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“De Novo” aneurysms. A clinical review
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"De N o v o " Aneurysms A Clinical Review Carole A. Miller, M.D., Stephen A. Hill, M.D., and William E. Hunt, M.D. Ohio State University Hospital, Columbus, Ohio
Miller CA, Hill SA, Hunt WE. "De novo" aneurysms. A clinical review. Surg Neurol 1985;24:173-80.
The authors present seven cases drawn from 620 consecutive cases over 30 years, in which previously undemonstrated (hence "de novo") intracranial aneurysms formed and ruptured at intervals of 3-20 years, after clipping of an initial aneurysm. Six patients were treated for rupture of a second aneurysm. All six had undergone successful treatment of a previous aneurysm; pre- and postoperative angiography showed not only successful clipping of the first aneurysm but also no incidence of multiple aneurysms. In no case was a major artery occluded at the time of the initial surgery. The implications as to natural history and the advisability of repeated arteriography in some patients with aneurysms are discussed. KEY WORDS: "De novo" cerebral aneurysm; cerebral hemorrhage; Subarachnoid hemorrhage
Multiple intracranial arterial aneurysms are a well-recognized p h e n o m e n o n , but only rarely has a new aneurysm been d o c u m e n t e d after successful treatment for an aneurysm elsewhere. This report concerns seven such patients, six treated for berry aneurysms and one for pituitary tumor, who, at intervals o f 3 - 2 0 years, were found to have other aneurysms not seen on earlier angiograms. Such a "de novo" aneurysm might be considered a special case of multiple aneurysms in which the lesions appear in series rather than in parallel. Their incidence and behavior provide some insight into the poorly understood natural history o f these lesions. T h e reported incidence of initial subarachnoid hemorrhage in the general population varies from 4 per 100,000 per year to 19.4 per 100,000 per year [1,2,6, 12,17,22,44]. In, reports that specifically noted aneurysm as the etiology of the hemorrhage [7,30,41,46], incidence ranges from about 3 per 100,000 per year to Address reprint requests to: Carole A. Miller, M.D., University Hospital, N-911,410 West 10th Avenue, Columbus, Ohio 43210. © 1985 by Elsevier Science PublishingCo., Inc.
9.6 per 100,000 per year. In our consecutive series of 620 patients with intracranial saccular arterial aneurysm collected from 1954 to 1983 (29 years), the seven cases presented here (Table 1) suggest an incidence of "de novo" aneurysm formation and hemorrhage of three to four times the expected rate. The average postoperative observation was 16 years or 10,000 patient years. This would give a rate of about 60 per 100,000 per year.
Case Reports
Case 1 A 31-year-old woman suffered a sudden, severe, generalized headache while at work. She lost consciousness briefly, and awoke with a stiff neck and pain in her head. The diagnosis of subarachnoid hemorrhage, grade II [33], was confirmed by lumbar puncture. Panangiography showed an aneurysm in the left posterior communicating artery; the size of the aneurysm was 4 × 8 mm. T h e aneurysm was clipped on the second day after the hemorrhage with no untoward results. T h r e e years later a second subarachnoid hemorrhage occurred with severe retroorbital headache on the right side. She was again admitted to the hospital with grade II hemorrhage. Arteriography demonstrated a 2 × 4m m aneurysm in the right posterior communicating artery. T h e previously placed clip on the left side was in the appropriate position. On the day of admission, 1 day posthemorrhage, the aneurysm in the right posterior communicating artery was clipped. She was discharged without deficit.
Case 2 This 49-year-old woman had a subarachnoid hemorrhage, confirmed by lumbar puncture, while vacationing in Italy in 1967. She was admitted to Ohio State University Hospital on her return to this country. A right retrograde brachial arteriogram was normal: an arteriogram o f the left carotid artery showed a 1.5 × 2.0-cm aneurysm o f the internal carotid termination. A Mayfield clip was placed across the neck of the aneurysm, but 0090-3019/85/$3.30
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Table
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1.
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Clinical Summary of Seven Patients
Patient
Site of first First admission aoeurysm Grade
1. 31
WF
11-21-73
2. 49
WF
3. 41
Surgery
Lt. PCoA
II
Clip
4-13-67
Lt. lCA
Ia
Clip
WF
2-12-76
Rt. MCA
Il
Clip & coating
4. 30
WM
8-16-73
Rt. MCA
1V
Clip & coating
5. 51
WF
7-24-69
Rt. PCoA
IIl
Clip
6. 48
WF
5-16-58
Rt. PCoA
IV
Clip
7. 39
WF
8-31-70
Pituitary tumor
--
--
Outcome Recovery g deficit Recovery minimal deficit Recovery ~ deficit
Second admission
Site of second aneurysm Grade Surgery
3-6-77
Rt. PCoA
lI
Clip
6-11-78
1. A. 2. 1. 2. A.
O
(D
II
3-14-80
Basilar (Tip) Lt. PCoA ACoA Basilar (Tip)
Outcome Recovery ~ deficit No change to date
Recovery ~ moderate deficit Recovery g deficit
9-27-77
ACoA
III
7-26-76
1. ACoA 2. Rt. MCA
II
Recovery g deficit --
6-10-78
Basilar A. (Tip) Rt. PCoA
V
1. Clip Expired (ACoA) after clip 2. Clip of basilar Basilar Clip Recovery ~ no new deficit Clip & Recovery g coating deficit ACoA 6 Expired
III
Clip
6-21-79
Recovery g deficit
Abbreviations: ACoA = anterior communicating artery; F = female; ICA = internal carotid artery; Lt. - left; M = male; MCA = middle cerebral artery; PCoA - posterior communicating artery; Rt. = right.
