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Cost-effectiveness of magnetic resonance angiography for mass screening for intracranial aneurysms
Cost-Effectiveness of Magnetic Resonance Angiography for Mass Screening for Intracranial AneurySms Mutsumasa Takahashi, MD
n spite of niodern advances in management, the morbidity and mortality
I of subamclinoid hemorrhage due to the rupture of cerebral aneurysms
are high [1, 2]. Surgical treatment of unruptured intracranial aneurysms, on the other hand, has a relatively low risk of serious complications and death [1, 3, 4]. In Japan, the screening of asymptomatic persons--or mass screening--has therefore been advocated to detect asymptomatic unruptured cerebral aneurysms before major hemorrhage occurs [5, 6]. Various radiologic techniques have been advocated for such screening, including magnetic resonance (MR) angiography, computed "tomography angiography, and conventional angiography [5, 6], and trials of the feasibility of using MR angiography for this purpose are under way in a number of hospitals and clinics in Japan. The purpose of this study is to evaluate the feasibil!ty of mass screening for cerebral aneurysms with MR angiography. SCOPE OF THE PROBLEM Prevalence and Incidence of Unruptured Cerebral Aneurysms and Their Rupture
The prevalence or incidence of subarachnoid hemorrhage has been reported from epidemiology studies to be 10-20 per 100,000 population [2, 7]. The prevalence of unruptured cerebral aneurysms has been reported from autopsy and cerebral angiography to be 2-5% [8, 9]. Incidence rises with advancing age and is lower when a large number of young persons are included in the subject group. An incidence rate of 2%, however, is an acceptable figure for the general population. Among the various possible predisposing factors for rupture of a cerebral aneurysm, the size of the aneurysm has been reported to be the most important [1]. Aneurysms larger than 10 mm tend to rupture more frequently than smaller aneurysms do [10], and some reports indicate that aneurysms 5 mm or less rarely rupture [1]. The reported rupture rate of cerebral aneurysms varies considerably [11-13]. In patients with multiple aneurysms in whom one aneurysm is clipped and the other is left untouched, the incidence of rupture of the
$40
From the Department of Radiology, Kumamoto University School of Medicine, Kumamoto, Japan.
Address reprint requests to M. Takahashi, MD, Department of Radiology, Kumamoto University School of Medicine, 1-1-1 Honio, Kumamoto 860, Japan. Acad Radiol 1996;3:$40-$43
9 1996, Association of University Radiologists
Vol. 3, Suppl. 1, April 1996
untouched aneurysms is 1-2% annually [11-13]. Approximately 2% is an acceptable figure for rupture rate per year, a statistic that corresponds roughly to the number of subarachnoid hemorrhages in the general population.
MATERIALS AND METHODS Diagnostic Accuracy of MR Angiography The most important factor in evaluating the feasibility of mass screening for cerebral aneurysms with MR angiography is the accuracy of MR angiogmphy for detecting cerebral aneurysms. A special committee of the Japanese Society of Magnetic Resonance in bledicine conducted two retrospective studies (using 131 patients and 203 patients, respectively) analyzing the diagnostic a c c u r a c y of blR angiography for mass screening for Ferebral aneurysms [14-16]. Fimt evahte~tion. The first study included 131 patients who underwent blR angiography within 1 month of conventional iangiogmphy for evaluation of possible vascular disease [14, 15]. The scans were interpreted by five experienced observers. The study included 61 patients with:78 aneurysms and a control group that consisted of 70 patients, some with no disease, some with stenoocclusive disease, and some with. arteriovenous malformations and dural arteriovenous fistulas. Three-dimensional Fourier transform time-of-flight MR angiograms were obtained on three 1.5-T superconductive MR units (two Signa systems [General Electric Medical Systems, Milwaukee, WI] and one Magnetom system [Siemens Medical Systems, Iselin, NJ]). The results of conventional angiography, done within 1 month of the MR angiography studies and using a femoral catheter technique, were considered the