Size of Ruptured Intracranial Aneurysms Is Decreasing: Twenty-Year Long Consecutive Series of Hospitalized Patients
Abstract
Background and Purpose—
Decrease in the incidence of subarachnoid hemorrhage over the past decades has been related to decreased smoking rates, especially among <50-year-old people. We studied whether these epidemiological changes are reflected in changes in the size and location of ruptured intracranial aneurysms (RIAs).
Methods—
We identified consecutive patients admitted to a nonprofit academic hospital with saccular RIAs between 1989 and 2008. We averaged and analyzed mean sizes of RIAs in 4-year admission groups. In statistical analysis, we used the χ2 test for categorical variables and the Kruskal–Wallis test to assess differences between continuous and categorical variables. For linear trend assessments, we used the linear-by-linear association and ANOVA tests.
Results—
Of 2660 consecutive patients (59% women) with RIAs, 1176 (44%) were <50 years on admission. In people <50 years, the averaged annual mean size of RIAs decreased 16% from 9.2 mm in 1989 to 1992 to 7.7 mm in 2005 to 2008 in women and 13% (from 9.3 to 8.1 mm) in men (decreasing linear trend; P=0.001). RIA sizes did not change in 50-year-old or older patients, whereas the proportion of posterior circulation RIAs almost tripled to 13%, also with a linear relationship (P<0.001).
Conclusions—
The size of RIAs seems to be decreasing among younger generations of hospital-admitted subarachnoid hemorrhage patients, whereas 50-year-old and older subarachnoid hemorrhage patients have an increasing proportion of posterior circulation RIAs. These epidemiological changes are noteworthy, especially if they are universal and ongoing.
Introduction
Preventive actions in healthcare originate from epidemiological evidence, and therefore changes in this evidence shape preventive actions. According to well-known treatment guidelines and risk prediction models, such as the American Heart Association and American Stroke Association guideline,1 PHASES aneurysm risk score,2 and Unruptured Intracranial Aneurysm Treatment Score model,3 the size and location of unruptured intracranial aneurysm (UIA) are key prognostic factors for future subarachnoid hemorrhage (SAH).
Nationwide incidence rates of SAH are known only in a few countries,4 and in these countries, the incidence of SAH has decreased rapidly since 1980s and 1990s.5–8 In Finland, the incidence decrease between 1998 and 2012 has been most evident among people <50 years, and this decrease has been attributed to a significant decline in smoking rates.8 Given the changed SAH incidence, that is presumably coupled with changed smoking rates, we studied whether the observed epidemiological changes are mirrored through alterations in the size and location of ruptured intracranial aneurysms (RIAs).
Methods
The data that support the findings of this study are available from one of the authors (Dr Lehto) on reasonable request.
Ethical Statement
Retrospective data collection and analysis were approved by the local ethics committee (Dnro 402/13/03/00/2015). The hospital research board waived the need for patient consent.
Study Data
Diagnostic angiographic images have been archived since 1989. The images are currently reanalyzed. By the end of June 2017, data on the size and location of RIAs were reanalyzed for consecutive patients diagnosed between January 1989 and August 2009, with 2008 being the latest full-year data available.
Diagnosis, Location, and Size of RIAs
The diagnosis of SAH is based on lumbar punctures and computed tomographic scans. For the size measurement, we used 2-dimensional computed tomographic angiography reformats or digital subtraction angiography images. Digital subtraction angiography image measurements were calibrated using the diameter of petrous internal carotid artery as a standard reference measure. We preferred digital subtraction angiography images, if available, for size measurements.
Preventive Treatments of UIAs
We also identified all adult (≥18 years) patients without a history of SAH, and who were endovascularly or surgically treated for asymptomatic UIAs between 1989 and 2008.
