You are on page 1of 6

Prevalence and Risk of Rupture of Intracranial Aneurysms

A Systematic Review
Gabriel J.E. Rinkel, MD; Mamuka Djibuti, MD; Ale Algra, MD; J. van Gijn, MD, FRCPE

Background and Purpose—The estimates on the prevalence and the risk of rupture of intracranial saccular aneurysms vary
widely between studies. We conducted a systematic review on prevalence and risk of rupture of intracranial aneurysms and
classified the data according to study design, study population, and aneurysm characteristics.
Methods—We searched for studies published between 1955 and 1996 by means of a MEDLINE search and a cumulative
review of the reference lists of all relevant publications. Two authors independently assessed eligibility of all studies and
extracted data on study design and on numbers and characteristics of patients and aneurysms.
Results—For data on prevalence we found 23 studies, totalling 56 304 patients; 6685 (12%) of these patients were from 15
angiography studies. Prevalence was 0.4% (95% confidence interval, 0.4% to 0.5%) in retrospective autopsy studies, 3.6%
(3.1 to 4.1) for prospective autopsy studies, 3.7% (3.0 to 4.4) in retrospective angiography studies, and 6.0% (5.3 to 6.8)
in prospective angiography studies. For adults without specific risk factors, the prevalence was 2.3% (1.7 to 3.1); it tended
to increase with age. The prevalence was higher in patients with autosomal dominant polycystic kidney disease (relative
risk [RR], 4.4 [2.7 to 7.2]), a familial predisposition (RR, 4.0 [2.7 to 6.0]), or atherosclerosis (RR, 2.3 [1.7 to 3.1]). Only
8% (5 to 11) of the aneurysms were .10 mm. For the risk of rupture, we found nine studies, totalling 3907 patient-years.
The overall risk per year was 1.9% (1.5 to 2.4); for aneurysms 510 mm, the annual risk was 0.7% (0.5 to 1.0). The risk
was higher in women (RR, 2.1[1.1 to 3.9]) and for aneurysms that were symptomatic (RR, 8.3 [4.0 to 17]), .10 mm
(RR, 5.5 [3.3 to 9.4]), or in the posterior circulation (RR, 4.1 [1.5 to 11]).
Conclusions—Data on prevalence and risk of rupture vary considerably according to study design, study population, and
aneurysm characteristics. If all available evidence with inherent overestimation and underestimation is taken together, for
adults without risk factors for subarachnoid hemorrhage, aneurysms are found in approximately 2%. The vast majority of
these aneurysms are small (510 mm) and have an annual risk of rupture of approximately 0.7%. (Stroke.
Downloaded from http://ahajournals.org by on December 27, 2022

1998;29:251-256.)
Key Words: subarachnoid hemorrhage n aneurysms n epidemiology n systematic review

U ncertainty surrounds the prevalence of unruptured saccular


aneurysms on intracranial arteries. In angiographic and
autopsy studies, estimates for prevalence vary between 2 and 90
aneurysms would mean that unruptured aneurysms are less
dangerous.
We conducted a systematic review of all reports on preva-
per 1000.1,2 This wide range probably reflects methodological lence of intracranial aneurysms and classified the data according
differences between studies: prospective or retrospective de- to study design, diagnostic methods, and study population. To
signs, diagnostic tools (angiography or autopsy), and study assess the accuracy of the data on prevalence, we also system-
populations. Many studies have included patients with rup- atically reviewed data on the risk of SAH in patients with
tured aneurysms, which results in too high a prevalence. On unruptured intracranial aneurysms because prevalence com-
the other hand, studies reviewing routine autopsy records or bined with annual risk of rupture should equal the incidence of
angiograms of only a single carotid artery probably underesti- SAH. This calculated incidence can then be compared with the
mate the prevalence. Accurate data on the prevalence of incidence observed in the population.5
intracranial aneurysms are essential in evaluating the results of
screening programs for aneurysms in patients with increased Methods
risk for SAH such as patients with ADPKD3 or first-degree Identification of Studies
relatives of patients with SAH.4 Also, the management strategy To identify studies published between 1955 and June 1996 on
prevalence and natural history of intracranial saccular aneurysms, we
for unruptured aneurysms is influenced by the prevalence;
first performed a MEDLINE search from 1966 onward. Second, we
because the incidence of SAH has been properly assessed and searched the reference lists of all relevant publications for additional
is stable,5 a higher than previously assumed prevalence of studies. The references of the publications thus found were checked