standard for diagnosis. Of the 61 patients with aneurysms, 13 had multiple aneurysms, including two aneurysms in 10 cases, three aneurysms in two cases, and four aneurysms in one case. In the overall detection of these 78 aneurysms, the sensitivity of MR angiography ranged from 58% to 68~ (M = 63%). When the criterion for a positive study was the detection of at least one aneurysm, the sensitivity increased to 66-81% 61/= 74o/0) and specificity was 68--89o/0(3/= 76%). Seco,ld evahtation. The second study was performed in a similar manner, with 203 cases obtained from two hospitals using two 1.5-T (hospital A; Signa) and 1.0-T (hospital B; Magnetom) superconductive units [16]. One hundred three cases were from hospital A (group A), including 19 n o r m a l cases, 58 cases of aneurysms, 28 cases of stenoocclusive disease, and two cases of miscel-
SCREENING FOR INTRACRANIAL ANEURYSMS
laneous conditions. One hundred cases were from hospital B (group B), including 34 normal cases, 38 cases of aneurysms, 27 cases of stenoocclusive disease, and two cases of miscellaneous conditions. Twice within an interval of 1 month, five experienced observers interpreted the blR angiograms on five scales of confidence levels. The first interpretation was performed on the basis of maximum intensity projection (MIP) images without source images, and the secon d interpretatio n was done 2 weeks later using MIP and source images. For group A, with specificity set at 80%, sensitivity for the detection of one aneurysm ranged from 63% to 82% on bliP images. With bliP and source images, sensitivity improved to 6487%. Improvement from the first to the second interpretation was minimal, but the observers had more confidence in their interpretation of aneurysms when the source images were used. For all 68 individual aneurysms, the sensitivity was 41-77% for MIP images a l o n e and 57-79~ for bliP and source images. For group B, with specificity set at 80%, sensitivity was 58-89% on bliP images and improved to 65-91% with MIP and source images. For the detection of 45 individual aneurysms, the sensitivity was 56--82% with bliP images and 62-82% with MIP and source images. In this instance, sensitivity did not improve significantly with use of source images.
Complications of Conventional Angiography Numerous reports of complications associated with cerebral angiogmphy have been published. These can be divided into general, local, and neurologic complications. The incidence of permanent neurologic deficits has been reported to be 0.2-5.7% [17-21]. According to a report by Waugh and Sacharias [17], who used digital subtraction angiography and nonionic contrast medium, the incidence of permanent neurologic complications was 0.3%, and the incidence of fatal complications was 0.1% or less. Other published reports put the incidence of fatal complications at 04).16% [17, 18]. With data obtained from a group of patients with various neurologic disorders, including cerebrovascular disease, cerebral tumors, and other vascular diseases, 0.1% or less appears to be a reasonably accurate figure for fatal complications associated with cerebral angiography.
Surgery of Unruptured Aneurysms Unruptured aneurysms can be treated surgically with a low complication rate [1, 3, 4]. Fatal complications are
$41
TAKAHASHI
rare, and the average figure for permanent neurologic
complications is only 0.3% [1]. With recent advances in the treatment of unrupmred cerebral aneurysms, associated morbidity and mortality are minimal. DISCUSSION
Using prevalence figures for cerebral aneurysms and annual incidence of rupture, we can calculate the number of.patients who should undergo screening MR angiograplay, cerebral angi0graphy, and. surgery in order to save one patient with prospective sul)arachnoid hemorrhage. If one uses a 2% figure for both prevalence of cerebral aneurysm and annual aneurysmal rupture rate (acceptable figures derived from published data), mass screening with MR angiography for cerebritl aneurysms should be done on 2,500 patients, among whom 500 patients Should undergo conventional cerebral angiography because the r specificity of MR angiography is 80%. Fifty patients (2% of the 2,500 patients screened) will have cerebral aneurysms and will require