Statistical Analysis
Because relatively low number of annual SAH cases if divided into groups by age and sex, and to reduce the likelihood of false-positive results generated by chance, we averaged and depicted mean sizes of RIAs in 4-year admission groups (eg, patients admitted between 1989 and 1992 were grouped together). The approach is similar to the one used in reporting changing incidence rates in nationwide SAH studies.5,8 A χ2 test was used to test statistical relationships between 2 categorical variables and the linear-by-linear association test for testing trends in larger than 2×2 tables. We used the Kruskal–Wallis test to assess for differences on continuous dependent variables by categorical variables and subsequent ANOVA test for linear trend assessments. For post hoc analysis, we used the Mann–Whitney test and adjusted the P value with the Bonferroni correction. We used an IBM SPSS 24.0 statistical software for Mac OS X in statistical analyses.
Results
Study Cohort
Of 2660 patients, 59% were women and 44% <50 years (Table 1). On admission, the mean and median ages of 2660 patients were 52 years (range, 13–93 years). Only 3 patients (1 women) were <18 years.
| Mean, mm | 95% CI | Median, mm | Range, mm | |
|---|---|---|---|---|
| All | 8.7 | 8.5–8.9 | 8.0 | 2–43 |
| Women (59%, 1570 pts) | 8.6 | 8.4–8.8 | 8.0 | 2–41 |
| Men (41%, 1090 pts) | 8.9 | 8.6–9.2 | 8.0 | 2–43 |
| <50 y of age (44%, 1176 pts) | 8.5 | 8.3–8.8 | 8.0 | 2–42 |
| Women (51%, 599 of 1176 pts) | 8.4 | 8.0–8.7 | 7.0 | 2–35 |
| Men (49%, 577 of 1176 pts) | 8.6 | 8.3–9.0 | 8.0 | 2–42 |
| ≥50 y of age (56%, 1484 pts) | 8.8 | 8.6–9.1 | 8.0 | 2–43 |
| Women (65%, 971 of 1484 pts) | 8.7 | 8.4–9.0 | 8.0 | 2–41 |
| Men (35%, 513 of 1484 pts) | 9.1 | 8.7–9.6 | 8.0 | 2–43 |
| Four-year admission groups | 8.7 | 8.5–8.9 | 8.0 | 2–43 |
| 1989–1992 (19%, 517 pts) | 9.3 | 8.9–9.6 | 8.0 | 2–42 |
| 1993–1996 (17%, 450 pts) | 9.0 | 8.7–9.5 | 8.0 | 2–35 |
| 1997–2000 (20%, 539 pts) | 8.3 | 7.9–8.7 | 7.0 | 2–43 |
| 2001–2004 (22%, 598 pts) | 8.2 | 7.9–8.6 | 7.0 | 2–28 |
| 2005–2008 (21%, 556 pts) | 8.8 | 8.4–9.2 | 8.0 | 2–41 |
CI indicates confidence interval.
Changes in RIA Locations
Anterior circulation RIAs accounted for 91%, and 4 most common locations accounted for 84% of all 2660 RIAs (middle cerebral artery 33%, anterior communicating artery 32%, posterior communicating artery 14%, pericallosal artery 5%). From the first 4-year admission group (1989–1992) to the last (2005–2008), the proportion of posterior circulation RIAs of all 2660 RIAs increased from 7% to 12% (P=0.032) with a linear relationship (P=0.002), with no significant sex differences. In patients aged ≥50 years, the proportion of posterior circulation RIAs increased from 5% to 13% between the first and last 4-year admission groups (P=0.002), also with a linear relationship (P<0.001). No such changes or linear trends were observed for patients <50 years. For the 4 most common locations of RIAs, percentages did not change or have linear trends.
Size Changes of RIAs
Mean and median sizes of RIAs are presented in Table 1. Mean sizes decreased from the first 4-year admission group to the last (P<0.001; Table 1). The decreasing trend was linear (P=0.007) even though the mean size increased from the second last to the last 4-year admission group (Table 1). Furthermore, in a post hoc analysis, the mean sizes between the first and last 4-year admission groups differed (P=0.006).
