Not uncommonly, cerebral microaneurysms are found incidentally during surgery for another previously diagnosed cerebral aneurysm(s). The frequency and angiographic characteristics of such incidental microaneurysms are retrospectively summarized. Seventeen patients were identified as harboring incidental microaneurysms, comprising 4.9% of the whole series. The middle cerebral artery (MCA) was the most frequent location (seven cases, 41 %) of these microaneurysms. There was a tendency for MCA microaneurysms to be contiguous to a previously known, larger aneurysm at the same location. Neurosurgeons as well as interventional neuroradiologists should be aware of the possible presence of these incidental microaneurysms while treating patients with a cerebral aneurysm(s). Although the actual clinical implications of these incidental microaneurysms have not been elucidated, the few additional risks to patients already surgically exposed for the treatment of another aneurysm, along with the possible benefit of preventing their rupture and growth, would justify the surgical treatment of these microaneurysms. [Neurol Res 2001; 23: 304-308]
Keywords: Microaneurysm; incidental; angiogram; clipping; wrapping
INTRODUCTION
Cerebral microaneurysms are defined as 'aneurysms having a diameter of less than 3 mm1,2. Occasionally, microaneurysms are found incidentally during surgery for another previously diagnosed aneurysm(s), and they have been called 'baby aneurysms', or 'angiographically occult microaneurysms'1-3. The clinical significance of these microaneurysms remains unclear, although it has recently been reported that aneurysms having a diameter of less than 5 mm very rarely rupture 4, neurosurgeons occasionally encounter incidental microaneurysms whose aneurysmal wall is very thin and which show signs of impending rupture. Moreover, regrowth of a previously clipped aneurysm or development of a de novo aneurysm, often attributed as a cause of delayed rebleeding after successful clipping of a previously ruptured aneurysm5, may possibly be related to the existence of an occult microaneurysm. So far, only a few studies have documented the actual frequency of encountering such incidental microaneurysms1,3. The frequency and angiographic characteristics of the incidental microaneurysms are summarized, and their clinical implications are discussed.
PATIENTS AND METHODS
The authors retrospectively investigated the medical records, operation charts and intra-operative videotapes of 351 patients who underwent surgical treatment for a cerebral aneurysms) at our institution from January 1989 to December 1998. Most of the patients underwent 3- or 4-vessel digital-subtraction angiogram (DSA) with antero-posterior, lateral, and bilateral oblique projections before the surgery. Angiograms were examined by a group of experienced neurosurgeons and neuroradiologists.
RESULTS
Seventeen patients were identified as harboring incidental microaneurysms, comprising 4.9% (17 of 351 patients) of the whole series. Each patient had a single incidental microaneurysm. The clinical characteristics of these 17 patients are summarized in Table 1. They comprised six men and 11 women. The average age at the time of presentation was 57.8 years for the men and 55.4 years for the women. Seven patients presented with subarachnoid hemorrhage (SAH), nine patients underwent surgery for a previously diagnosed asymptomatic unruptured aneurysm(s), and the remaining one patient presented with the oculomotor nerve palsy due to the mass effect of an aneurysm. All patients were operated on via the pterional approach following Pronto-temporal craniotomy. All of the pre-operatively-- diagnosed aneurysms were clipped successfully. The diameter of the microaneurysms was equal to or less than 2 mm in all of the patients. The distribution of the aneurysms in the 17 cases were as follows: at the middle cerebral artery (MCA) bifurcation in seven, in the internal carotid (IC)-anterior choroidal artery (IC-Ach) in three, in the IC-posterior communicating (IC-PC) in three, in the anterior communicating artery (ACoA) in one, in the IC-ophthalmic (IC-Oph) artery in one, and at the IC-bifurcation (IC-Bif), in one. Although a statistical comparison was not considered due to the relatively small number of the patients, MCA microaneurysms were the most numerous (n = 7, 41 %) as compared with the frequency at any other locations. IC-Ach and IC-PC microaneurysms were the second most numerous (n= 3, 18%).
Notably, the four-sevenths of MCA aneurysms and the two-thirds of IC-Ach aneurysms were found to be contiguous to the previously diagnosed aneurysms. Representative cases are shown in Figures 1 and 2 and Figures 3 and 4, respectively.
Twelve of the 17 microaneurysms were successfully clipped. In the remaining five patients, although clipping was attempted, it was abandoned for fear of constricting the parent artery and these cases underwent wrapping of their aneurysm. The post-operative course was uneventful in all cases. The follow-up period after discharge ranged from 11 to 120 months (mean 34.6 months). None of the patients was noted to have neurological deterioration after discharge.
DISCUSSION
For neurosurgeons, it is not uncommon to find an incidental microaneurysm during surgery for a previously diagnosed aneurysm(s)1-3. Aside from the welldocumented limitation in resolution of angiograms, in which aneurysms less than 2 mm in diameter are often missed6 , there have been several explanations as to why microaneurysms often remain undetected until surgery. Karasawa et al.3 reported that microaneurysms are not visible because (1) they are sandwiched between two arteries, (2) they are completely obscured by a contiguous pre-operatively diagnosed aneurysm, (3) they are diagnosed pre-operatively as a bleb of a contiguously located aneurysm, (4) the height of the microaneurysm is extremely low. In our series, the majority of the incidental microaneurysms was considered to be obscured by a contiguous, pre-operatively noted aneurysm (nine cases).