Received July 21, 1997; final revision received October 23, 1997; accepted October 24, 1997.
From the University Department of Neurology Utrecht, The Netherlands.
Correspondence to Gabriel J.E. Rinkel, MD, University Department of Neurology, Heidelberglaan 100, 3584 CX Utrecht, Netherlands.
E-mail g.j.e.rinkel@neuro.azu.nl
© 1998 American Heart Association, Inc.

251
252 Intracranial Aneurysms: Prevalence and Risk of Rupture

Results
Selected Abbreviations and Acronyms For the overview of prevalence of aneurysms, we found 8
ACA 5 anterior communicating artery autopsy and 15 angiography studies that fulfilled all the
ADPKD 5 autosomal dominant polycystic kidney disease
inclusion criteria (Fig 1).1,2,7–27 One of these 23 publications was
ICA 5 internal carotid artery
MCA 5 middle cerebral artery
in French,13 another in Japanese,25 and the remaining 21 were
SAH 5 subarachnoid hemorrhage in English. The number of patients studied in these 23 series
totalled 56 304; 49 619 of these patients (88%) were from
autopsy studies, and 6685 patients (12%) were from angiogra-
again for additional studies published between 1955 and June of 1996. phy studies. In 738 patients, one or more aneurysms were
This method of cross-checking was continued until no further found; 405 of these patients (55%) were from autopsy studies.
publications were found. In case of multiple publications on the same Data on whether more than one aneurysm was found in single
study population, we used the most recent publication. Language
other than English was not an exclusion criterion.6
patients could be extracted from two autopsy studies13,18 and
from all angiography studies; the number of extra aneurysms
Eligibility Studies was 23 in the autopsy studies and 69 in the angiography studies.
To assess eligibility, two authors independently reviewed all studies The total number of aneurysms found was 830.
with a set of predefined inclusion criteria. A first inclusion criterion for The prevalence in the retrospective autopsy studies was
all studies was that the presentation of data included crude numbers or much lower than in prospective autopsy studies or in angiog-
allowed recalculation into crude numbers. In autopsy studies, addi-
raphy studies (retrospective or prospective) (Fig 1). The
tional inclusion criteria were that ruptured saccular aneurysms and also
fusiform and mycotic aneurysms had to be excluded or separately prevalence in these last three types of studies combined was 4.3
reported. In angiography studies on prevalence, additional criteria (95% confidence interval, 4.0 to 4.7) per 100. The prevalence
were (1) angiography had to be intra-arterial, (2) the indication for of aneurysms was very low in the first two decades of life and
angiography had to be given, and (3) the number of patients had to be steadily increased after the third decade; this increase was
more than 10. In studies that used CT angiography or MR angiog- statistically significant in a weighted linear regression (Fig 2).
raphy, the presence of aneurysms had to be confirmed by conventional
angiography. The inclusion criteria for follow-up studies about the Autopsy studies did not allow relating the frequency of
risk of bleeding in patients with unruptured aneurysms were (1) the aneurysms to sex, comorbidity, or cause of death. In angiog-
type of aneurysm had to be identifiable as one of three categories: raphy studies, more men (n51754) than women (n51254)
incidental (found by chance), additional (multiple aneurysms in were studied; the prevalence was lower in men (Table 1). If
patients with SAH), or symptomatic but unruptured; (2) in patients subdivided according to the indication for angiography, pa-
with additional aneurysms, the ruptured (“index”) aneurysm had to
have been clipped (wrapping was considered inadequate to prevent tients with ADPKD and patients with a positive family history
Downloaded from http://ahajournals.org by on December 27, 2022