In patients <50 years, the mean RIA sizes decreased linearly (P<0.001) from 9.3 mm (95% confidence interval [CI], 8.7–9.9) to 7.9 mm (95% CI, 7.3–8.4) from late 1980s to 2005 to 2008 (P<0.001; Figure A; Table 1). This decrease was evident both in women (mean size changed from 9.2 mm [95% CI, 8.5–10.0] to 7.7 mm [95% CI, 6.9–8.4]; P=0.026; linearity P=0.001) and men (mean size changed from 9.3 mm [95% CI, 8.5–10.2] to 8.1 mm [95% CI, 7.3–8.9]; P<0.001; linearity P=0.001; Figure A and B). In 50-year-old or older patients, no decreasing size changes or linear trends were observed (Figure A). In fact, the mean size increased insignificantly from 9.2 mm (95% CI, 8.7–9.7) in 1989 to 1992 to 9.3 mm (95% CI, 8.7–9.8) in 2005 to 2008, and more so in men (from 9.5 mm [95% CI, 8.5–10.5] to 10.2 mm [95% CI, 9.1–11.2]).
Preventively Treated UIAs
The number and size of treated UIAs between 1989 and 2008 were small, specifically among <50-year-old patients (Table 2).
| Year | All Patients | Under 50-Y-Old | ||||
|---|---|---|---|---|---|---|
| n | Mean, mm | Median, mm | n | Mean, mm | Median, mm | |
| 1989 | 3 | 4.3 | 4.0 | 2 | 5.5 | 5.5 |
| 1990 | 5 | 10.4 | 11.0 | 3 | 11.7 | 11.0 |
| 1991 | 3 | 6.0 | 5.0 | 3 | 6.0 | 5.0 |
| 1992 | 9 | 14.7 | 10.0 | 5 | 18.6 | 8.0 |
| 1993 | 7 | 6.9 | 5.0 | 4 | 7.8 | 5.5 |
| 1994 | 11 | 8.9 | 9.0 | 7 | 9.0 | 8.0 |
| 1995 | 9 | 9.2 | 10.0 | 3 | 10.7 | 10.0 |
| 1996 | 8 | 7.1 | 6.5 | 4 | 6.8 | 6.5 |
| 1997 | 17 | 7.4 | 7.0 | 6 | 7.2 | 7.5 |
| 1998 | 29 | 8.5 | 8.0 | 10 | 6.3 | 6.0 |
| 1999 | 29 | 7.9 | 8.0 | 8 | 10.4 | 10.0 |
| 2000 | 39 | 7.1 | 6.0 | 20 | 6.3 | 6.0 |
| 2001 | 41 | 6.6 | 5.0 | 21 | 6.0 | 5.0 |
| 2002 | 68 | 7.0 | 5.5 | 28 | 6.0 | 5.0 |
| 2003 | 63 | 6.1 | 6.0 | 21 | 5.3 | 5.0 |
| 2004 | 85 | 6.5 | 6.0 | 31 | 4.9 | 5.0 |
| 2005 | 88 | 6.2 | 5.0 | 29 | 5.8 | 4.0 |
| 2006 | 66 | 7.7 | 6.0 | 14 | 6.9 | 3.5 |
| 2007 | 92 | 6.7 | 6.0 | 27 | 5.3 | 4.0 |
| 2008 | 83 | 5.5 | 5.0 | 26 | 4.7 | 4.0 |
| Total | 755 | 6.9 | 6.0 | 272 | 6.3 | 5.0 |
Discussion
We found that the maximum diameter of RIAs decreased 15% in 20 years in patients <50 years, whereas the size of RIAs in older patients did not change. In parallel with size changes, the proportion of posterior circulation RIAs almost tripled in 50-year-old and older patients. Reasons for the observed findings remain speculative.
Conceivably, the recent decrease in the SAH incidence8 together with decreased smoking rates8 may affect aneurysm characteristics. Smoking is one of the main risk factors for intracranial aneurysm growth,9,10 and therefore any smoking-related growth changes are likely to be most prevalent among people with most dramatic changes in smoking habits. During the past decades, daily smoking has nearly halved among younger generations in Finland.8 However, changes in the prevalence of hypertension may also contribute to size changes of RIAs even though hypertension is less common among younger people. Reasons for the increased percentage of posterior circulation RIAs in 50-year-old and older patients may also relate to changes in risk factors. However, it is also possible that early survival rates for SAH from posterior circulation RIAs have improved especially among older generations, for example, because of improved emergence medical achievability and services.