The frequency of encountering incidental microaneurysms in the present series (4.9%) is intermediate between that reported by Karasawa et al. (3.7%) and that reported by Yasargil et al. (11.2%)1-3. The rate may vary from surgeon to surgeon, depending on the extent of surgical dissection and exploration, and also on the resolution of the angiograms in each surgical institution. Further development of new diagnostic modalities such as three-dimensional CT or MR angiography could lead to an increased detection rate of previously missed microaneurysms by DSA.7
Of note is that the MCA is the most frequent site of the incidental microaneurysms. In our series, seven out of the 17 incidental microaneurysms (41 %) were located at the MCA bifurcation. Similarly, in the series of Karasawa et al., the rate of incidental MCA microaneurysm was as high as 65% (13 of 20 cases)3. The reason is unclear, but the complex, entangled shape of the MCA bifurcation may make pre-operative detection of a microaneurysm(s) difficult. Another possibility is that since the MCA bifurcation is one of the most superficial from the brain surface, and the most easily accessible during aneurysm surgery, it is the site most frequently explored by neurosurgeons.
Interestingly, four of the seven MCA microaneurysms (57%) were contiguous to a larger aneurysm at the same location. This incidence is similar to the result of a previous study in which nine of 13 incidental MCA microaneurysms (69%) were contiguous to a larger MCA aneurysm3. Although it is unknown whether the vessel wall at the MCA bifurcation is especially fragile and thus prone to the multiple aneurysm formation, this could explain the polymorphism of the MCA aneurysms observed during surgery2. It is probable that small MCA microaneurysms may coalesce to form a multilobulated aneurysm. Similarly, there were two cases in which the view of an IC-Ach microaneurysm was hindered by a contiguously located IC-PC aneurysm. Utmost caution must be exercised so as not to injure the relatively small anterior choroidal artery during surgery.
The finding that incidental MCA microaneurysms have a tendency to occur in association with a previously known, larger aneurysms) at the same location may be cautiously interpreted by endovascular radiologists, because a microaneurysm may remain unobliterated and recurrence of a treated aneurysm may occur after presumed complete embolization. Microsurgery seems to be superior to endovascular surgery for the treatment of microaneurysms in that it allows obliteration of microaneurysms under direct vision within the surgical field.
The actual clinical implications of these incidental microaneurysms have not been clarified; it remains unknown whether these microaneurysms grow larger or remain of the same size, and whether they may eventually rupture or not. Although a recent study on the natural history of unruptured aneurysms has revealed that small aneurysms (less than 5 mm in diameter) only rarely rupture 4, there is no guarantee that the incidentally found microaneurysms, whose walls are occasionally thin and through which a whirling blood stream can be seen, would never rupture or grow larger. In that sense, the authors agree with Nussbaum et al.8 who report that with the microaneurysms being so readily accessible and in some cases already surgically exposed, with the patient exposed to the inherent risks of a craniotomy for the treatment of another aneurysm(s), they should be treated by some appropriate method. Especially when a microaneurysm is found during the surgery for a ruptured aneurysm, it should be treated aggressively as the risk of subsequent rupture is higher than that during the surgery for unruptured aneurysms.
Concerning the treatment of incidental microaneurysms, obliteration of the aneurysm with a clip has been recommended in appropriate cases, i.e., those with a definite aneurysmal neck3. However, in those cases in which clipping can compromise the blood flow of the parent artery or the perforators, wrapping of the microaneurysm seems more suitable1,3. No case with subsequent post-operative rupture has been reported among cases with microaneurysms treated by the wrapping technique1-3.
In summary, neurosurgeons may find an incidental microaneurysm during aneurysm surgery at a frequency of between 4% and 11 %. These microaneurysms have a tendency to be located at the MCA bifurcation. Surgeons as well as neuroradiologists should be aware of the possible presence of the incidental microaneurysms in the treatment of a cerebral aneurysm(s).
REFERENCES
1 Yasargil MG. Microneurosurgery 1, Stuttgart: Thierme, 1984
2 Yasargil MG. Microneurosurgery 2, Stuttgart: Thierme, 1984
3 Karasawa H, Matsumoto H, Naito H, Sugiyama K, Ueno J, Kin H. Angiographically unrecognized microaneurysms: Intraoperative observation and operative technique. Acta Neurochir (Wien) 1997; 139:416-420
4 International Study of Unruptured Intracranial Aneurysms Investigators. Unruptured intracranial aneurysms: Risks of rupture and risks of surgical intervention. N Engl J Med 1998; 339: 1774-1775
5 Tsutsumi K, Ueki K, Usui M, Kwak S, Kirino T. Risk of recurrent subarachnoid hemorrhage after surgical treatment of complete obliteration of cerebral aneurysms. Stroke 1998; 29: 2511-2513
6 Krayenbuhl H, Yasargil MG, Huber P. Cerebral Angiography, 2nd edn, Stuttgart: Thieme, 1982
7 Velthuis BK, van Leeuwen MS, Witkamp TD, Ramos LMP, van der Sprenkel JWB, Rinkel GJE. Computerized tomography angiography in patients with subarachnoid hemorrhage: From aneurysm detection to treatment without conventional angiography. J Neurosurg 1999; 91: 761-767
8 Nussbaum ES, Erickson DL. The fate of intracranial microaneurysms treated with bipolar electrocoagulation and parent vessel reinforcement. Neurosurgery 1999; 45: 1172-1175
Joji Inamasu, Sadao Suga, Takashi Horiguchi, Kazunori Akaji, Keita Mayanagi and Takeshi Kawase
Department of Neurosurgery, Keio University School of Medicine, Tokyo, Japan
Correspondence and reprint requests to: Joji Inamasu, MD, Department of Neurosurgery, Keio University School of Medicine, Shinanomachi 35, Shinjuku-ku, Tokyo 160-8582, Japan. [georges@med.keio.ac.jp] Accepted for publication August 2000.
Copyright Forefront Publishing Group Jun 2001
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