surgery to save one patient with i an aneurysm before prospective subarachnoid hemorrlmge. If t!m prevalence and rupture rates are changed to 5% and 1%, respectively, then 2,000 patients would need to undergo MR angiogmphic screening and 400 would need conventional angiogmphy. Under these conditions, 100 patients with cerebral aneurysms would need surgery in order to save one patient with an aneurysm before prospective subarachnoid henlorrhage. In a third scenario, with a prevalence rate of 5% and a rupture rate of 2%1 1,000 patients would need to undergo MR angiographic screening and 200 patients wot, ld need conventional cerebral angiography. Fifty patients with cerebral: aneurysms would need surgery to save one patient with an aneurysm before its rupture. As these numbers indicate, mass screening for cerebral aneurysms with MR angiography is not cost-effective at present. One problem is that the diagnostic accuracy of MR angiograplay for cerebral aneurysms is approximately 80% with 80% specificity and 80% sensitivity. Therefore, 20% of the patients undergoing screening for aneurysms with MR angiogmphy would need to be further studied with conventional angiograplay. Unfortunately, conventional angiogmphy carries a 0.3% risk of neurologic complications as well as a fatality risk of less than 0.1%. In addition, the combination of the high cost of MR units and the relatively slow throughput drives up the medical costs for MR studies. Another problem with MR angiographic screening for
$42
Vol. 3, Suppl. 1, April 1996
cerebral aneurysms is that tile natural history of the disorder has not been clarified. Because the rupture rate t of cerebral aneurysms is relatively low, in the range of 1-2%, the majority of aneurysms never rt, pture during the patient's lifetime. Some authorities believe that aneurysmal ruptures occur only when aneuwsms arise and enlarge very rapidly. Overall, it appears that at present the costs of MR studies, conventional angiography, and surgew, in addition to the expenses incurred by a relatively large medical staff, make screening with MR angiography infeasible. Randomized controlled trials should be undertaken, however, to establish the true cost-effectiveness of such a progmnl. Of course, patients should be informed of the details of mass screening, including the natural history of cerebral aneurysms, the diagnostic accuracy of MP, angiography, and complications associated with cerebral angiography and surgery. Even though mass screening may not be practical, screening in certain high-risk groups may be more practical. For instance, the incidence of cerebral aneurysm is considerab!y higher in asymptoinatic persons who have a family member who has a subamchnoid hemorrhage. Screening may be justified to detect unruptured aneurySlllS before a major catastrophic event occurs in such individuals. In addition, patients with polycystic kidney disease, fibromuscular dysplasia, and severe atherosclerotic disease of other vessels may be candidates for screening of cerebral aneurysms with MR angiogmphy [22], Technological advances may also make screening more attractive. Once the diagnostic accuracy of MR angiography is improved, and conventional angiograplay is not required for surgery, screening programs may be inore likely to be accepted. REFERENCES 1. Kassell NF, Torner JC. Size of intracranial aneurysms. Neurosurgery
1983;12:291-297. 2. Bonita R, Thomson S. Subarachnoid hemorrhage: epidemiology, diagnosis, management, and outcome. Stroke1985;16:591-594. 3. Wirth FP, Laws ER Jr, Piepgras D, Scott RM. Surgical treatment of incidental intracranial aneurysms. Neurosurgery1983;12:507-511. 4. Heiskanen O. Risks of surgery for unruptured intracranial aneurysms. J Neurosurg1986;65:451-453. 5. Nakagawa "1",Hashi K. The incidence and treatment of asymptomatic, unruptured cerebral aneurysms. J Neurosurg1994;80:217-223. 6. Schievink Wl, Limburg M, Dreissen JJR, Peeters FLM, ter Berg HWM. Screening for unruptured familial intracranial aneurysms: subarachnoid hemorrhage 2 years after angiography negative for aneurysms. Neurosurgery 1991;29:434-438. 7. Phillips LH, Whisnant JP, O'Fallon WM, Sundt TM Jr. The unchanging pattern of subarachnoid hemorrhage in a community. Neurology 1980; 30:1034-1040.