It seems unlikely that preventive treatments of larger UIAs have a significant effect on our results. If preventive treatments have an effect on the size of RIAs, such effect should be more evident among 50-year-old and older patients, who are more often treated for UIAs, especially for larger ones. Moreover, the size of RIAs started to diminish already during years when preventive treatments were rarely performed, especially for patients <50 years.
This study has shortcomings. First, up to one fourth of people die suddenly from SAH before hospitalization,8,11 and these sudden deaths were not included in the study. How this may affect the study results is unclear. Second, external validity of cohort studies can always be questioned. However, the study hospital covers one third of the country’s population, and the incidence of SAH in Finland is similar to other countries with reliable incidence estimates.8 Third, the study approach did not allow us to analyze causative factors. Fourth, because of the different size measurement procedures for aneurysms detected with digital subtraction angiography and computed tomographic angiography, we may have introduced measurement errors. However, any systematic error should be identical for the whole cohort, not only for patients <50 years.
In conclusion, if critical epidemiological variables of SAH, such as size and location of aneurysm, are changing, we may need to update our knowledge on most critical risk factors for aneurysm rupture. These preliminary results warrant further validation in other countries.
References
1.
Thompson BG, Brown RD, Amin-Hanjani S, Broderick JP, Cockroft KM, Connolly ES, et al.; American Heart Association Stroke Council; Council on Cardiovascular and Stroke Nursing; Council on Epidemiology and Prevention; American Heart Association; American Stroke Association. Guidelines for the management of patients with unruptured intracranial aneurysms: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2015;46:2368–2400. doi: 10.1161/STR.0000000000000070.
2.
Greving JP, Wermer MJ, Brown RD, Morita A, Juvela S, Yonekura M, 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.
3.
Etminan N, Brown RD, Beseoglu K, Juvela S, Raymond J, Morita A, et al. The unruptured intracranial aneurysm treatment score: a multidisciplinary consensus. Neurology. 2015;85:881–889. doi: 10.1212/WNL.0000000000001891.
4.
Korja M, Kaprio J. Controversies in epidemiology of intracranial aneurysms and SAH. Nat Rev Neurol. 2016;12:50–55. doi: 10.1038/nrneurol.2015.228.
5.
Lindekleiv HM, Njølstad I, Ingebrigtsen T, Mathiesen EB. Incidence of aneurysmal subarachnoid hemorrhage in Norway, 1999-2007. Acta Neurol Scand. 2011;123:34–40. doi: 10.1111/j.1600-0404.2010.01336.x.
6.
Engberg AW, Teasdale TW. [Epidemiology of non-traumatic brain injury of sudden onset in Denmark 1994-2002]. Ugeskr Laeger. 2007;169:204–208.
7.
Koffijberg H, Buskens E, Granath F, Adami J, Ekbom A, Rinkel GJ, et al. Subarachnoid haemorrhage in Sweden 1987-2002: regional incidence and case fatality rates. J Neurol Neurosurg Psychiatry. 2008;79:294–299. doi: 10.1136/jnnp.2007.123901.
8.
Korja M, Lehto H, Juvela S, Kaprio J. Incidence of subarachnoid hemorrhage is decreasing together with decreasing smoking rates. Neurology. 2016;87:1118–1123. doi: 10.1212/WNL.0000000000003091.
9.
Juvela S, Poussa K, Porras M. Factors affecting formation and growth of intracranial aneurysms: a long-term follow-up study. Stroke. 2001;32:485–491.
10.
Villablanca JP, Duckwiler GR, Jahan R, Tateshima S, Martin NA, Frazee J, et al. Natural history of asymptomatic unruptured cerebral aneurysms evaluated at CT angiography: growth and rupture incidence and correlation with epidemiologic risk factors. Radiology. 2013;269:258–265. doi: 10.1148/radiol.13121188.
11.
