Multiple separated and multi-lobular aneurysms of the anterior communicating artery complex

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ABSTRACT

The anterior communicating artery complex [ACoA] is the most common site of occurrence of intracranial aneurysms, harboring about 30 % of these lesions. Multiple aneurysms account for 20 % of all cerebral aneurysms. Multiple aneurysms on the same artery correspond to 2.8 % of aneurysms, usually found in the internal carotid artery or middle cerebral artery. Multiple aneurysms of the ACoA are very rare and there are only a few cases reported in the literature.

In cases of multiple aneurysms of the anterior communicating artery complex, not all lesions may be detected on preoperative radiological studies, due to the complex angioarchiecture around the ACoA. Careful dissection is mandatory to ensure the completeness of aneurysm surgery. Multiple separated and multi-lobular aneurysms of the anterior communicating artery are unusual lesions and should be studied as a special topic.

The authors present four cases of these rare aneurysms, namely three multiple separated aneurysms and one multi-lobular aneurysm of the ACoA. Three of these patients presented with subarachnoid hemorrhage

[SAH]. There were no familial or arteriovenous malformation-related aneurysms reported in our series. We propose a new classification for this type of aneurysm on the ACoA. The literature is reviewed. The results, physiopathology and management are discussed.

Key words: anterior communicating artery, intracranial aneurysm, microsurgery, multiple aneurysms

INTRODUCTION

Multiple cerebral aneurysms reportedly account for 14-33% of all cerebral aneurysms. Incidence of multiple cerebral aneurysms has been increasing 1-15 since the development of imaging techniques such as digital subtraction angiography [DSA], MR angiography [MRA] and CT angiography [CTA]. However, multiple aneurysms from the same parent artery are uncommon. These have been found most frequently in the ICA, followed by the middle cerebral artery. Multiple separated aneurysms arising from the anterior communicating artery [ACoA] are rare, as well as complex multi-lobular aneurysms. In this article, we describe angiographic features and operative findings of these rare lesions.

CLINICAL MATERIAL AND METHODS

The main author performed microsurgical clipping in 127 patients with cerebral aneurysms from June 1995 to October 2007. All reports were analyzed and we performed surgery of 32 ACoA aneurysms. Findings of DSA and CIA were reviewed and compared with those of microsurgery. Only 3 patients were confirmed to have multiple separated aneurysms of the ACoA, and 1 patient confirmed to have a multilobular aneurysm. Data regarding clinical and imaging records are summarized on table 1.

Three patients presented with subarachnoid hemorrhage [SAH] and were diagnosed preoperatively, two of these with multiple aneurysms [figures 2A to 2D, 5A to 5F]. In these cases the size of ruptured aneurysms was larger than or at least the same as that of unruptured aneurysms. We classified the projection of the aneurysm into four types [fig. 1]. Multiple aneurysms may be associated with familial aneurysms or arteriovenous malformations, however, there was no such case in our series. These patients as well as the others with ACoA aneurysms were treated successfully with multiple clippings. The patients showed good outcome. All multiple aneurysms were of the type C [figures 2,3,4]. The fourth case may be classified as multi-lobular on angiogram views [figures 5A to 5F].

[FIGURA 1 OMITIR]

DISCUSSION

Despite advanced imaging techniques, multiple ACoA aneurysms may be misdiagnosed. They may not be detected on DSA due to complex angio-archiecture around the ACoA. CTA is helpful in distinguishing multiple aneurysms from multilobular ones with a common neck. We present 3 cases with multiple necks and 1 case with a complex multi-lobular aneurysm. The third one, however, may be misdiagnosed as multi-lobular.

Mathematical modeling of aneurysms is critical to understand the biophysical phenomena that contribute to aneurysm growth and rupture. With the advent of high quality 3-D imaging, many physical parameters regarding aneurysm size and shape can be recorded and studied. Isolated measurements, such as maximum size, location and presence of irregularities are fairly simple yet significant parameters that may predict future rupture. Certain geometric relationships such as aspect ratio [aneurysm height/neck width ratio] seem to correlate with rupture.

During surgery, exploration of the entire ACoA complex is necessary if preoperative CTA and DSA show multi-lobular ACoA aneurysms. In multiple aneurysms, the size of the sac is an important factor to identify the ruptured one. In our cases, the size of ruptured aneurysms was larger than or the same as that of unruptured aneurysms. In multiple aneurysms with separate necks, each aneurysm was occluded with separate clips. On the other hand, multi-lobular aneurysms with common neck were occluded with a single clip.

According to Yasargi1 (15), the anterior communicating artery aneurysm is situated in the most developed Al junction with the anterior communicating segment. There are 3 basic situations where the aneurysm may be originated, and confirmed during surgery:

1- Right Al junction in the cases where the left Al is hypoplastic.

2- Left junction Al.

3- Middle portion of ACoA in the case where the A1 are similar.

Big or giant aneurysms are complex. They are projected into multiple directions, and frequently show a large neck, making it difficulty to assess their exact limit and the parent artery. Fortunately, multiple aneurysms in the ACoA are unusual; a few points ought to be observed (5):

1- In bi- or tri-lobular aneurysms, special views and projections on the 3D-CT angiogram may be useful to obtain an exact diagnosis. The differentiation of 2 aneurysms from a bi-lobular one is very important in management planning.

2- The detection of the exact area of rupture is frequently unlikely.

3- Resection of rectus girus is necessary to obtain a correct view of the operatory field.

4-Adequate choice of clip is important, and we prefer straight and short ones. Occlusion of contra-lateral A1 must be avoided.

The same rules might be observed for multiple aneurysms in the anterior communicating artery.