further ruptures); and (3) in patients with previously clipped aneu- had the highest risk for aneurysms, but patients with a
rysms, the source of subsequent bleeding had to be identified by CT, suspected pituitary adenoma (in whom the angiogram was
surgery, or autopsy, to exclude rerupture of the previously clipped often specifically done to exclude an aneurysm as cause of
aneurysm as a cause for the hemorrhage. In some studies, only subsets compression on the optic nerve) and patients with atheroscle-
of patients met all inclusion criteria; only those patients were included
in the review. rosis also had a higher risk than patients with a brain tumor or
other indications for angiography (Table 1).
Data Extraction The site of the aneurysm was recorded for 563 aneurysms,
After the initial assessment for eligibility, two authors independently from all angiography studies and two autopsy studies. ICA
extracted the following data for studies on prevalence: total number of aneurysms were most commonly found, and posterior circu-
patients; number of patients with aneurysms; age and sex of all patients lation aneurysms least commonly (Table 2). The size of the
and of patients with aneurysms; and site and size of the aneurysms
found. The indications for angiography were categorized into the
aneurysm could be studied for categories of 5 mm in 356
following groups: family history of SAH, ADPKD, atherosclerosis aneurysms, from 10 angiography and 2 autopsy studies (Table
(carotid artery disease or ischemic heart disease), suspected pituitary 2). The proportions within these categories were similar in the
adenoma, brain tumor, and other. The ages of the patients were autopsy and angiography studies. One study used categories of
grouped into decades; the sites of the aneurysms were grouped into 10 mm18; when the 83 aneurysms #10 mm and the 10
one of four locations: (1) ICA, (2) ACA or anterior cerebral and
aneurysms .10 mm from this study were added, the propor-
pericallosal artery, (3) MCA, and (4) vertebrobasilar arteries. The sizes
of the aneurysms were categorized into categories of 5-mm increases, tion of aneurysms 10 mm remained essentially the same (8%;
and the size was also dichotomized into 10 mm or larger. For 95% confidence interval, 5% to 11%).
follow-up studies in patients with unruptured aneurysms, we recorded For the analysis of the risk of SAH in patients with
the total number of patients, the period of follow-up, and the number unruptured aneurysms, nine studies, totalling 3907 patient-
of patients with SAH. When possible, we stratified data according to
years, fulfilled the inclusion criteria (Table 3).28 –36
age and sex of the patients and to site and size of the aneurysms.
The risk of rupture of aneurysms depended more on the
Data Analysis characteristics of the aneurysm than on those of the patient.
For calculating the risk of SAH in patients with unruptured aneu- Women and patients at higher age tended to have an increased
rysms, we multiplied the number of patients by the average period of risk of rupture, but the 95% confidence intervals were wide.
follow-up to obtain the total number of patient-years of follow-up. Symptomatic aneurysms, posterior circulation aneurysms, and
The number of patients with subsequent SAH was then divided by this large (.10 mm) aneurysms had a higher risk of rupture.
number of patient-years, yielding the risk of SAH per patient-year.
We used this method for calculating the risk of SAH in all patients as Additional aneurysms also had a higher risk of rupture than
well as in the prespecified subgroups (according to age group and sex accidentally found asymptomatic aneurysms, but this difference
or to type, site, and size of aneurysms). was not statistically significant. Data provided in the publica-
Rinkel et al 253

Figure 1. Methods, overall prevalence,


and subgroups distinguished for
autopsy studies (retrospective and
prospective) and angiography studies
(retrospective and prospective).
Downloaded from http://ahajournals.org by on December 27, 2022

