Elsevier

World Neurosurgery

Volume 111, March 2018, Pages e199-e205
World Neurosurgery

Original Article
Predictors of Occurrence and Anatomic Distribution of Multiple Aneurysms in Patients with Aneurysmal Subarachnoid Hemorrhage

Preliminary results of this study were presented in form of a short oral communication at the Joint Annual Meeting of the Swiss Society of Neurosurgery and the Society of Neuroradiology in Bern, Switzerland, June 8–9, 2017. Treatment and outcome data of the same patient cohort are at present in review in form of an independent original publication (MS ID: NEU-D-17-01466).
https://doi.org/10.1016/j.wneu.2017.12.046Get rights and content

Background

The literature on multiple intracranial aneurysms (MIA) in patients with aneurysmal subarachnoid hemorrhage (aSAH) focuses largely on risk factor analysis and consists essentially of retrospective cohort studies of limited sample size, or studies in populations outside Europe and North America. The purpose of this cohort study was to identify predictors for aneurysm multiplicity and to investigate the anatomic distribution of MIA in a representative Western cohort of patients with aSAH.

Methods

The Swiss Study of Subarachnoid Hemorrhage (SOS) database includes anonymized data from all tertiary neurovascular facilities in Switzerland. The dataset for 2009–2014 was used to compare characteristics of patients with aSAH and MIA and those with a single intracranial aneurysm (SIA) by means of descriptive and multivariate regression analysis.

Results

Among 1689 unselected patients with aSAH, 467 had MIA (prevalence, 27.6%). The location of the ruptured index aneurysm was correlated with the probability of finding bystander aneurysms and predicted their likely anatomic distribution. Patients with a ruptured basilar artery aneurysm (odds ratio [OR], 2.11; 95% confidence interval [CI], 1.30–3.44) or a ruptured middle cerebral artery aneurysm (OR, 1.86; 95% CI, 1.35–2.55) were at the greatest risk for having MIA. Larger size of the index aneurysm (OR per 1 mm, 1.03; 95% CI, 1.01–1.06) was also positively correlated with aneurysm multiplicity. Males were less likely than females to have MIA (OR, 0.79; 95% CI, 0.61–1.01).

Conclusions

In patients with aSAH, the location of the ruptured index aneurysm is correlated with the probability of finding bystander aneurysms, and is predictive of the sites at which bystander aneurysms are most likely to be found.

Introduction

Aneurysm formation likely results from a combination of genetic predisposition, acquired degenerative changes, and local hemodynamic stresses. Known risk factors for aneurysm formation include constitutional factors, such as female sex, age >60 years, and genetic or acquired diseases, such as polycystic kidney disease and diabetes mellitus.1 Multiple intracranial aneurysms (MIA) are found in 20%–33% of patients with aneurysmal subarachnoid hemorrhage (aSAH).2, 3 Predisposing factors for MIA include female sex, higher body mass index, smoking, and black race.4, 5, 6 In contrast to single intracranial aneurysm (SIA), hypertension and a family history of cerebrovascular disease have been associated with aneurysm multiplicity.1, 4

The available literature on MIA in patients suffering from aSAH consists largely of retrospective cohort studies of limited sample size and studies in populations outside Europe and North America.1, 4, 7 Only a few registries offer the combination of a dedicated nationwide all-inclusive registration of patients with aSAH with highly detailed data acquisition that is not part of more general stroke registries.8, 9, 10, 11, 12, 13 High-quality datasets comprising a large number of unselected patients, such as the Swiss Study on Subarachnoid Hemorrhage (SOS) registry, offer opportunities for epidemiologic research with increased accuracy and statistical power. Consequently, we expect our data to provide a more solid epidemiologic basis than earlier studies, and we anticipate that our findings will eventually apply to all Western countries with typical aging demographics and a similar health care system, meaning universal access and coverage. In sum, the purpose of this cohort study was to determine the predictors of occurrence and to investigate the anatomic distribution of MIA in a representative central European cohort of patients with aSAH.

Section snippets

Patient Registry

The SOS registry is a multicenter cohort database containing core data that are collected prospectively in a standardized manner. It is managed independently by each participating center. The registry was initiated in 2009; study details have been published elsewhere.14 Internal Review Board and Ethical Committee approval was obtained for all participating centers (under the supervision of the Geneva Ethical Committee; no. 11-233R, NAC 11-085R). Most local Ethics Committees waived the

Study Population

The locked SOS dataset for 2009–2014 includes data from a total of 1787 patients, of whom 1313 had SIA (73.5%) and 474 had MIA (26.5%). Of these, 1689 patients met the inclusion criteria for the present study, including 1222 with SIA (72.4%) and 467 (27.6%) with MIA (Supplemental Figure 1).

