focused on ruptured aneurysms and whether ATMs were previously administered or not, 5 on follow-up of patients with unruptured aneurysms, and 1 on both scenarios. Untreated and surgically or endovascularly treated patients were included. The results are summarized inTable 3。大部分的数据APT IAs地址;其他e are only a few papers on OACs and they are predominantly concerned with the endovascular treatment period.
Summary of the included studies on IA
| Authors & Year | Type of Study | No. of Aneurysms on ATM (%) | Ruptured or Unruptured Aneurysm | Treatment | Type of Medication | Mortality | Morbidity | IB or DCI | Conclusions |
|---|---|---|---|---|---|---|---|---|---|
| Nakamizo et al., 201716 | Retrospective cohort | 42 (11.2) | Unruptured | Surgical | APT, ACT | No difference | 8.9% (ATM) vs 3.9% (no ATM) | IB in 13.3% (ATM) vs 3.9% (no ATM) | IB incidence increased in ATM group |
| Gross et al., 201417 | Retrospective cohort | 114 (15.3) | Unruptured | Not available | APT | Not available | Not available | IB in 40% (no ATM) vs 28% (ATM) | Lower rate of hemorrhagic presentation w/ APT |
| Simard et al., 201318 | Retrospective cohort | 43 (50) | Ruptured | Surgical & endovascular | ACT, intravenous LDH | 1 (no ACT) vs 0 (ACT) | 25(58%)(没有行为)和16 (37%)(ACT)排放rehabilitation centers | DCI in 9 (21%) (no ACT) vs 0 (0%) (ACT) | Postprocedural LDH use may be safe & beneficial in patients w/ ruptured aneurysms |
| Fuji et al., 202019 | Retrospective cohort | 8 (5.16) | Ruptured | Endovascular | APT, ACT | Not available | Not available | IB in 0 (0%) (ACT) vs 5 (3.4%) (no ACT), delayed aneurysm rupture in 2 (25%) (ACT) vs 0 (0%) (no ACT) | Additional ACT before flow diverter placement does not reduce ischemic complications compared w/ dual APT but does increase hemorrhagic complications |
| Toussaint et al., 200420 | Retrospective cohort | 29 (9.5) | Ruptured | Surgical & endovascular | APT | 0 | 62.5% w/ rebleeding vs 31.3% w/o rebleeding | Not available | No significant effect of previous aspirin use on overall outcome after aSAH |
| Narata et al., 201921 | Retrospective cohort | 113 | Unruptured | Endovascular | ACT (HGH vs LDH) | 3 (4.2%) (HDH) vs 1 (1.2%) (LDH) | Symptomatic neurological complications in 8 (11.1%) (HDH) vs 1 (1.2%) (LDH) | IB in 5 (6.9%) (HDH) vs 1 (1.2%) (LDH) | LDH administered during endovascular procedure decreased the overall number of symptomatic neurological complications |
| Nisson et al., 202022 | Retrospective cohort | 347 | Ruptured & unruptured | Surgical | ACT, APT | 4% (no ATM) vs 2% (ATM) | No difference | IB in 10% (clopidogrel) vs 46% (control) & 16% (ASA) vs 51% (control) | Patients receiving APT were less likely to present w/ ruptured aneurysms; no difference w/ ACT |
| Hasan et al., 201123 | Prospective cohort | 271 | Ruptured | Surgical & endovascular | APT | Not available | Not available | Odds ratio 0.40–0.87 for IB in aspirin group vs control group | Aspirin use may confer a protective effect against risk of IA rupture |
| Dasenbrock et al., 201724 | Retrospective cohort | 353 | Ruptured | Surgical & endovascular | ACT, APT (aspirin) | 19.4% (ACT) vs 12.6% (no ACT) & 13.5% (APT) vs 12.6% (no APT) | Poor outcomes in 53.6% (ACT) vs 37.6% (no ACT) & 36.1% (APT) vs 37.8% (no APT) | IB (APT) 9.8% vs 9.7% (APT) & (ACT)和10.2%9.7% (no ACT) | APT & ACT were not associated w/ differential mortality or complication rates after SAH |
ASA = acetylsalicylic acid; HDH = high-dose heparin; IB = intracranial bleeding; LDH = low-dose heparin.
Taking into account only original studies, the risk of bleeding for unruptured and treated aneurysms on APT varied from 13% to 28%,16,17while the risk was estimated at 3% to 40% in the control group without APT. Similarly, the risk of presenting with subarachnoid hemorrhage (SAH) among those patients receiving APT ranged from 10% to 28% and in those not receiving APT from 40% to 51%.22,24In summary, 2 articles suggested a lower rate of hemorrhagic presentation with APT, 1 demonstrated augmented bleeding risk, and 1 was inconclusive.