Vol. 3, Suppl. 1, April 1996
8. Wiebers DO, Tomer JC, Meissner I. Impact of unruptured intracranial aneurysms on public health in the United States. Stroke 1992;23:14161419. 9. Sekhar LN, Heros RC. Origin, growth, and rupture of saccular aneurysms: a review. Neurosurgery1981 ;8:248-260. 10. Wiebers DO, Whisnant JP, Sundt TM Jr, O'FaTlonWM. The significance of unruptured intracranial saccular aneurysms. J Neurosurg 1987;66:23-29. 11. Winn HR, Almaani WS, Berga SL, Jane JA, Richardson AE. The longterm outcome in patients with multiple aneurysms. J Neurosurg 1983; 59:642-651. 12. Heiskanen O. Risk of bleeding from unruptured aneurysms in cases with multiple intracranial aneurysms. J Neurosurg 1981;55:524-526. 13. Jane JA, Kassell NF, Tomer JC, Winn HR. The natural history of aneurysms and artedovenous malformations. J Neurosurg 1985;62:321-323. 14. Korogi Y, Takahashi M, Mabuchi N, et aL Intracranial aneurysms: diagnostic accuracy of three-dimensional, Fourier transform, time-of-flight MR angiography. Radiology1994;193:181-186. 15. Korogi Y, Takahashi M, Mabuchi N, et al. Intracranial vascular stenosis and occlusion: diagnostic accuracy of three-dimensional, Fourier trans-
SCREENING FOR INTRACRANIAL ANEURYSMS
form, time-of-flight MR angiography. Radiology 1994;193:187-193. 16. Korogi Y, Takahashi M, O'Uchi T, et al. Diagnostic accuracy of 3DFT timeof-flight MR angiography for intracranial aneurysms and steno-occlusive diseases: report on 1994 study (Fourth Report,of Special Committee). Jpn J Magn Reson Med 1994;14:415-421. 17. Waugh JR, Sacharias N. Arteriographic complications in the DSA era. Radiology 1992; 182:243-246. 18. Dion JE, Gates PC, Fox AJ, Barnett HJM, Blom RJ. Clinical events following neuroangiography: a prospective study. Stroke 1987;18:997-1004. 19. Hankey GJ, Wadow CP, Senar RJ. Cerebral angiographic risk in mild cerebrovascular disease. Stroke 1990;21:209-222. 20. Olivecrona H. Complications of cerebral angiography. Neuroradiology 1977;14:175-181. 21. Mclvor J, Steiner TJ, Perkin GD, Greenhalgh RM, Rose FC. Neurological morbidity of arch and carotid artedography in cerebrovasculardisease: the influence of contrast medium and radiologist.Br J Radio11987;60:117-122. 22. Ruggied PM, Poulos N, Masaryk TJ, et al. Occult intracranial aneurysms in polycystic kidney disease: screening with MR angiography. Radiology 1994;191:33-39.
$43
n spite of niodern advances in management, the morbidity and mortality
I of subamclinoid hemorrhage due to the rupture of cerebral aneurysms
are high [1, 2]. Surgical treatment of unruptured intracranial aneurysms, on the other hand, has a relatively low risk of serious complications and death [1, 3, 4]. In Japan, the screening of asymptomatic persons--or mass screening--has therefore been advocated to detect asymptomatic unruptured cerebral aneurysms before major hemorrhage occurs [5, 6]. Various radiologic techniques have been advocated for such screening, including magnetic resonance (MR) angiography, computed "tomography angiography, and conventional angiography [5, 6], and trials of the feasibility of using MR angiography for this purpose are under way in a number of hospitals and clinics in Japan. The purpose of this study is to evaluate the feasibil!ty of mass screening for cerebral aneurysms with MR angiography. SCOPE OF THE PROBLEM Prevalence and Incidence of Unruptured Cerebral Aneurysms and Their Rupture
The prevalence or incidence of subarachnoid hemorrhage has been reported from epidemiology studies to be 10-20 per 100,000 population [2, 7]. The prevalence of unruptured cerebral aneurysms has been reported from autopsy and cerebral angiography to be 2-5% [8, 9]. Incidence rises with advancing age and is lower when a large number of young persons are included in the subject group. An incidence rate of 2%, however, is an acceptable figure for the general population. Among the various possible predisposing factors for rupture of a cerebral aneurysm, the size of the aneurysm has been reported to be the most important [1]. Aneurysms larger than 10 mm tend to rupture more frequently than smaller aneurysms do [10], and some reports indicate that aneurysms 5 mm or less rarely rupture [1]. The reported rupture rate of cerebral aneurysms varies considerably [11-13]. In patients with multiple aneurysms in whom one aneurysm is clipped and the other is left untouched, the incidence of rupture of the
$40
From the Department of Radiology, Kumamoto University School of Medicine, Kumamoto, Japan.