incompletely occluded it, as demonstrated on postoperative angiograms. The middle cerebral artery was occluded at the site o f application o f a temporary clip, but there was good hemispheral collateral circulation. She recovered with mild right-sided hemiparesis but no aphasia. On her second admission, 11 years later, she presented with a 2-week history of right-sided ptosis. She denied diplopia, orbital pain, or defect in her visual field. A minimal spastic hemiparesis on the right side was noted, unchanged over the preceding 11 years. An arteriogram o f the left carotid artery showed a persistence of the nonoccluded portion o f the aneurysm from the previous 11 years, approximately 10 x 14 mm in size, located just at the left carotid bifurcation. The ascending frontoparietal artery now filled. Two new aneurysms were seen during the study. On the right there was a 2-mm infundibulum at the internal carotid-posterior communicating artery junction. A sessile aneurysm measuring 2 mm was seen on the right vertebral injection, between the right posterior cerebral and right superior cerebellar arteries, arising from the distal portion of the basilar artery. Surgical treatment was not advised. During subsequent outpatient examinations, her headache and ptosis had resolved completely and 1 year later had not recurred. They remain unexplained.
angiographic study was normal. H e r case was a clinical grade III on admission, and improved to a grade II. She underwent a right temporal craniotomy with clipping and coating o f the aneurysm of the right middle cerebral artery. She did well after the operation and was readmitred 8 months later for repeat angiography. This demonstrated that the aneurysm o f the middle cerebral artery had been successfully clipped and no other aneurysms in the anterior or the posterior circulation were demonstrated. Five years later the patient was readmitted to another hospital after having suffered a massive subarachnoid hemorrhage. At that time a huge basilar tip aneurysm was found and she expired following an operation (Figure 1).
Case 4 This 40-year-old man was admitted in 1973, following rupture of a single 6 x 3-mm aneurysm o f the right middle cerebral artery. H e underwent clipping and coating of the aneurysm and recovered with mild neurological deficit--a left-sided hemiparesis. In 1977, he suffered a second subarachnoid hemorrhage and was admitted with a grade III case. This time a 10 x 6-mm aneurysm was found on the anterior communicating artery. H e again made a satisfactory recovery after clipping and coating o f this aneurysm. T h e r e was no new neurological deficit (Figure 2).
Case 3 This 42-year-old woman was admitted to University Hospital in February 1976. An aneurysm in the right middle cerebral artery had bled; the remainder of the
Case 5 This 51-year-old woman was admitted in 1969, with a headache and stiff neck. The cerebrospinal fluid was
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Figure 1. Case 3--vertebral angiogram 2-1976 after rupture of aneurysm of the right middle cerebral artery with no aneurysm seen. Angiogram of 3-21-80 u,ith large basilar tip aneurysm.
yellow on lumbar puncture and because o f focal neurological sign she was classified as a grade III case. Fourvessel angiography demonstrated a 3-mm aneurysm arising at the right posterior communicating artery. T h e aneurysm was clipped on posthemorrhage day 16 and she was discharged with a third nerve paresis, which later cleared, but there was no other neurological deficit. Eight years later at age 59, she had a sudden, severe, generalized headache and came to the emergency r o o m saying that her headache was "just like the other time." Arteriography demonstrated an aneurysm o f the anterior communicating artery measuring 12 x 8 ram; the d o m e of the aneurysm pointed inferiorly. T h e r e was also an aneurysm of the trifurcation of the right middle cerebral artery measuring 10 x 7 x 3 mm. T h e aneurysm o f the anterior communicating artery was clipped and
coated. N o attempt was made to approach the aneurysm of the middle cerebral artery.
Case 6
This 49-year-old woman was admitted in 1958, comatose and decerebrate (grade IV). Angiography demonstrated an aneurysm of the right posterior communicating artery. After her recovery from the acute ictus, the lesion was repaired and she was discharged in good condition but with a spastic left-sided hemiparesis. She was able to walk but had p o o r function of the left hand. She was readmitted 20 years later after an acute loss of consciousness, and remained comatose and unresponsive until her death 7 weeks later. Arteriographic studies p e r f o r m e d during the second week o f her hos-
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Figure 2. Case 4--angiogram of the left carotid artery: large aneurysm of the anterior communicating artery after clipping and coating of aneurysm of the right middle cerebralartery.
pital stay showed a basilar tip aneurysm measuring 20 × 25 mm with an irregular anterior wall. This aneurysm was not seen on the vertebral studies performed in 1958 (Figure 3).
Case 7 This 39-year-old woman first presented with Nelson's syndrome and a pituitary tumor for which she was op-
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erated upon in 1970. Preoperative angiography and a repeat study done in May 1979 failed to show any aneurysms. In July 1979, she was admitted in a confused state with headache and stiff neck. Computed axial tomography demonstrated hemorrhage in the chiasmal area. Initially it was thought she had hemorrhaged into recurrent pituitary tumor and no preoperative arteriography was done. At operation she was found to have an aneurysm o f the right posterior communicating artery; the aneurysm was clipped. She subsequently made a good recovery.
Discussion Figure 3. Case 6--Large aneurysm of the basilar tip demonstrated 20 years after successful clipping of an aneurysm of the right posterior communicating artery.