In terms of secondary outcomes, the mortality rate ranged from 4% to 12.6% in patients not on ATMs and from 2% to 19.4% in the ATM group, including those with both ruptured and unruptured IAs.21,22,24Poor neurological outcomes were found in 8.9%–11.1% (of those receiving ATMs) and 1.2%–3.9% (of those not receiving ATMs) of unruptured IA cases16,21versus 37%–53.6% (ATMs) and 37.6%–58% (no ATMs) of ruptured IA cases.18,24The incidence rate of DCI, for both surgically and endovascularly treated ruptured IAs, ranged from 0% in patients without ATMs to 21% in patients with ATMs.18
Discussion
Arteriovenous Malformations
Brain AVMs are high-flow cerebrovascular malformations characterized by abnormal connections between afferent arteries and draining veins, without an interposing capillary net, and a high risk of severe intracranial bleeding. Prior reviews on brain AVMs have noted an incidence of 1.12–1.42/100,000 person-years29–32and described the most common presenting symptoms as hemorrhage (occurring in as many as 50% of patients), headache, or seizure.33AVMs carry a risk of spontaneous bleeding of up to 2%–4% per year, or up to 78% in a lifetime. Of note, this risk depends on several AVM characteristics such as previous rupture, location of the malformation nidus, type of venous drainage, and presence of a concurrent aneurysm.33–35
Unfortunately, there is limited information in the literature about ATMs and their role in the risk of AVM-related intracranial hemorrhage (ICH). Management of these patients is often determined by surgeons and neuroradiologists on the basis of personal experience and opinions. The first randomized controlled trial (A Randomized Trial of Unruptured Brain Arteriovenous Malformations [ARUBA]) demonstrated increased rates of stroke and mortality associated with intervention compared with medical management.36,37Therefore, this translated to an increasing number of patients entering conservative management and regular neuroradiological follow-up instead of surgery, leading to a greater number of patients reaching an age where they may develop cardiovascular diseases requiring ATMs. Despite this scenario becoming more frequent, the association between ATMs and risk of intracranial bleeding still remains poorly understood for any kind of cerebrovascular malformation.
The rates of in-hospital mortality and poor outcomes in patients with SAH appear to be higher among long-term ATM users;29however, other studies show that correct use of aspirin is associated with lower adjusted odds of aneurysmal SAH (aSAH).38Given that inflammation is considered an important player in the formation and rupture of brain aneurysms and AVMs, these latter studies suggest the importance of the anti-inflammatory properties of aspirin in protecting against AVM hemorrhage.39,40如前所述,本文只找到2 AVMstudies, of which 1 included only a subset of AVM patients with HHT, for a total of only 14 patients receiving ATMs. With such a small number of AVM patients on ATMs—even though an increased risk of neither hemorrhagic presentation nor rebleeding was demonstrated—it is impossible to express strong conclusions regarding the safety of long-term ATM use. For the same reason, it was also impossible to report a difference in management between AVMs with previous bleeding and those without, nor a difference between APT and OACs. In light of the fact that AVMs have an increasingly longer clinical course, involving radiosurgery rather than surgery itself, further studies are needed to define the impact of ATMs on the risk of bleeding in the natural history of this disease.
Cerebral Cavernous Malformations
CCM是第二个最常见的血管finding after aneurysm on brain MRI, with a prevalence of 1 in 625 neurologically asymptomatic people. Overall, CCMs have a prevalence of 0.1%–0.5%, representing 10%–20% of all cerebrovascular lesions, and may arise in either sporadic or autosomal dominant forms.26,32These patients can be asymptomatic, symptomatic with seizures or stroke caused by CCM-related ICH, or symptomatic with focal neurological deficits without radiological signs of recent bleeding. Similar to other neurovascular pathologies, the use of ATMs in CCMs is burdened by the theorical risk of bleeding; however, unlike AVMs and IAs, CCMs are less likely to have a surgical indication and thus more likely to be managed conservatively over long periods of time. Even in the event of a CCM bleed, this is usually of little concern and causes relatively minor neurological deficits to the patient. The bleeding rates of CCMs are approximately 0.5% and 2.8% per patient-year for supratentorial and brainstem lesions, respectively.26Thus, greater attention should be paid to these patients with untreated CCMs who may require ATMs for future medical reasons during their long follow-up period.