tions were insufficient for a multivariate analysis to assess prospective autopsy studies or in angiography studies of either
whether these factors are independent prognosticators. design. A probable explanation for this low prevalence in
retrospective autopsy studies is that these review old files,
Discussion rather than original materials, in contrast to retrospective
The frequency of incidental aneurysms varied considerably angiography studies that can review the actual studies. The data
according to the indication for the imaging studies. The derived from the retrospective autopsy studies are therefore
prevalence of 2.3 per 100 in patients with brain tumors or probably an underestimation of the prevalence. The much
miscellaneous indications may most closely represent the higher prevalence found in prospective angiography studies
prevalence in the general population, although this number compared with prospective autopsy studies is probably ex-
probably overestimates the actual rate because the prevalence plained by selection bias because patients with ADPKD, a
in patients younger than 20 years is very low and this age group familial predisposition for SAH, or atherosclerosis are overrep-
is obviously underrepresented in this study sample. The fre- resented in the prospective angiography series. The prospective
quency of aneurysms is higher in patients investigated for angiography series therefore seem to overestimate the
ADPKD or with a familial predisposition for SAH, suspected prevalence.
pituitary adenomas, and atherosclerosis; moreover, it tends to For the risk of rupture, the type of aneurysm is an important
increase with age in adults. factor. Incidentally found aneurysms tend to have a lower risk
The methods used to detect the aneurysms markedly influ- of rupture than aneurysms found additional to a ruptured
enced the proportion of aneurysms. In retrospective autopsy aneurysm. Symptomatic aneurysms, aneurysms larger than
studies, the prevalence was much lower (0.4%) than in 10 mm, and basilar artery aneurysms were all found to have a
254 Intracranial Aneurysms: Prevalence and Risk of Rupture

TABLE 1. Risk Factors for Presence of Intracranial Aneurysms in Angiography Studies


No. No. of Prevalence per Relative Risk
Investigated Aneurysms 100 (95% CI) (95% CI)
Sex
Men 1754 61 3.5 (2.7-4.5) 0.8 (0.5-1.1)
Women 1254 58 4.6 (3.5-5.9) Ref
Indications
Family history 476 45 9.5 (7.0-12) 4.0 (2.7-6.0)
ADPKD 202 21 10 (6.2-15) 4.4 (2.7-7.3)
Atherosclerosis 3676 196 5.3 (4.6-6.1) 2.3 (1.7-3.1)
Pituitary adenoma 183 11 6.0 (3.0-11) 2.6 (1.4-4.9)
Brain tumor1other 2052 48 2.3 (1.7-3.1) Ref
Ref indicates reference category; CI, confidence interval. Data on sex are derived from nine studies, 2,11,14,16,17,19,21,23,24

on family history from three studies,23,26,27 on ADPKD from three studies,16,20,24 on atherosclerosis from five
studies,2,19,21,22,25 on pituitary adenoma from two studies,14,15 and on other (including brain tumor) conditions from five
studies.11,17,21,23,25

markedly increased risk of rupture. Because symptomatic .10 mm. If the annual risk of rupture in this cohort (0.7% for
aneurysms are often large, size and being symptomatic may not aneurysms ,10 mm and 4% for those of $10 mm) is corrected
be independent risk factors, but unfortunately the data pro- on the assumption that in the general population almost all
vided in the publications did not allow us to assess the ruptured aneurysms are previously asymptomatic and not
interdependence of these factors. additional to a ruptured aneurysm (0.8/1.950.4) in a single
Despite all these sources of bias, the data seem reasonably year, 0.4p0.7% of the 1605 small aneurysms (n54.6) and
accurate. A hypothetical calculation of the incidence from the 0.4p4% of the 120 large aneurysms (n51.9) will rupture; the
data on prevalence and risk of rupture should approximate the total number of SAHs within the cohort of 100 000 subjects
incidence of SAH observed in the population (6 per 100 000 will therefore be 6.5. This calculated incidence is similar to the
patient-years).5 If one assumes a cohort of 100 000, only the incidence of 6 per 100 000 patient-years observed in the
Downloaded from http://ahajournals.org by on December 27, 2022

proportion (75%) of individuals older than 20 years is at risk for population.


aneurysms.37 Most of these 75 000 individuals will not have Other factors also corroborate the accuracy of the data in
risk factors for the presence of aneurysms and will therefore this review. First, women more often had aneurysms than men
have a prevalence comparable to the subset of patients with and their aneurysms had a greater risk of rupture, which
“brain tumor and other indications for angiography” (2.3%). In explains the higher incidence of SAH in women.5 Second,
these 75 000 individuals, 1725 will have an aneurysm. Because patients with ADPKD and patients with a familial predisposi-
93% of aneurysms are #10 mm, 1605 subjects in the cohort tion for SAH had an increased risk of aneurysms. This finding
will have an aneurysm #10 mm, and 120 subjects an aneurysm is in keeping with the increased risk of SAH for first-degree
relatives of patients with SAH4 and suggests that at least part of
the increased risk for SAH is explained by a higher frequency