In 1964 Graf and Hamby [16] reported a patient with a right middle cerebral artery aneurysm (which was
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clipped) who died 3 years later o f a ruptured left middle cerebral artery mirror aneurysm which had not been visualized on the initial angiogram series. The authors introduced the term "de novo." This is possibly the first reported incident of this phenomenon. T h e r e have been nine other reported instances of de novo aneurysm formation. Gurdjian et al [ 18], in a study of 41 carotid ligations, mentioned one case of mirror aneurysm on the opposite carotid siphon "not seen on films earlier." Du Boulay [4] reported mirror aneurysms of the posterior communicating artery developing with a hiatus of 10 years. The initial lesion had been treated by carotid ligation. Somach and Shenkin [52] studied 20 patients with internal carotid artery ligation. They reported one case with an 8-year lapse between the first aneurysm (posterior communicating artery) and the second aneurysm (parasellar) on the opposite side, and another case with a 7-year hiatus between carotid ligation for an aneurysm of the left posterior communicating artery and fatal hemorrhage from an aneurysm o f the right anterior communicating a r t e r y - - t h e aneurysm was not visible on the first set of angiograms. They postulated that new aneurysms may arise due to altered pressure-flow relationship after carotid ligation. Heiskanen and Marttila [23], in a study of the risk from untreated second aneurysms, cite one case in which a clipped right middle cerebral artery sac was followed 10 years later by a previously undemonstrated aneurysm of the left posterior communicating artery. Klemme [29] reported a case in which the second aneurysm (left posterior communicating artery) followed right carotid ligation for an aneurysm of the right posterior communicating artery 9 years before. H e concluded that carotid stenosis, for any reason, changes the hemodynamics of the contralateral circle of Willis, making new aneurysms more likely to form. Winn et al [62] reported a case of mirror image left posterior communicating artery aneurysm occurring 3 years and 8 months after right common carotid ligation for a right posterior communicating artery aneurysm. Finally, Nukui et al [39] reported two cases in which new aneurysms were revealed. In the first, angiography was initially for severe head trauma; 8 years later aneurysms o f the anterior communicating artery and pericallosal artery were discovered and clipped. The other patient had placement of a clip for an aneurysm of the left internal carotid artery, but developed an aneurysm o f the left posterior communicating artery after a 3-year hiatus. Less well-documented but probable examples o f de novo aneurysms also exist [14,15,20,48,58]. With two exceptions [14,48] these appeared on the opposite internal carotid artery after carotid ligation for internal carotid or posterior communicating aneurysms.
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There are also reports that suggest de novo cases [31,33,37,38] but cannot be confirmed, usually because only unilateral angiography was performed at the time of the initial presentation. The existence of patients who bleed from second, "new" aneurysms has also been alluded to without detail by Symon [57], who believes most neurosurgeons have had this experience. The coexistence of aneurysms with sellar neoplasms (case 7) has been reviewed by Jakubowski and Kendall [27], who found 11 aneurysms among 150 pituitary adenomas and 33 craniopharyngiomas, an incidence of 6%. This is about twice the general population average. The 9-year interval between tumor and aneurysm in our case seems to argue a fortuitous coincidence of the two lesions in one patient. One problem with reviews of this kind is that what we assume to be a de novo aneurysm may have been present but unrecognized at the time of the first arteriograms. This question has been addressed by various authors, some documenting the rate of multiplicity, others attempting to estimate the rate o f false-negative arteriograms in patients with subarachnoid hemorrhage. T h e r e are even a few estimates of missed multiple lesions in patients thought to have single aneurysms [32,35]. In reported series, the incidence of multiple aneurysms discovered at time of arteriography, [3,34,36, 45,46,63], autopsy [5,8,9,24,61], or both [22,35,40] varies from 7.8% [3] to 31% [5], with 1 5 % - 2 0 % being the range most often accepted. Stehbens [55] has pointed out that the reported incidences of cerebrovascular diseases depend more upon the interest and thoroughness o f the seeker than upon any other factor, and this is clearly true for saccular aneurysms. McKissock et al [35] noted that 12% of patients thought in life to have harbored a single aneurysm were found at necropsy to have multiple lesions. Further, 8 % of their patients thought to have multiple aneurysms, based on findings ofangiography, actually had more than were expected. In all, 27 aneurysms in 20 patients were "missed." The most common site for these was the middle cerebral artery, with greater than 50% of the "missed" aneurysms being at the middle cerebral artery trifurcation. Some o f this error may be attributable to vasospasm preventing visualization of the lesions, or to the technical limits of radiography as it was then practiced: the concept of "missed aneurysms" remains. Locksley [32] estimated that of patients studied with bilateral carotid arteriograms and found to have an aneurysm, 2 % actually had a second, missed aneurysm. Perret and Nishioka [43] and Forster et al [13] studied patients with subarachnoid hemorrhage and negative angiograms, and estimated false-negative rates of 3.8% and 1.8%, respectively, a considerable improvement over earlier studies when the limits of radiographic technique caused 1 0 % - 1 5 % false-negative studies [19,42]. The
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reasons for failing to recognize aneurysms on arteriographic studies were studied by Perrett and Bull [42] in an autopsy-confirmed series o f 210 aneurysms [6,31,45,67,79]. The arguments concerning origin and etiology o f cerebral berry aneurysms have been summarized by Sekhar and H e r o s [49], and incorporate current views that aneurysms result from a combination of inherent or acquired tissue weakness plus hemodynamic effects [28,59,60]. T h e appearance o f de novo aneurysms supports this view and argues against the so-called "congenital" hypothesis. The use of the term "de novo" is misleading, of course, because all aneurysms arise at some point in the patient's life. Aneurysms are not congenital [ 10,54,55], although the vascular defect that causes predisposition to them probably is. Use o f the term "de novo" may be defended because aneurysm appearance, growth, and rupture is now documented [49,64,65]. Defects in the media are known to be especially large contralateral to established aneurysms and in mirror locations [ 11 ]. It may be that in combination with carotid ligation [3,51] or intracranial surgery for the initial aneurysm, the balance and periodicity o f pulsatile collateral flow are altered to allow aneurysmal expression, at fairly predictable sites, of what would otherwise remain a "preaneurysmal" lesion [21,25,47,50,53,56]. Many o f the early reports o f this entity involved contralateral aneurysm neoformation after treatment of the initial, symptomatic lesion [4,15,16,18,20,23,29,31, 52,62]. In the seven patients o f our series with prior aneurysms the de novo sacs were clearly ipsilateral in only one instance, clearly contralateral in three, and midway (anterior communicating or basilar tip) in four. Interestingly, four o f the six initial sacs were located in the posterior communicating artery, the site noted in many o f the earlier reports. It is probable that the reason for de novo aneurysm formation is the existence o f the same inherent defect that led to development o f the first aneurysm. It is not unreasonable to expect that medial defects, acquired injury o f the internal elastic lameUa, atherosclerosis, hypertension, and variations in the circle o f Willis will also cause a predisposition to further aneurysm formation. From a practical standpoint, these seven cases of"new" aneurysms over a 30-year period suggest that patients with an aneurysm are at an increased risk o f hemorrhage from another aneurysm at some later time. Since we do not have complete postoperative observations on our series, the risk is probably higher than reported here. Certainly the clinician's level o f suspicion should be high if a patient with a previously treated aneurysm presents with any symptoms that suggest another lesion, even if postoperative arteriography was normal. Angi-
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ography should be considered if a typical headache or any suggestion of cranial nerve dysfunction develops or if special risk factors can be identified. Routine late angiography, though it may in the future be justifiable, would be of a questionable risk-benefit ratio at this time. New high-resolution imaging techniques may make this feasible in the future.