ATMs may play a protective role in regard to intracranial bleeding caused by CCM rupture. The association between long-term ATM use and lower risk of ICH is based on the theory that these bleeding events may be triggered by thrombus formation either in an associated developmental venous anomaly or within the dilated caverns of a CCM caused by slow or stagnant blood flow. Nonetheless, this relationship could also be due to the fact that CCM hemorrhage is more common in younger than older patients, and older patients are more likely to require ATMs. To address this potential confounding variable, Zuurbier et al.12adjusted for age and still found a statistically significant association between ATM use and lower rates of CCM rupture. As such, ATMs may improve outcomes and reduce the risk of recurrent bleeding in CCMs.
Aneurysms
Accounting for almost 85% of nontraumatic SAH cases, IAs affect nearly 3.2% of the population.22,41In patients harboring unruptured IAs, the use of ATMs, especially after bleeding, is controversial20,27and must be addressed.17A protective role of aspirin has been reported in the context of SAH; however, the risk of devastating bleeding events is still a concern for patients with IAs on ATMs.22,24,42
Antiplatelet Therapy
The protective role of APT, such as aspirin, has been suggested in several studies that have shown a reduced risk of SAH of 33%–73%;22this has been attributed to the anti-inflammatory effects of these molecules. Attention should instead be focused on the timing of APT intake.
In the International Study of Unruptured Aneurysms, Hasan et al.23found that 271 patients who were taking aspirin at least 3 times per week to daily had decreased risk of aSAH. Moreover, long-term use (> 1 year) of low-dose aspirin was found to be protective against SAH by Cea Soriano et al.42This finding was corroborated by Dasenbrock et al.24who, in a 2017 retrospective analysis of 1509 patients, also demonstrated that patients on APT had significantly lower odds of a cardiac complication or a venous thromboembolic event and patients on long-term APT had shorter hospital length of stay and fewer nonroutine discharges. In a retrospective series of 63 patients taking APT, Nisson et al.22highlighted the protective role of APT in contributing to a significantly lower risk of IA rupture and subsequent SAH. In the present study, however, the timing of APT intake was not specified. Another 2014 retrospective analysis of 717 patients with IAs performed by Gross et al.17showed a greater risk of hemorrhage in patients not taking aspirin compared with patients taking aspirin (40% vs 28%). Furthermore, of the 274 patients who presented with aSAH, 81 were taking aspirin and no significant difference in presenting clinical or radiographic grade was found. In a 2013 study by García-Rodríguez and colleagues43involving 1340 patients with SAH, long-term low-dose aspirin therapy was found to have a protective effect against SAH, especially for patients on long-term aspirin therapy (> 3 years). Equally important was the finding that aspirin did not increase the risk of ICH. The results from an early 2004 retrospective study by Toussaint et al.20indicated that the overall clinical outcomes after aSAH in patients taking aspirin before hemorrhage were not different from those who were not taking aspirin. However, trends toward an increased risk of rebleeding and a decreased risk of a permanent neurological deficit from vasospasm were seen in patients who used aspirin before they had SAH. In contrast to these abovementioned findings, a 2017 meta-analysis by Phan et al. of 226 patients demonstrated that those who received aspirin had an increased risk of SAH in the first 3 months of use.27
Although long-term APT use was associated with some benefits in terms of the prevention of aneurysmal rupture and lack of worsening outcomes in cases of SAH, care needs to be taken in the perioperative period for the neurosurgical treatment of unruptured IAs. Nakamizo et al.16analyzed 401 patients and showed no particular risks in terms of mortality, morbidity, or symptomatic brain infarction; however, ICH occurred more frequently in the ATM group than in the non-ATM group. Conversely, a 2003 meta-analysis by Dorhout Mees et al.28demonstrated that the administration of APT after aSAH reduced the risk of DCI, while the ICH risk was not substantially higher if APT was started before surgery.
OACs and Heparin
Regarding the use of OACs in patients with IAs, there are less data in the literature, but most articles support the evidence of an increased risk of bleeding and worse outcomes. In the study by Dasenbrock et al.,24long-term use of OACs was associated with a higher rate of complications after SAH, nonroutine discharge, and longer length of stay. In the same manner, systemic anticoagulation with warfarin therapy has been associated with poor outcomes after aSAH.20In only one retrospective analysis were OACs not associated with an increased risk of aSAH: this was the case for the subgroup of 12 patients taking OACs in the study by Nisson et al.22Overall, ATMs are relatively safe in patients harboring IAs, with APT performing better than OACs, as demonstrated by Fujii et al.19In this study, 155 patients with unruptured IAs received dual APT before endovascular treatment. Patients on long-term OACs were more likely to have delayed aneurysm ruptures with hemorrhagic complications and no reductions in the incidence of ischemic complications, additional treatment, and incomplete obliteration at final follow-up.