Korja M, Silventoinen K, Laatikainen T, Jousilahti P, Salomaa V, Kaprio J. Cause-specific mortality of 1-year survivors of subarachnoid hemorrhage. Neurology. 2013;80:481–486. doi: 10.1212/WNL.0b013e31827f0fb5.
Information & Authors
Information
Published In
The image is taken from an article in this issue, “Late Window Paradox” by Albers et al (Stroke. 2018;49:768–771. doi: 10.1161/STROKEAHA.117.020200). The image is Figure 2.
Copyright
© 2018 American Heart Association, Inc.
Versions
You are viewing the most recent version of this article.
History
Received: 29 August 2017
Revision received: 21 November 2017
Accepted: 8 December 2017
Published online: 25 January 2018
Published in print: March 2018
Keywords
Subjects
Authors
Disclosures
None.
Sources of Funding
This study was supported, in part, by the Finnish State Research Grant (B. Rezai Jahromi).
Metrics & Citations
Metrics
Citations
Download Citations
If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Select your manager software from the list below and click Download.
- Changes in treatment of intracranial aneurysms during the last decade in a large European neurovascular center, Acta Neurochirurgica, 166, 1, (2024).https://doi.org/10.1007/s00701-024-06064-4
- Case Fatality in Patients With Aneurysmal Subarachnoid Hemorrhage in Finland, Neurology, 100, 3, (2023).https://doi.org/10.1212/WNL.0000000000201402
- Coil embolization for ruptured and unruptured very small intracranial aneurysms: A retrospective review of a 10-year single-center experience, Medicine, 102, 30, (e34493), (2023).https://doi.org/10.1097/MD.0000000000034493
- Impact of Very Small Aneurysm Size and Anterior Communicating Segment Location on Outcome after Aneurysmal Subarachnoid Hemorrhage, Neurosurgery, 92, 2, (370-381), (2022).https://doi.org/10.1227/neu.0000000000002212
- European Stroke Organisation (ESO) guidelines on management of unruptured intracranial aneurysms, European Stroke Journal, 7, 3, (LXXXI-CVI), (2022).https://doi.org/10.1177/23969873221099736
- Size at Which Aneurysms Rupture: A Hospital‐Based Retrospective Cohort From 3 Decades, Stroke: Vascular and Interventional Neurology, 2, 4, (2022)./doi/10.1161/SVIN.121.000193
- A new home for the Helsinki Neurosurgical Department — closure of Töölö Hospital after 90 years of neurosurgical history, Acta Neurochirurgica, 164, 6, (1447-1452), (2022).https://doi.org/10.1007/s00701-022-05202-0
- Aging Patient Population With Ruptured Aneurysms: Trend Over 28 Years, Neurosurgery, 88, 3, (658-665), (2021).https://doi.org/10.1093/neuros/nyaa494
- Application of unruptured aneurysm scoring systems to a cohort of ruptured aneurysms: are we underestimating rupture risk?, Neurosurgical Review, 44, 6, (3487-3498), (2021).https://doi.org/10.1007/s10143-021-01523-3
- Small Aneurysms with Low PHASES Scores Account for Most Subarachnoid Hemorrhage Cases, World Neurosurgery, 139, (e580-e584), (2020).https://doi.org/10.1016/j.wneu.2020.04.074
- See more
Loading...
View Options
Login options
Check if you have access through your login credentials or your institution to get full access on this article.
Personal login Institutional LoginPurchase Options
Purchase this article to access the full text.
eLetters(0)
eLetters should relate to an article recently published in the journal and are not a forum for providing unpublished data. Comments are reviewed for appropriate use of tone and language. Comments are not peer-reviewed. Acceptable comments are posted to the journal website only. Comments are not published in an issue and are not indexed in PubMed. Comments should be no longer than 500 words and will only be posted online. References are limited to 10. Authors of the article cited in the comment will be invited to reply, as appropriate.
Comments and feedback on AHA/ASA Scientific Statements and Guidelines should be directed to the AHA/ASA Manuscript Oversight Committee via its Correspondence page.