Conclusions Seven patients in a series o f 620 cases over 29 years developed symptomatic, previously undemonstrated intracranial aneurysms. This is an incidence of at least 100 cases per 100,000 per year in known patients with aneurysms. Since the incidence of de novo cases in our material is based mainly on aneurysm rupture, the true incidence must be higher. The statistics are also expressed in terms of total number of patients with aneurysms admitted for neurosurgical care, 1954-1983, and have not been corrected for patients who died during or after the initial attack. The population at risk, patients who survive long enough to develop new lesions, is thus greatly overestimated, probably by a factor of two or three, because of incomplete observations. The possibility exists that some individuals with de novo aneurysms, lost to observation, have become symptomatic and died without diagnosis or autopsy. These would not enter our statistics. The estimates for de novo aneurysms given here are, therefore, minimal figures.
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36. Moyes PD. Surgical treatment of multiple aneurysms and of incidentally-discovered unruptured aneurysms. J Neurosurg 1971 ; 35:291-5. 37. Nishioka H. Results of the treatment of intracranial aneurysms by occlusion of the carotid artery in the neck. J Neurosurg 1966;25:660-704. 38. Nofzinger JD, Britt LG, Murphey F, PateJW. Unusual treatment of an intracranial aneurysm contralateral to a previous common carotid ligation. A case report. J Neurosurg 1965 ;22:182-4. 39. Nukui H, Nagaya T, Miyagi O, Tamada J, Kaneko M, Sasaki H, Mitsuka S, Kawafuchi J, Kohno H, Kanoh T. Development of new aneurysm and enlargement of small aneurysm. Report of seven cases. Neurol Med Chir (Tokyo) 1982;22:437-45. 40. Overgaard J, Riishede J. Multiple cerebral saccular aneurysms. Acta Neurol Stand 1965;41:363-71. 41. Pakarinen S. Incidence, etiology, and prognosis of primary subarachnoid hemorrhage. A study based on 589 cases diagnosed in a defined urban population during a defined period. Acta Neurol Scand 1967;43:Suppl 29:1-28. 42. Perrett LV, Bull JWD. Some aspects of subarachnoid hemorrhage: a symposium III. The accuracy of radiology in demonstrating ruptured intracranial aneurysms. Br J Radiol 1959; 32:85-92. 43. Perret G, Nishioka H. Diagnostic value and complications of carotid and vertebral angiography. In: Sahs AL, Perret GE, Locksley HB, Nishioka H, editors, lntracranial aneurysms and subarachnoid hemorrhage. A cooperative study. Philadelphia: JB. Lippincott, 1969:109-24. 44. Phillips LH 2d, Whisnant JP, O'Fallon WM, Sundt TM Jr. The unchanging pattern of subarachnoid hemorrhage in a community. Neurology (NY) 1980;30:1034-40. 45. Poppen JL, Fager CA. Multiple intracranial aneurysms. J Neurosurg 1959;16:581-9. 46. Rasmussen P, Busch H, HaaseJ, HansenJ, Harmsen A, Knudsen V, Marcussen E, Midholm ST, Olsen RB, Rosenorn J, Schmidt K, Voldby B, Hansen L. Intracranial saccular aneurysms. Results of treatment in 851 patients. Acta Neurochir (Wien) 1980;53:1-17. 47. Riggs HE, Rupp C. Military aneurysms. Relation of anomalies of the circle of Willis to aneurysm fi)rmation. J Neuropathol Exp Neurol 1942;1:442. 48. Salar G, Mingrino S. Development of intracranial saccular aneurysms: report of two cases. Neurosurgery 1981;8:462-5. 49. Sekhar LN, Heros RC. Origin, growth, and rupture of saccular aneurysms: a review. Neurosurgery 1981;8:248-60. 50. Sheffield EA, Weller RO. Age changes at cerebral artery bifurcations and the pathogenesis of berry aneurysms. J Neurol Sci 1980;46:341-52. 5 l. Shenkin HA, Cabiese F, van den Noordt G, Sayers P, Coopperman R. The hemodynamic effect of unilateral carotid ligation on the cerebral circulation of man. J Neurosurg 1951 ;8:38-45. 52. Somach FM, Shenkin HA. Angiographic end-results of carotid ligation in the treatment of carotid aneurysm..l Neurosurg 1966;24:966-74. 53. Spallone A, Cantore G. The role of extracranial carotid abnormalities in the genesis of cerebral aneurysms. J Neurosurg 1981 ;55:693-700. 54. Stehbens WE. Medial defects of the cerebral arteries of man. J Pathol Bacteriol 1959;78:179-85. 55. Stehbens WE. Intracranial Arterial Aneurysms. In: Pathology of the Cerebral Blood Vessels, St. Louis: C.V. Mosby, 1972:351-470. 56. Stehbens WE. Histopathology of cerebral aneurysms. Arch Neurol 1963;8:272-85. 57. Symon L. Subarachnoid hemorrhage from intracranial aneurysm and angioma. In: Russell RWR, editor. Cerebral arterial disease. Edinburgh: Churchill Livingstone, 1976:231-61.