TABLE 2. Sites and Sizes of Aneurysms*


n % (95% CI)
Size of aneurysm, total number
with data on size 356
,6 257 72 (68-77)
6-10 74 21 (17-25)
11-20 23 6.5 (4.1-9.5)
.20 2 0.8 (0.09-2.8)
Site of aneurysm, total number with
data on site 563
ACA 126 24 (20-27)
MCA 159 30 (26-34)
ICA 223 42 (37-46)
PC 55 10 (7.7-13)
PC indicates posterior circulation.
*Sites of aneurysms found in 2 autopsy studies13,18 and 15 angiography
Figure 2. Prevalence of aneurysms per age group from five studies2,11,14-17,19-27 and sizes of aneurysms in 2 autopsy studies12,18 and 10
autopsy studies1,8,9,12,18 and five angiography studies.2,11,17,21,23 angiography studies.2,14,17,19-21,23-25,27
Rinkel et al 255

TABLE 3. Risk of Rupture of Aneurysms28-36


Risk of Rupture per
Patient-Years No. of 100 Patient-Years Relative Risk
Investigated Ruptures (95% CI) (95% CI)
Overall 3907 75 1.9 (1.5-2.4)
Sex
Male 1027 13 1.3 (0.7-2.1) Ref
Female 1304 34 2.6 (1.8-3.6) 2.1 (1.1-3.9)
Age, y
,20 No data
20-39 26 0 0 (0-13) NA
40-59 203 7 3.5 (1.4-7.0) Ref
60-79 297 17 5.7 (3.4-9.0) 1.7 (0.7-4.0)
.80 No data
Type of aneurysm
Asymptomatic 1145 9 0.8 (0.4-1.5) Ref
Additional 1997 27 1.4 (0.9-2.0) 1.7 (0.8-3.7)
Symptomatic 463 30 6.5 (4.4-9.1) 8.2 (3.9-17)
Site
ACA 464 5 1.1 (0.4-2.5) Ref
MCA 1519 17 1.1 (0.7-1.8) 1.0 (0.4-2.8)
ICA 2449 30 1.2 (0.8-1.7) 1.1 (0.4-2.9)
PC 434 19 4.4 (2.7-6.8) 4.1 (1.5-11)
Size, mm
#10 3742 27 0.7 (0.5-1.0) Ref
.10 675 27 4.0 (2.7-5.8) 5.5 (3.3-9.5)
Downloaded from http://ahajournals.org by on December 27, 2022

Ref indicates category; CI, confidence interval; PC, posterior circulation; and NA, not available.