Address reprint requests to M. Takahashi, MD, Department of Radiology, Kumamoto University School of Medicine, 1-1-1 Honio, Kumamoto 860, Japan. Acad Radiol 1996;3:$40-$43
9 1996, Association of University Radiologists
Vol. 3, Suppl. 1, April 1996
untouched aneurysms is 1-2% annually [11-13]. Approximately 2% is an acceptable figure for rupture rate per year, a statistic that corresponds roughly to the number of subarachnoid hemorrhages in the general population.
MATERIALS AND METHODS Diagnostic Accuracy of MR Angiography The most important factor in evaluating the feasibility of mass screening for cerebral aneurysms with MR angiography is the accuracy of MR angiogmphy for detecting cerebral aneurysms. A special committee of the Japanese Society of Magnetic Resonance in bledicine conducted two retrospective studies (using 131 patients and 203 patients, respectively) analyzing the diagnostic a c c u r a c y of blR angiography for mass screening for Ferebral aneurysms [14-16]. Fimt evahte~tion. The first study included 131 patients who underwent blR angiography within 1 month of conventional iangiogmphy for evaluation of possible vascular disease [14, 15]. The scans were interpreted by five experienced observers. The study included 61 patients with:78 aneurysms and a control group that consisted of 70 patients, some with no disease, some with stenoocclusive disease, and some with. arteriovenous malformations and dural arteriovenous fistulas. Three-dimensional Fourier transform time-of-flight MR angiograms were obtained on three 1.5-T superconductive MR units (two Signa systems [General Electric Medical Systems, Milwaukee, WI] and one Magnetom system [Siemens Medical Systems, Iselin, NJ]). The results of conventional angiography, done within 1 month of the MR angiography studies and using a femoral catheter technique, were considered the standard for diagnosis. Of the 61 patients with aneurysms, 13 had multiple aneurysms, including two aneurysms in 10 cases, three aneurysms in two cases, and four aneurysms in one case. In the overall detection of these 78 aneurysms, the sensitivity of MR angiography ranged from 58% to 68~ (M = 63%). When the criterion for a positive study was the detection of at least one aneurysm, the sensitivity increased to 66-81% 61/= 74o/0) and specificity was 68--89o/0(3/= 76%). Seco,ld evahtation. The second study was performed in a similar manner, with 203 cases obtained from two hospitals using two 1.5-T (hospital A; Signa) and 1.0-T (hospital B; Magnetom) superconductive units [16]. One hundred three cases were from hospital A (group A), including 19 n o r m a l cases, 58 cases of aneurysms, 28 cases of stenoocclusive disease, and two cases of miscel-
SCREENING FOR INTRACRANIAL ANEURYSMS
laneous conditions. One hundred cases were from hospital B (group B), including 34 normal cases, 38 cases of aneurysms, 27 cases of stenoocclusive disease, and two cases of miscellaneous conditions. Twice within an interval of 1 month, five experienced observers interpreted the blR angiograms on five scales of confidence levels. The first interpretation was performed on the basis of maximum intensity projection (MIP) images without source images, and the secon d interpretatio n was done 2 weeks later using MIP and source images. For group A, with specificity set at 80%, sensitivity for the detection of one aneurysm ranged from 63% to 82% on bliP images. With bliP and source images, sensitivity improved to 6487%. Improvement from the first to the second interpretation was minimal, but the observers had more confidence in their interpretation of aneurysms when the source images were used. For all 68 individual aneurysms, the sensitivity was 41-77% for MIP images a l o n e and 57-79~ for bliP and source images. For group B, with specificity set at 80%, sensitivity was 58-89% on bliP images and improved to 65-91% with MIP and source images. For the detection of 45 individual aneurysms, the sensitivity was 56--82% with bliP images and 62-82% with MIP and source images. In this instance, sensitivity did not improve significantly with use of source images.
Complications of Conventional Angiography Numerous reports of complications associated with cerebral angiogmphy have been published. These can be divided into general, local, and neurologic complications. The incidence of permanent neurologic deficits has been reported to be 0.2-5.7% [17-21]. According to a report by Waugh and Sacharias [17], who used digital subtraction angiography and nonionic contrast medium, the incidence of permanent neurologic complications was 0.3%, and the incidence of fatal complications was 0.1% or less. Other published reports put the incidence of fatal complications at 04).16% [17, 18]. With data obtained from a group of patients with various neurologic disorders, including cerebrovascular disease, cerebral tumors, and other vascular diseases, 0.1% or less appears to be a reasonably accurate figure for fatal complications associated with cerebral angiography.