Finally, the use of low-dose heparin in patients with IAs was investigated by only a few articles. Narata et al.21demonstrated that the administration of low-dose heparin during endovascular treatment decreased the overall number of symptomatic neurological complications without any statistically significant association with hemorrhagic complications. Meanwhile, Simard et al.18showed that patients who were administered a low-dose intravenous heparin infusion within 48 hours of SAH experienced significantly fewer occurrences of symptomatic vasospasm and infarcts compared with controls. Likewise, Hoh et al.44found that heparinization for cerebral aneurysm coiling can be safely performed even after external ventricular drain placement within 24 hours.
Limitations
As previously mentioned in the specific subsections, the currently available data in the literature on this topic are extremely limited and heterogeneous, particularly with regard to study design, inclusion criteria, and outcome definition. For these reasons, a proper quantitative analysis could not be performed.
Almost all of the included studies were retrospective cohort studies (13 of 15), with only 2 prospective and no randomized controlled trials. Furthermore, the risk of bias assessment of the included studies highlighted a high or unclear risk of bias in more than 50% of them.
Future Perspectives
本文的结果应被视为一个wide overview of the topic of UCVMs and ATMs. Future research should consider the relationship of AVMs, CCMs, and IAs with APT and OACs independently. In particular for CCMs, further studies should focus on discovering a possible protective role of ATMs against CCM bleeding. The management of ATMs in patients with IAs needs to be further investigated, with prospective studies focusing separately on APT and OACs, as well as distinguishing between ruptured and unruptured aneurysms and between surgical and endovascular treatment.
Conclusions
Data on AVMs and ATMs are limited and weak, relying on small case series. Nevertheless, there is no evidence for either an increased risk of ICH in patients with AVMs who are receiving ATMs or the need to interrupt ATMs in those patients who have been diagnosed with sporadic, unruptured brain AVMs.
With respect to CCMs, the literature review suggested the safety of ATMs in these patients.
IAs而言,使用自动取款机re complex and debated because the benefits of ATMs may vary according to the type of intervention and specific drug administered. Evidence supports the continuation of long-term APT in patients newly diagnosed with an IA,17,41whereas starting APT in patients with incidentally discovered IAs as a means of prophylaxis against rupture is unclear.
Appendix
Search string for PubMed/MEDLINE: ("brain arteriovenous malformation" or "cavernous haemangiomas" or "cerebral cavernous malformation" or "aneurysm") and ("anticoagulants" or "antithrombotic agents" or "antiplatelet" or "antithrombotic" or "antithrombotic drug") and ("haemorrhage" or "intracranial bleeding" or "subarachnoid haemorrhage" or "delayed cerebral ischemia"). Search string for Embase: ("brain arteriovenous malformation" or "intracranial arteriovenous malformation") and ("anticoagulants" or "antiplatelet") and "haemorrhage"; "intracranial aneurysm" and ("anticoagulants" or "antiplatelet") and "subarachnoid hemorrhage" and "delayed cerebral ischemia"; and ("cavernous haemangioma" or "brain cavernous malformation") and ("anticoagulants" or "antiplatelet") and ("bleeding" or "haemorrhage").
Disclosures
The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.
Author Contributions
Conception and design: Bianconi, Ceraudo, Prior, Fiaschi. Acquisition of data: Bianconi, Minardi, Allevi. Analysis and interpretation of data: Bianconi, Ceraudo, Minardi, Allevi. Drafting the article: Bianconi, Ceraudo, Minardi, Allevi. Critically revising the article: Ceraudo, Nico, Zona, Fiaschi. Reviewed submitted version of manuscript: Bianconi, Nico, Zona, Fiaschi. Approved the final version of the manuscript on behalf of all authors: Bianconi. Administrative/technical/material support: Allevi. Study supervision: Bianconi, Garbossa, Fiaschi.