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58. Waga S, Morikawa A. Aneurysm developing on the infundibular widening of the posterior communicating artery. Surg Neurol 1979;11:125-7. 59. Walker AE, Allegre GW. The pathology and pathogenesis of cerebral aneurysms. J Neuropathol Exp Neurol 1954; 13:248-59. 60. Walton JN. Observations on the pathogenesis of intracranial aneurysms. In: Subarachnoid Hemorrhage. Edinburgh: E & S Livingstone, 1956. 61. Williams RR, Bahn RC, Sayre GP. Congenital cerebral aneurysms. Proc Mayo Clin 1955;30:161-8. 62. Winn HR, Richardson AE, Jane JA. Late morbidity and mortality
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of common carotid ligation for posterior communicating aneurysms. A comparison to conservative treatment. J Neurosurg 1977;47:727-36. 63. Yoshimoto T, Kayama T, Kodama N, Suzuki J. Distribution of intracranial aneurysms. Tohoku J Exp Med 1978;126:125-32. 64. Yoshimoto T, Suzuki J. Eight-year documented study of an aneurysm growth at the origin of the posterior communicating artery. Neurol Surg 1974;2:571-73. 65. Young B, Meacham WF, Allen JH. Documented enlargement and rupture of a small arterial sacculation. Case report. J Neurosurg 1971;34:814-7.
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"De N o v o " Aneurysms A Clinical Review Carole A. Miller, M.D., Stephen A. Hill, M.D., and William E. Hunt, M.D. Ohio State University Hospital, Columbus, Ohio
Miller CA, Hill SA, Hunt WE. "De novo" aneurysms. A clinical review. Surg Neurol 1985;24:173-80.
The authors present seven cases drawn from 620 consecutive cases over 30 years, in which previously undemonstrated (hence "de novo") intracranial aneurysms formed and ruptured at intervals of 3-20 years, after clipping of an initial aneurysm. Six patients were treated for rupture of a second aneurysm. All six had undergone successful treatment of a previous aneurysm; pre- and postoperative angiography showed not only successful clipping of the first aneurysm but also no incidence of multiple aneurysms. In no case was a major artery occluded at the time of the initial surgery. The implications as to natural history and the advisability of repeated arteriography in some patients with aneurysms are discussed. KEY WORDS: "De novo" cerebral aneurysm; cerebral hemorrhage; Subarachnoid hemorrhage
Multiple intracranial arterial aneurysms are a well-recognized p h e n o m e n o n , but only rarely has a new aneurysm been d o c u m e n t e d after successful treatment for an aneurysm elsewhere. This report concerns seven such patients, six treated for berry aneurysms and one for pituitary tumor, who, at intervals o f 3 - 2 0 years, were found to have other aneurysms not seen on earlier angiograms. Such a "de novo" aneurysm might be considered a special case of multiple aneurysms in which the lesions appear in series rather than in parallel. Their incidence and behavior provide some insight into the poorly understood natural history o f these lesions. T h e reported incidence of initial subarachnoid hemorrhage in the general population varies from 4 per 100,000 per year to 19.4 per 100,000 per year [1,2,6, 12,17,22,44]. In, reports that specifically noted aneurysm as the etiology of the hemorrhage [7,30,41,46], incidence ranges from about 3 per 100,000 per year to Address reprint requests to: Carole A. Miller, M.D., University Hospital, N-911,410 West 10th Avenue, Columbus, Ohio 43210. © 1985 by Elsevier Science PublishingCo., Inc.
9.6 per 100,000 per year. In our consecutive series of 620 patients with intracranial saccular arterial aneurysm collected from 1954 to 1983 (29 years), the seven cases presented here (Table 1) suggest an incidence of "de novo" aneurysm formation and hemorrhage of three to four times the expected rate. The average postoperative observation was 16 years or 10,000 patient years. This would give a rate of about 60 per 100,000 per year.
Case Reports
Case 1 A 31-year-old woman suffered a sudden, severe, generalized headache while at work. She lost consciousness briefly, and awoke with a stiff neck and pain in her head. The diagnosis of subarachnoid hemorrhage, grade II [33], was confirmed by lumbar puncture. Panangiography showed an aneurysm in the left posterior communicating artery; the size of the aneurysm was 4 × 8 mm. T h e aneurysm was clipped on the second day after the hemorrhage with no untoward results. T h r e e years later a second subarachnoid hemorrhage occurred with severe retroorbital headache on the right side. She was again admitted to the hospital with grade II hemorrhage. Arteriography demonstrated a 2 × 4m m aneurysm in the right posterior communicating artery. T h e previously placed clip on the left side was in the appropriate position. On the day of admission, 1 day posthemorrhage, the aneurysm in the right posterior communicating artery was clipped. She was discharged without deficit.