of aneurysms and not only, or not at all, by a higher risk of Acknowledgments


rupture. Third, patients with atherosclerosis also had an in- This study was partially funded by a clinical investigator grant from the
creased frequency of aneurysms, which corresponds with the University Hospital Utrecht to G.J.E. Rinkel and a NUFFIC grant to
finding that cardiovascular diseases and SAH share the risk M. Djibuti (CN.1942). We would like to thank Fleur Bominaar for
accurate help in preparing the tables and figures and Stef Koele for
factors smoking, hypertension, and alcohol abuse.38 Fourth, the excellent secretarial assistance.
relative risk of ADPKD and familial predisposition was higher
than that of atherosclerosis, which confirms previous findings
that hypertension contributes less to the familial predisposition References
1. McCormick WF, Nafzinger JD. Saccular intracranial aneurysms: an
for SAH than other, probably genetic, factors.39 autopsy study. J Neurosurg. 1965;22:155–159.
In conclusion, data on prevalence vary considerably accord- 2. Griffiths PD, Worthy S, Gholkar A. Incidental intracranial vascular
ing to methods used to detect aneurysms. Retrospective pathology in patients investigated for carotid stenosis. Neuroradiology. 1996;
autopsy studies probably give an underestimation and prospec- 38:25–30.
3. Schievink WI, Torres VE, Piepgras DG, Wiebers DO. Saccular intracranial
tive angiography studies an overestimation of the actual prev- aneurysms in autosomal dominant polycystic kidney disease. J Am Soc
alence. If all available evidence is taken together, for adults Nephrol. 1992;3:88 –95.
without risk factors for SAH, aneurysms can be found in 4. Bromberg JEC, Rinkel GJE, Algra A, Greebe P, van Duyn CM, Hasan D,
ten Berg HWM, Wijdicks EFM, van Gijn J. Subarachnoid haemorrhage in
approximately 2%; it is possible that the prevalence increases
first and second degree relatives of patients with subarachnoid haemor-
with age, but we could not convincingly demonstrate this. The rhage. BMJ. 1995;311:288 –289.
large majority of these aneurysms are small (,10 mm), and the 5. Linn FHH, Rinkel GJE, Algra A, van Gijn J. Incidence of subarachnoid
annual risk of rupture of these small aneurysms is low (0.7% per hemorrhage: role of region, year and rate of computed tomography: a
meta-analysis. Stroke. 1996;27:625– 629.
year). These data should be kept in mind when one is
6. Moher D, Fortin P, Jadad AR, Jüni P, Klassen T, Le Lorier J, Liberati A,
confronted with the task of advising patients with an acciden- Linde K, Penna A. Completeness of reporting of trials published in lan-
tally found asymptomatic aneurysm. In patients with athero- guages other than English: implications for conduct and reporting of
sclerosis and especially in patients with familial predisposition systematic reviews. Lancet. 1996;347:363–366.
7. Cohen MM. Cerebrovascular accidents: a study of two hundred one cases.
or ADPKD, aneurysms are found more often. Prospective Arch Pathol. 1955;60:296 –307.
studies should evaluate whether screening and treating these 8. Chason JL, Hindman WM. Berry aneurysms of the circle of Willis: results
patients with an increased risk is beneficial. of a planned autopsy study. Neurology. 1958;8:41– 44.
256 Intracranial Aneurysms: Prevalence and Risk of Rupture