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22 ↑
NissonPL,MeybodiT,SecombTW,BergerGK,RoeDJ,LawtonMT。Patients taking antithrombotic medications present less frequently with ruptured aneurysms。World Neurosurg。2020;136:e132–e140。
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23 ↑
HasanDM,MahaneyKB,BrownRDJr,et al.Aspirin as a promising agent for decreasing incidence of cerebral aneurysm rupture。Stroke。2011;42(11):3156–3162。
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24 ↑
DasenbrockHH,YanSC,GrossBA,et al.The impact of aspirin and anticoagulant usage on outcomes after aneurysmal subarachnoid hemorrhage: a Nationwide Inpatient Sample analysis。J Neurosurg。2017;126(2):537–547。
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25 ↑
BrinjikjiW,IyerVN,WoodCP,LanzinoG。Prevalence and characteristics of brain arteriovenous malformations in hereditary hemorrhagic telangiectasia: a systematic review and meta-analysis。J Neurosurg。2017;127(2):302–310。
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26 ↑
HorneMA,FlemmingKD,SuIC,et al.Clinical course of untreated cerebral cavernous malformations: a meta-analysis of individual patient data。Lancet Neurol。2016;15(2):166–173。
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27 ↑
PhanK,MooreJM,GriessenauerCJ,OgilvyCS,ThomasAJ。Aspirin and risk of subarachnoid hemorrhage: systematic review and meta-analysis。Stroke。2017;48(5):1210–1217。
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28 ↑
Dorhout MeesSM,RinkelGJE,HopJW,AlgraA,van GijnJ。Antiplatelet therapy in aneurysmal subarachnoid hemorrhage: a systematic review。Stroke。2003;34(9):2285–2289。
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29 ↑
HillmanJ。Population-based analysis of arteriovenous malformation treatment。J Neurosurg。2001;95(4):633–637。
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30
StapfC,MastH,SciaccaRR,et al.The New York Islands AVM Study: design, study progress, and initial results。Stroke。2003;34(5):e29–e33。
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31
GabrielRA,KimH,SidneyS,et al.Ten-year detection rate of brain arteriovenous malformations in a large, multiethnic, defined population。Stroke。2010;41(1):21–26。
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32 ↑
Al-ShahiR,BhattacharyaJJ,CurrieDG,et al.Prospective, population-based detection of intracranial vascular malformations in adults: the Scottish Intracranial Vascular Malformation Study (SIVMS)。Stroke。2003;34(5):1163–1169。
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33 ↑
AbecassisIJ,XuDS,BatjerHH,BendokBR。Natural history of brain arteriovenous malformations: a systematic review。Neurosurg Focus。2014;37(3):E7。
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34
StapfC,MastH,SciaccaRR,et al.Predictors of hemorrhage in patients with untreated brain arteriovenous malformation。Neurology。2006;66(9):1350–1355。
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35 ↑
ChoiJH,MastH,SciaccaRR,et al.Clinical outcome after first and recurrent hemorrhage in patients with untreated brain arteriovenous malformation。Stroke。2006;37(5):1243–1247。
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36 ↑
LaaksoA,DashtiR,SeppänenJ,et al.Long-term excess mortality in 623 patients with brain arteriovenous malformations。开云体育app官方网站下载入口。2008;63(2):244–255。
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37 ↑
MohrJP,ParidesMK,StapfC,et al.Medical management with or without interventional therapy for unruptured brain arteriovenous malformations (ARUBA): a multicentre, non-blinded, randomised trial。Lancet。2014;383(9917):614–621。
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38 ↑
GarbeE,KreiselSH,BehrS。Risk of subarachnoid hemorrhage and early case fatality associated with outpatient antithrombotic drug use。Stroke。2013;44(9):2422–2426。
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39 ↑
SturialeCL,PucaA,SebastianiP,et al.Single nucleotide polymorphisms associated with sporadic brain arteriovenous malformations: where do we stand?Brain。2013;136(Pt 2):665–681。
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40 ↑
ChyatteD,BrunoG,DesaiS,TodorDR。Inflammation and intracranial aneurysms。开云体育app官方网站下载入口。1999;45(5):1137–1147。
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41 ↑
StarkeRM,ChalouhiN,DingD,HasanDM。Potential role of aspirin in the prevention of aneurysmal subarachnoid hemorrhage。Cerebrovasc Dis。2015;39(5-6):332–342。
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42 ↑
Cea SorianoL,GaistD,Soriano-GabarróM,BromleyS,García RodríguezLA。Low-dose aspirin and risk of intracranial bleeds: an observational study in UK general practice。Neurology。2017;89(22):2280–2287。
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43 ↑
García-RodríguezLA,GaistD,MortonJ,CooksonC,González-PérezA。Antithrombotic drugs and risk of hemorrhagic stroke in the general population。Neurology。2013;81(6):566–574。
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44 ↑
HohBL,NogueiraRG,LedezmaCJ,PryorJC,OgilvyCS。Safety of heparinization for cerebral aneurysm coiling soon after external ventriculostomy drain placement。开云体育app官方网站下载入口。2005;57(5):845–849。