Surgery of Unruptured Aneurysms Unruptured aneurysms can be treated surgically with a low complication rate [1, 3, 4]. Fatal complications are
$41
TAKAHASHI
rare, and the average figure for permanent neurologic
complications is only 0.3% [1]. With recent advances in the treatment of unrupmred cerebral aneurysms, associated morbidity and mortality are minimal. DISCUSSION
Using prevalence figures for cerebral aneurysms and annual incidence of rupture, we can calculate the number of.patients who should undergo screening MR angiograplay, cerebral angi0graphy, and. surgery in order to save one patient with prospective sul)arachnoid hemorrhage. If one uses a 2% figure for both prevalence of cerebral aneurysm and annual aneurysmal rupture rate (acceptable figures derived from published data), mass screening with MR angiography for cerebritl aneurysms should be done on 2,500 patients, among whom 500 patients Should undergo conventional cerebral angiography because the r specificity of MR angiography is 80%. Fifty patients (2% of the 2,500 patients screened) will have cerebral aneurysms and will require surgery to save one patient with i an aneurysm before prospective subarachnoid hemorrlmge. If t!m prevalence and rupture rates are changed to 5% and 1%, respectively, then 2,000 patients would need to undergo MR angiogmphic screening and 400 would need conventional angiogmphy. Under these conditions, 100 patients with cerebral aneurysms would need surgery in order to save one patient with an aneurysm before prospective subarachnoid henlorrhage. In a third scenario, with a prevalence rate of 5% and a rupture rate of 2%1 1,000 patients would need to undergo MR angiographic screening and 200 patients wot, ld need conventional cerebral angiography. Fifty patients with cerebral: aneurysms would need surgery to save one patient with an aneurysm before its rupture. As these numbers indicate, mass screening for cerebral aneurysms with MR angiography is not cost-effective at present. One problem is that the diagnostic accuracy of MR angiograplay for cerebral aneurysms is approximately 80% with 80% specificity and 80% sensitivity. Therefore, 20% of the patients undergoing screening for aneurysms with MR angiogmphy would need to be further studied with conventional angiograplay. Unfortunately, conventional angiogmphy carries a 0.3% risk of neurologic complications as well as a fatality risk of less than 0.1%. In addition, the combination of the high cost of MR units and the relatively slow throughput drives up the medical costs for MR studies. Another problem with MR angiographic screening for
$42
Vol. 3, Suppl. 1, April 1996
cerebral aneurysms is that tile natural history of the disorder has not been clarified. Because the rupture rate t of cerebral aneurysms is relatively low, in the range of 1-2%, the majority of aneurysms never rt, pture during the patient's lifetime. Some authorities believe that aneurysmal ruptures occur only when aneuwsms arise and enlarge very rapidly. Overall, it appears that at present the costs of MR studies, conventional angiography, and surgew, in addition to the expenses incurred by a relatively large medical staff, make screening with MR angiography infeasible. Randomized controlled trials should be undertaken, however, to establish the true cost-effectiveness of such a progmnl. Of course, patients should be informed of the details of mass screening, including the natural history of cerebral aneurysms, the diagnostic accuracy of MP, angiography, and complications associated with cerebral angiography and surgery. Even though mass screening may not be practical, screening in certain high-risk groups may be more practical. For instance, the incidence of cerebral aneurysm is considerab!y higher in asymptoinatic persons who have a family member who has a subamchnoid hemorrhage. Screening may be justified to