9. Housepian EM, Pool JL. A systematic analysis of intracranial aneurysms in polycystic kidney disease: screening with MR Angiography. Radiology.
from the autopsy file of the Presbyterian hospital 1914 to 1956. J Neuro- 1994;191:33–39.
pathol Exp Neurol. 1958;17:409 – 423. 25. Sugai Y, Hamamoto Y, Ookubo T, So K. Angiographical frequency of
10. Stehbens WE. Aneurysms and anatomical variation of cerebral arteries. Arch unruptured incidental intracranial aneurysms. No Shinkei Geka. 1994;22:
Pathol. 1963;75:45–76. 429 – 432.
11. du Boulay GH. Some observations on the natural history of intracranial 26. Leblanc R, Melanson D, Tampieri D, Guttmann RD. Familial cerebral
aneurysms. Br J Radiol. 1965;38:721–757. aneurysms: a study of 13 families. Neurosurgery. 1995;37:633– 639.
12. McCormick WF, Acosta-Rua GJ. The size of intracranial aneurysms: an 27. Ronkainen A, Puranen MI, Hernesniemi JA, Vanninen RL, Partanen PL,
autopsy study. J Neurosurg. 1970;33:422– 427. Saari JT, Vainio PA, Ryynanen M. Intracranial aneurysms: MR angio-
13. Romy M, Werner A, Wildi E. De la fréquence des anéurisme artériels graphic screening in 400 asymptomatic individuals with increased familial
intra-craniens et de leur rupture, d’après une série d’autopsies de routine. risk. Radiology. 1995;195:35– 40.
Neurochirurgie. 1973;19:611– 626. 28. Locksley HB. Natural history of subarachnoid hemorrhage, intracranial
14. Jakubowski J, Kendall B. Coincidental aneurysms with tumours of pituitary aneurysms and arteriovenous malformations. J Neurosurg. 1966;25:321–368.
origin. J Neurol Neurosurg Psychiatry. 1978;41:972–979. 29. Zacks DJ, Russell DB, Miller JDR. Fortuitously discovered intracranial
15. Wakai S, Fukushima T, Furihata T, Sano K. Association of cerebral aneurysms. Arch Neurol. 1980;37:39 – 41.
aneurysm with pituitary adenoma. Surg Neurol. 1979;12:503–507. 30. Przelomski MM, Fisher M, Davidson RI, Jones HR, Marcus EM.
16. Wakabayashi T, Fujita S, Ohbora Y, Suyama T, Tamaki N, Matsumoto S. Unruptured intracranial aneurysm and transient focal cerebral ischemia: a
Polycystic kidney disease and intracranial aneurysms: early angiographic follow-up study. Neurology. 1986;36:584 –587.
diagnosis and early operation for the unruptured aneurysm. J Neurosurg. 31. Eskesen V, Rosenorn J, Schmidt K, Espersen JO, Haase J, Harmsen A,
1983;58:488 – 491. Hein O, Knudsen V, Marcussen E, Midholm S, et al. Clinical features and
17. Atkinson JLD, Sundt TM, Houser OW, Whisnant JP. Angiographic fre- outcome in 48 patients with unruptured intracranial saccular aneurysms: a
quency of anterior circulation intracranial aneurysms. J Neurosurg. 1989;70: prospective consecutive study. Br J Neurosurg. 1987;1:47–52.
551–555. 32. Wiebers DO, Whisnant JP, Sundt TM, O’Fallon WM. The significance of
18. Inagawa T, Hirano A. Autopsy study of unruptured incidental intracranial unruptured intracranial saccular aneurysms. J Neurosurg. 1987;66:23–29.
aneurysms. Surg Neurol. 1990;34:361–365. 33. Inagawa T, Hada H, Katoh Y. Unruptured intracranial aneurysms in
19. Iwata K, Misu N, Terada K, Kawai S, Momose M, Nakagawa H. elderly patients. Surg Neurol. 1992;38:364 –370.
Screening for unruptured asymptomatic intracranial aneurysms in patients 34. Juvela S, Porras M, Heiskanen O. Natural history of unruptured intra-
undergoing coronary angiography. J Neurosurg. 1991;75:52–55. cranial aneurysms: a long-term follow-up study. J Neurosurg. 1993;79:
20. Chapman AB, Rubinstein D, Hughes R, Stears JC, Earnest MP, Johnson 174 –182.
AM, Gabow PA, Kaehny WD. Intracranial aneurysms in autosomal 35. Asari S, Ohmoto T. Natural history and risk factors of unruptured cerebral
dominant polycystic kidney disease. N Engl J Med. 1992;327:916 –920. aneurysms. Clin Neurol Neurosurg. 1993;95:205–214.
21. Ujiie H, Sato K, Onda H, Oikawa A, Kagawa M, Takakura K, Kobayashi 36. Mizoi K, Yoshimoto T, Nagamine Y, Kayama T, Koshu K. How to treat
N. Clinical analysis of incidentally discovered unruptured aneurysms. incidental cerebral aneurysms: a review of 139 consecutive cases. Surg
Stroke. 1993;24:1850 –1856. Neurol. 1995;44:114 –120.
22. Nagashima M, Nemoto M, Hadeishi H, Suzuki A, Yasui N. Unruptured 37. Statistical Yearbook of the Netherlands 1996. The Hague, Netherlands: Sdu/
aneurysms associated with ischaemic cerebrovascular diseases: surgical indi- publishers; 1996:39.
cation. Acta Neurochir (Wien). 1993;124:71–78. 38. Teunissen LL, Rinkel GJE, Algra A, van Gijn J. Risk factors for subarach-
Downloaded from http://ahajournals.org by on December 27, 2022

23. Nakagawa T, Hashi K. The incidence and treatment of asymptomatic noid hemorrhage: a systematic review. Stroke. 1996;27:544 –549.
unruptured intracranial aneurysms. J Neurosurg. 1994;80:217–223. 39. Bromberg JEC, Rinkel GJE, Algra A, van den Berg UAC, Tjin-A-Ton
24. Ruggieri PM, Poulos N, Masaryk TJ, Ross JS, Obuchowski NA, Awad IA, MLR, van Gijn J. Hypertension, stroke and coronary heart disease in
Braun WE, Nally J, Lewin JS, Modic MT. Occult intracranial aneurysms relatives of patients with subarachnoid hemorrhage. Stroke. 1996;27:7–9.

You might also like