Predictors of Aneurysm Multiplicity and Anatomic Distribution

Ruptured anterior communicating artery (ACoA) aneurysms were the most common aneurysms in the patients with SIA, and middle cerebral artery (MCA) aneurysms were the most common ruptured aneurysms (index

Discussion

In this large nationwide cohort study, the location of the ruptured aneurysm (index aneurysm) was the single strongest predictor for the presence of additional aneurysms (Supplemental Figure 2). In addition, we found evidence of aneurysm clustering, with the location of the index aneurysm as a strong independent predictor for the likely anatomic distribution of bystander aneurysms (Table 2 and Supplemental Tables 2 and 3). Other independent predictors for MIA included female sex and larger

Conclusions

Ruptured aneurysms arising from such locations as the MCA, BA, and PCoA are more common in females than males. They tend to be larger at the time of rupture, and more often present with aneurysm multiplicity. Thus, imaging workups in patients with aSAH who harbor an index aneurysm at one of these locations should include extra-careful screening for additional aneurysms, especially at the sites at which bystander aneurysms can be expected to occur.

Acknowledgments

We thank Ethan Taub, MD, for reviewing the manuscript, Selina Ackermann for providing editorial assistance, and David Lucco for anatomical illustration (Figure 2). Further members or collaborators of the Swiss SOS Study Group that contributed to the study include: Javier Fandino, Daniel Colluccia, Marta Arrighi, Alice Venier, Dominique E. Kuhlen, Thomas Robert, Michael Reinert, Astrid Weyerbrock, Martin Hlavica, Jean-Yves Fournier, Andreas Raabe, Juergen Beck, David Bervini, Karl Schaller, Roy

References (29)

  • A.I. Qureshi et al.

    Factors associated with aneurysm size in patients with subarachnoid hemorrhage: effect of smoking and aneurysm location

    Neurosurgery

    (2000)
  • M.M. McDowell et al.

    Demographic and clinical predictors of multiple intracranial aneurysms in patients with subarachnoid hemorrhage

    J Neurosurg

    (2017)
  • C.M. Pleizier et al.

    Relation between age and number of aneurysms in patients with subarachnoid haemorrhage

    Cerebrovasc Dis

    (2002)
  • B.N. Jaja et al.

    The Subarachnoid Hemorrhage International Trialists (SAHIT) Repository: advancing clinical research in subarachnoid hemorrhage

    Neurocrit Care

    (2014)
  • Cited by (14)

    • Factors Associated with Subsequent Subarachnoid Hemorrhages in Patients with Multiple Intracranial Aneurysms

      2021, World Neurosurgery
      Citation Excerpt :

      About 15%–22% of patients with unruptured IAs (UIAs) and 20%–33% of patients with aSAH present with multiple IAs (MIAs), with a predisposition for female sex.2-9 In patients with aSAH size and location of the ruptured aneurysm (at the basilar terminus and middle cerebral artery [MCA]) is correlated with a higher possibility of finding bystander aneurysms.7 Other reported factors associated with the presence of MIAs are age >40 years, arterial hypertension, smoking, and familiar history positive for IAs.9

    • Clinical Characteristics of Ruptured Intracranial Aneurysm in Patients with Multiple Intracranial Aneurysms

      2021, World Neurosurgery
      Citation Excerpt :

      Regarding the impact of age, Liberato et al.6 reported that younger age is a risk factor for rupture in patients with MIA, whereas Juvela17 reported that MIA are more prevalent in older patients. Furthermore, the presence of MIA is more common in female individuals than in male individuals.17-20 In the present study, older age and female sex were associated with a greater prevalence of multiple intracranial aneurysms.

    • Early versus Delayed Microsurgical Clipping of Additional Unruptured Aneurysms in Patients with Aneurysmal Subarachnoid Hemorrhage

      2020, World Neurosurgery
      Citation Excerpt :

      Multiple intracranial aneurysms occur in ∼20% of patients and increase the risk of eventual rupture and aneurysmal subarachnoid hemorrhage (aSAH) relative to patients with a single aneurysm.1-3

    View all citing articles on Scopus

    Conflict of interest statement: This work was supported by departmental funds from the Department of Surgery, Basel University Hospital, University of Basel, Basel, Switzerland. The Basel Institute for Clinical Epidemiology and Biostatistics receives funding from Stiftung Institut für klinische Epidemiologie.

    View full text