Case 2 This 49-year-old woman had a subarachnoid hemorrhage, confirmed by lumbar puncture, while vacationing in Italy in 1967. She was admitted to Ohio State University Hospital on her return to this country. A right retrograde brachial arteriogram was normal: an arteriogram o f the left carotid artery showed a 1.5 × 2.0-cm aneurysm o f the internal carotid termination. A Mayfield clip was placed across the neck of the aneurysm, but 0090-3019/85/$3.30
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Table
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1.
Miller et al
Clinical Summary of Seven Patients
Patient
Site of first First admission aoeurysm Grade
1. 31
WF
11-21-73
2. 49
WF
3. 41
Surgery
Lt. PCoA
II
Clip
4-13-67
Lt. lCA
Ia
Clip
WF
2-12-76
Rt. MCA
Il
Clip & coating
4. 30
WM
8-16-73
Rt. MCA
1V
Clip & coating
5. 51
WF
7-24-69
Rt. PCoA
IIl
Clip
6. 48
WF
5-16-58
Rt. PCoA
IV
Clip
7. 39
WF
8-31-70
Pituitary tumor
--
--
Outcome Recovery g deficit Recovery minimal deficit Recovery ~ deficit
Second admission
Site of second aneurysm Grade Surgery
3-6-77
Rt. PCoA
lI
Clip
6-11-78
1. A. 2. 1. 2. A.
O
(D
II
3-14-80
Basilar (Tip) Lt. PCoA ACoA Basilar (Tip)
Outcome Recovery ~ deficit No change to date
Recovery ~ moderate deficit Recovery g deficit
9-27-77
ACoA
III
7-26-76
1. ACoA 2. Rt. MCA
II
Recovery g deficit --
6-10-78
Basilar A. (Tip) Rt. PCoA
V
1. Clip Expired (ACoA) after clip 2. Clip of basilar Basilar Clip Recovery ~ no new deficit Clip & Recovery g coating deficit ACoA 6 Expired
III
Clip
6-21-79
Recovery g deficit
Abbreviations: ACoA = anterior communicating artery; F = female; ICA = internal carotid artery; Lt. - left; M = male; MCA = middle cerebral artery; PCoA - posterior communicating artery; Rt. = right.
incompletely occluded it, as demonstrated on postoperative angiograms. The middle cerebral artery was occluded at the site o f application o f a temporary clip, but there was good hemispheral collateral circulation. She recovered with mild right-sided hemiparesis but no aphasia. On her second admission, 11 years later, she presented with a 2-week history of right-sided ptosis. She denied diplopia, orbital pain, or defect in her visual field. A minimal spastic hemiparesis on the right side was noted, unchanged over the preceding 11 years. An arteriogram o f the left carotid artery showed a persistence of the nonoccluded portion o f the aneurysm from the previous 11 years, approximately 10 x 14 mm in size, located just at the left carotid bifurcation. The ascending frontoparietal artery now filled. Two new aneurysms were seen during the study. On the right there was a 2-mm infundibulum at the internal carotid-posterior communicating artery junction. A sessile aneurysm measuring 2 mm was seen on the right vertebral injection, between the right posterior cerebral and right superior cerebellar arteries, arising from the distal portion of the basilar artery. Surgical treatment was not advised. During subsequent outpatient examinations, her headache and ptosis had resolved completely and 1 year later had not recurred. They remain unexplained.
angiographic study was normal. H e r case was a clinical grade III on admission, and improved to a grade II. She underwent a right temporal craniotomy with clipping and coating o f the aneurysm of the right middle cerebral artery. She did well after the operation and was readmitred 8 months later for repeat angiography. This demonstrated that the aneurysm o f the middle cerebral artery had been successfully clipped and no other aneurysms in the anterior or the posterior circulation were demonstrated. Five years later the patient was readmitted to another hospital after having suffered a massive subarachnoid hemorrhage. At that time a huge basilar tip aneurysm was found and she expired following an operation (Figure 1).
Case 4 This 40-year-old man was admitted in 1973, following rupture of a single 6 x 3-mm aneurysm o f the right middle cerebral artery. H e underwent clipping and coating of the aneurysm and recovered with mild neurological deficit--a left-sided hemiparesis. In 1977, he suffered a second subarachnoid hemorrhage and was admitted with a grade III case. This time a 10 x 6-mm aneurysm was found on the anterior communicating artery. H e again made a satisfactory recovery after clipping and coating o f this aneurysm. T h e r e was no new neurological deficit (Figure 2).
Case 3 This 42-year-old woman was admitted to University Hospital in February 1976. An aneurysm in the right middle cerebral artery had bled; the remainder of the
Case 5 This 51-year-old woman was admitted in 1969, with a headache and stiff neck. The cerebrospinal fluid was
"De Now~" Aneurysms
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175
Figure 1. Case 3--vertebral angiogram 2-1976 after rupture of aneurysm of the right middle cerebral artery with no aneurysm seen. Angiogram of 3-21-80 u,ith large basilar tip aneurysm.
yellow on lumbar puncture and because o f focal neurological sign she was classified as a grade III case. Fourvessel angiography demonstrated a 3-mm aneurysm arising at the right posterior communicating artery. T h e aneurysm was clipped on posthemorrhage day 16 and she was discharged with a third nerve paresis, which later cleared, but there was no other neurological deficit. Eight years later at age 59, she had a sudden, severe, generalized headache and came to the emergency r o o m saying that her headache was "just like the other time." Arteriography demonstrated an aneurysm o f the anterior communicating artery measuring 12 x 8 ram; the d o m e of the aneurysm pointed inferiorly. T h e r e was also an aneurysm of the trifurcation of the right middle cerebral artery measuring 10 x 7 x 3 mm. T h e aneurysm o f the anterior communicating artery was clipped and
coated. N o attempt was made to approach the aneurysm of the middle cerebral artery.