detect unruptured aneurySlllS before a major catastrophic event occurs in such individuals. In addition, patients with polycystic kidney disease, fibromuscular dysplasia, and severe atherosclerotic disease of other vessels may be candidates for screening of cerebral aneurysms with MR angiogmphy [22], Technological advances may also make screening more attractive. Once the diagnostic accuracy of MR angiography is improved, and conventional angiograplay is not required for surgery, screening programs may be inore likely to be accepted. REFERENCES 1. Kassell NF, Torner JC. Size of intracranial aneurysms. Neurosurgery
1983;12:291-297. 2. Bonita R, Thomson S. Subarachnoid hemorrhage: epidemiology, diagnosis, management, and outcome. Stroke1985;16:591-594. 3. Wirth FP, Laws ER Jr, Piepgras D, Scott RM. Surgical treatment of incidental intracranial aneurysms. Neurosurgery1983;12:507-511. 4. Heiskanen O. Risks of surgery for unruptured intracranial aneurysms. J Neurosurg1986;65:451-453. 5. Nakagawa "1",Hashi K. The incidence and treatment of asymptomatic, unruptured cerebral aneurysms. J Neurosurg1994;80:217-223. 6. Schievink Wl, Limburg M, Dreissen JJR, Peeters FLM, ter Berg HWM. Screening for unruptured familial intracranial aneurysms: subarachnoid hemorrhage 2 years after angiography negative for aneurysms. Neurosurgery 1991;29:434-438. 7. Phillips LH, Whisnant JP, O'Fallon WM, Sundt TM Jr. The unchanging pattern of subarachnoid hemorrhage in a community. Neurology 1980; 30:1034-1040.
Vol. 3, Suppl. 1, April 1996
8. Wiebers DO, Tomer JC, Meissner I. Impact of unruptured intracranial aneurysms on public health in the United States. Stroke 1992;23:14161419. 9. Sekhar LN, Heros RC. Origin, growth, and rupture of saccular aneurysms: a review. Neurosurgery1981 ;8:248-260. 10. Wiebers DO, Whisnant JP, Sundt TM Jr, O'FaTlonWM. The significance of unruptured intracranial saccular aneurysms. J Neurosurg 1987;66:23-29. 11. Winn HR, Almaani WS, Berga SL, Jane JA, Richardson AE. The longterm outcome in patients with multiple aneurysms. J Neurosurg 1983; 59:642-651. 12. Heiskanen O. Risk of bleeding from unruptured aneurysms in cases with multiple intracranial aneurysms. J Neurosurg 1981;55:524-526. 13. Jane JA, Kassell NF, Tomer JC, Winn HR. The natural history of aneurysms and artedovenous malformations. J Neurosurg 1985;62:321-323. 14. Korogi Y, Takahashi M, Mabuchi N, et aL Intracranial aneurysms: diagnostic accuracy of three-dimensional, Fourier transform, time-of-flight MR angiography. Radiology1994;193:181-186. 15. Korogi Y, Takahashi M, Mabuchi N, et al. Intracranial vascular stenosis and occlusion: diagnostic accuracy of three-dimensional, Fourier trans-
SCREENING FOR INTRACRANIAL ANEURYSMS
form, time-of-flight MR angiography. Radiology 1994;193:187-193. 16. Korogi Y, Takahashi M, O'Uchi T, et al. Diagnostic accuracy of 3DFT timeof-flight MR angiography for intracranial aneurysms and steno-occlusive diseases: report on 1994 study (Fourth Report,of Special Committee). Jpn J Magn Reson Med 1994;14:415-421. 17. Waugh JR, Sacharias N. Arteriographic complications in the DSA era. Radiology 1992; 182:243-246. 18. Dion JE, Gates PC, Fox AJ, Barnett HJM, Blom RJ. Clinical events following neuroangiography: a prospective study. Stroke 1987;18:997-1004. 19. Hankey GJ, Wadow CP, Senar RJ. Cerebral angiographic risk in mild cerebrovascular disease. Stroke 1990;21:209-222. 20. Olivecrona H. Complications of cerebral angiography. Neuroradiology 1977;14:175-181. 21. Mclvor J, Steiner TJ, Perkin GD, Greenhalgh RM, Rose FC. Neurological morbidity of arch and carotid artedography in cerebrovasculardisease: the influence of contrast medium and radiologist.Br J Radio11987;60:117-122. 22. Ruggied PM, Poulos N, Masaryk TJ, et al. Occult intracranial aneurysms in polycystic kidney disease: screening with MR angiography. Radiology 1994;191:33-39.
$43