Case 6
This 49-year-old woman was admitted in 1958, comatose and decerebrate (grade IV). Angiography demonstrated an aneurysm of the right posterior communicating artery. After her recovery from the acute ictus, the lesion was repaired and she was discharged in good condition but with a spastic left-sided hemiparesis. She was able to walk but had p o o r function of the left hand. She was readmitted 20 years later after an acute loss of consciousness, and remained comatose and unresponsive until her death 7 weeks later. Arteriographic studies p e r f o r m e d during the second week o f her hos-
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Figure 2. Case 4--angiogram of the left carotid artery: large aneurysm of the anterior communicating artery after clipping and coating of aneurysm of the right middle cerebralartery.
pital stay showed a basilar tip aneurysm measuring 20 × 25 mm with an irregular anterior wall. This aneurysm was not seen on the vertebral studies performed in 1958 (Figure 3).
Case 7 This 39-year-old woman first presented with Nelson's syndrome and a pituitary tumor for which she was op-
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erated upon in 1970. Preoperative angiography and a repeat study done in May 1979 failed to show any aneurysms. In July 1979, she was admitted in a confused state with headache and stiff neck. Computed axial tomography demonstrated hemorrhage in the chiasmal area. Initially it was thought she had hemorrhaged into recurrent pituitary tumor and no preoperative arteriography was done. At operation she was found to have an aneurysm o f the right posterior communicating artery; the aneurysm was clipped. She subsequently made a good recovery.
Discussion Figure 3. Case 6--Large aneurysm of the basilar tip demonstrated 20 years after successful clipping of an aneurysm of the right posterior communicating artery.
In 1964 Graf and Hamby [16] reported a patient with a right middle cerebral artery aneurysm (which was
"De Novo" Aneurysms
clipped) who died 3 years later o f a ruptured left middle cerebral artery mirror aneurysm which had not been visualized on the initial angiogram series. The authors introduced the term "de novo." This is possibly the first reported incident of this phenomenon. T h e r e have been nine other reported instances of de novo aneurysm formation. Gurdjian et al [ 18], in a study of 41 carotid ligations, mentioned one case of mirror aneurysm on the opposite carotid siphon "not seen on films earlier." Du Boulay [4] reported mirror aneurysms of the posterior communicating artery developing with a hiatus of 10 years. The initial lesion had been treated by carotid ligation. Somach and Shenkin [52] studied 20 patients with internal carotid artery ligation. They reported one case with an 8-year lapse between the first aneurysm (posterior communicating artery) and the second aneurysm (parasellar) on the opposite side, and another case with a 7-year hiatus between carotid ligation for an aneurysm of the left posterior communicating artery and fatal hemorrhage from an aneurysm o f the right anterior communicating a r t e r y - - t h e aneurysm was not visible on the first set of angiograms. They postulated that new aneurysms may arise due to altered pressure-flow relationship after carotid ligation. Heiskanen and Marttila [23], in a study of the risk from untreated second aneurysms, cite one case in which a clipped right middle cerebral artery sac was followed 10 years later by a previously undemonstrated aneurysm of the left posterior communicating artery. Klemme [29] reported a case in which the second aneurysm (left posterior communicating artery) followed right carotid ligation for an aneurysm of the right posterior communicating artery 9 years before. H e concluded that carotid stenosis, for any reason, changes the hemodynamics of the contralateral circle of Willis, making new aneurysms more likely to form. Winn et al [62] reported a case of mirror image left posterior communicating artery aneurysm occurring 3 years and 8 months after right common carotid ligation for a right posterior communicating artery aneurysm. Finally, Nukui et al [39] reported two cases in which new aneurysms were revealed. In the first, angiography was initially for severe head trauma; 8 years later aneurysms o f the anterior communicating artery and pericallosal artery were discovered and clipped. The other patient had placement of a clip for an aneurysm of the left internal carotid artery, but developed an aneurysm o f the left posterior communicating artery after a 3-year hiatus. Less well-documented but probable examples o f de novo aneurysms also exist [14,15,20,48,58]. With two exceptions [14,48] these appeared on the opposite internal carotid artery after carotid ligation for internal carotid or posterior communicating aneurysms.
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177
There are also reports that suggest de novo cases [31,33,37,38] but cannot be confirmed, usually because only unilateral angiography was performed at the time of the initial presentation. The existence of patients who bleed from second, "new" aneurysms has also been alluded to without detail by Symon [57], who believes most neurosurgeons have had this experience. The coexistence of aneurysms with sellar neoplasms (case 7) has been reviewed by Jakubowski and Kendall [27], who found 11 aneurysms among 150 pituitary adenomas and 33 craniopharyngiomas, an incidence of 6%. This is about twice the general population average. The 9-year interval between tumor and aneurysm in our case seems to argue a fortuitous coincidence of the two lesions in one patient. One problem with reviews of this kind is that what we assume to be a de novo aneurysm may have been present but unrecognized at the time of the first arteriograms. This question has been addressed by various authors, some documenting the rate of multiplicity, others attempting to estimate the rate o f false-negative arteriograms in patients with subarachnoid hemorrhage. T h e r e are even a few estimates of missed multiple lesions in patients thought to have single aneurysms [32,35]. In reported series, the incidence of multiple aneurysms discovered at time of arteriography, [3,34,36, 45,46,63], autopsy [5,8,9,24,61], or both [22,35,40] varies from 7.8% [3] to 31% [5], with 1 5 % - 2 0 % being the range most often accepted. Stehbens [55] has pointed out that the reported incidences of cerebrovascular diseases depend more upon the interest and thoroughness o f the seeker than upon any other factor, and this is clearly true for saccular aneurysms. McKissock et al [35] noted that 12% of patients thought in life to have harbored a single aneurysm were found at necropsy to have multiple lesions. Further, 8 % of their patients thought to have multiple aneurysms, based on findings ofangiography, actually had more than were expected. In all, 27 aneurysms in 20 patients were "missed." The most common site for these was the middle cerebral artery, with greater than 50% of the "missed" aneurysms being at the middle cerebral artery trifurcation. Some o f this error may be attributable to vasospasm preventing visualization of the lesions, or to the technical limits of radiography as it was then practiced: the concept of "missed aneurysms" remains. Locksley [32] estimated that of patients studied with bilateral carotid arteriograms and found to have an aneurysm, 2 % actually had a second, missed aneurysm. Perret and Nishioka [43] and Forster et al [13] studied patients with subarachnoid hemorrhage and negative angiograms, and estimated false-negative rates of 3.8% and 1.8%, respectively, a considerable improvement over earlier studies when the limits of radiographic technique caused 1 0 % - 1 5 % false-negative studies [19,42]. The
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reasons for failing to recognize aneurysms on arteriographic studies were studied by Perrett and Bull [42] in an autopsy-confirmed series o f 210 aneurysms [6,31,45,67,79]. The arguments concerning origin and etiology o f cerebral berry aneurysms have been summarized by Sekhar and H e r o s [49], and incorporate current views that aneurysms result from a combination of inherent or acquired tissue weakness plus hemodynamic effects [28,59,60]. T h e appearance o f de novo aneurysms supports this view and argues against the so-called "congenital" hypothesis. The use of the term "de novo" is misleading, of course, because all aneurysms arise at some point in the patient's life. Aneurysms are not congenital [ 10,54,55], although the vascular defect that causes predisposition to them probably is. Use o f the term "de novo" may be defended because aneurysm appearance, growth, and rupture is now documented [49,64,65]. Defects in the media are known to be especially large contralateral to established aneurysms and in mirror locations [ 11 ]. It may be that in combination with carotid ligation [3,51] or intracranial surgery for the initial aneurysm, the balance and periodicity o f pulsatile collateral flow are altered to allow aneurysmal expression, at fairly predictable sites, of what would otherwise remain a "preaneurysmal" lesion [21,25,47,50,53,56]. Many o f the early reports o f this entity involved contralateral aneurysm neoformation after treatment of the initial, symptomatic lesion [4,15,16,18,20,23,29,31, 52,62]. In the seven patients o f our series with prior aneurysms the de novo sacs were clearly ipsilateral in only one instance, clearly contralateral in three, and midway (anterior communicating or basilar tip) in four. Interestingly, four o f the six initial sacs were located in the posterior communicating artery, the site noted in many o f the earlier reports. It is probable that the reason for de novo aneurysm formation is the existence o f the same inherent defect that led to development o f the first aneurysm. It is not unreasonable to expect that medial defects, acquired injury o f the internal elastic lameUa, atherosclerosis, hypertension, and variations in the circle o f Willis will also cause a predisposition to further aneurysm formation. From a practical standpoint, these seven cases of"new" aneurysms over a 30-year period suggest that patients with an aneurysm are at an increased risk o f hemorrhage from another aneurysm at some later time. Since we do not have complete postoperative observations on our series, the risk is probably higher than reported here. Certainly the clinician's level o f suspicion should be high if a patient with a previously treated aneurysm presents with any symptoms that suggest another lesion, even if postoperative arteriography was normal. Angi-
Miller et al
ography should be considered if a typical headache or any suggestion of cranial nerve dysfunction develops or if special risk factors can be identified. Routine late angiography, though it may in the future be justifiable, would be of a questionable risk-benefit ratio at this time. New high-resolution imaging techniques may make this feasible in the future.
Conclusions Seven patients in a series o f 620 cases over 29 years developed symptomatic, previously undemonstrated intracranial aneurysms. This is an incidence of at least 100 cases per 100,000 per year in known patients with aneurysms. Since the incidence of de novo cases in our material is based mainly on aneurysm rupture, the true incidence must be higher. The statistics are also expressed in terms of total number of patients with aneurysms admitted for neurosurgical care, 1954-1983, and have not been corrected for patients who died during or after the initial attack. The population at risk, patients who survive long enough to develop new lesions, is thus greatly overestimated, probably by a factor of two or three, because of incomplete observations. The possibility exists that some individuals with de novo aneurysms, lost to observation, have become symptomatic and died without diagnosis or autopsy. These would not enter our statistics. The estimates for de novo aneurysms given here are, therefore, minimal figures.
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58. Waga S, Morikawa A. Aneurysm developing on the infundibular widening of the posterior communicating artery. Surg Neurol 1979;11:125-7. 59. Walker AE, Allegre GW. The pathology and pathogenesis of cerebral aneurysms. J Neuropathol Exp Neurol 1954; 13:248-59. 60. Walton JN. Observations on the pathogenesis of intracranial aneurysms. In: Subarachnoid Hemorrhage. Edinburgh: E & S Livingstone, 1956. 61. Williams RR, Bahn RC, Sayre GP. Congenital cerebral aneurysms. Proc Mayo Clin 1955;30:161-8. 62. Winn HR, Richardson AE, Jane JA. Late morbidity and mortality
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of common carotid ligation for posterior communicating aneurysms. A comparison to conservative treatment. J Neurosurg 1977;47:727-36. 63. Yoshimoto T, Kayama T, Kodama N, Suzuki J. Distribution of intracranial aneurysms. Tohoku J Exp Med 1978;126:125-32. 64. Yoshimoto T, Suzuki J. Eight-year documented study of an aneurysm growth at the origin of the posterior communicating artery. Neurol Surg 1974;2:571-73. 65. Young B, Meacham WF, Allen JH. Documented enlargement and rupture of a small arterial sacculation. Case report. J Neurosurg 1971;34:814-7.