After clipping, it is reasonable to administer papaverin in the vessels involved in the dissection (13) in order to avoid vasospasm due to mechanical manipulation. The histological difference between the wall of umuptured aneurysms and ruptured aneurysms is well known, however, the histological factor is not the only factor to be regarded concerning indication of an occlusion by clipping or conservative management (3,7,8). The asymmetrical pattern of flow in both carotid systems may provoke in efferent vessels fluid slipstream into aneurysms, becoming worse in multi-lobular aneurysms (11). Kato et al (6) presented similar findings, suggesting that the use of a 4D-CT angiogram to predict impending rupture in intact aneurysms, real-time, is less invasive and allows prioritizing the intervention for unruptured aneurysm cases, provides an effective screening of the high-risk population, and aids preoperative planning of clip application. Hayakawa et al (4) obtained electrocardiographically [ECG] gated multi-section helical CT images of 23 patients with ruptured intracranial aneurysms. 4D-CTA [3D-CT angiography plus phase data] images were generated by ECG-gated reconstruction. Four patients showed pulsation of an aneurysmal bleb. Clipping was performed in two of these patients, and the rupture site matched the pulsatile bleb seen in 4D-CTA (4). The point of maximum amplitude of pulsation of the aneurysm wall in unison with the RR interval of the electrocardiogram determines the potential rupture point (4,6). Regarding kissing aneurysms, Wanifuchi (14) described a 45-year-old male who presented with an extremely rare case of symmetrical kissing aneurysms located at both ends of the anterior communicating artery. Angiography and three-dimensional computed tomography [3D-CT angiography] clearly showed the relationship of the kissing aneurysms. The aneurysms were clipped through the right pterional approach. Temporary clipping of the anterior cerebral arteries for 5 minutes was required to gain enough operative space. The patient was discharged without neurological deficits. 3D-CT angiography, magnetic resonance angiography, or digital subtraction angiography may be useful for detecting kissing aneurysms, but the most important issue is awareness of this unusual condition. In our series we did not find any kissing aneurysms. Kiuosue (12) studied 47 berry aneurysms, which were submitted to endovascular treatment by means of coils. They concluded that four anatomic parameters correlated significantly withthe rate of successful occlusion: neck size (P = .014), shape (P=.042), dome-to-neck ratio (P <.01), and relationship to neighboring artery (P=.025). The difficulty score based on two parameters (dome-to-neck ratio and relationship to neighboring artery) significantly correlated with the occlusion rate (r= 0.63, P <.01). Multi-lobular aneurysms were difficult to occlude with coils, especially in the ACoA.

In Khandelwal's seriesl (10), clipping for ruptured aneurysms was preferred to coiling in fusiform-shaped aneurysms, large or giant aneurysms, MCA aneurysms, blister aneurysms, complex configurations, partially thrombosed aneurysms, and aneurysms associated with cerebral hemorrhage. They preferred coiling for basilar tip and trunk aneurysms, high anterior communicating artery aneurysms, patients in subacute stages of subarachnoid hemorrhage, and those with associated medical complications (10). As for complex, surgically intractable aneurysms, intentional reconstruction of the aneurysm neck followed by endovascular coiling should be always considered (1).

One old female patient in our series had an unruptured aneurysm of the ACoA. Our option for surgery considered another aneurysm, located in the posterior communicating segment. By the same craniotomy we clipped both.

The directions of the domes of multi-lobular aneurysms may be different, and Debono et al concluded after a detailed analysis of 119 consecutive communicating artery aneurysms (2) that in their experience the direction of the aneurysm was the main morphological criterion in choosing between microsurgery or endovascular procedure for the treatment of ACoA aneurysms. Also, they proposed that microsurgical clipping should be preferred for ACoA aneurysms with anterior direction, and depending on morphological criteria, endovascular packing for those with posterior direction (2). Newly developed aneurysm increasing and rupturing in a short period of time after clipping of the first aneurysm has been described (8). Our hypothesis for the event is that the phenomena may occur both where the parent artery was abnormal and in residual neck of complex multi-lobular aneurysms. The mechanisms of cerebral aneurysm recurrence and enlargement were investigated in 11 patients by Kato (8,9): two with dissecting aneurysms, six with fully grown aneurysms after neck clipping, one with enlarged aneurysm after dome clipping, and two with enlarged aneurysm due to recanalization after GDC coil embolization. They concluded that it is fundamentally important to ensure complete attachment of the internal elastic lamina around the aneurysm neck by precise neck clipping and effective embolization, with accurate positioning of remaining internal elastic lamina. In our opinion, the methods to determine a precise clipping have to be used anyway, at any price, because the effects of new enlargement may be catastrophic for the patient, causing severe morbidity as well as mortality, when there has previously been the chance to cure him/her. This leads to better understanding the importance to study the multi-lobular and multiple communicating aneurysms as a special topic separated from the berry simple shape aneurysm or elongated single aneurysm.

CONCLUSIONS

Multiple ACoA aneurysms may not be detected on preoperative study. Close proximity or small size of the lesions may be responsible for the preoperative false negative angiographic findings. Therefore, DSA and CIA should be performed carefully and precisely in multi-lobular aneurysms on ACoA. Additionally, it is recommended to keep this possibility in mind during ACoA aneurysm surgery.

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[FIGURA 3 OMITIR]

[FIGURA 4 OMITIR]

[FIGURA 5 OMITIR]

Comentario

He revisado el articulo de Pires Aguiar et al, sobre aneurismas múltiples del complejo comunicante anterior. Analizando una pequeña serie personal se logró juntar 4 casos de aneurismas múltiples de la ACoA, uno de ellos multilobulado. Con un registro muy preciso y completo de estos casos se hace un análisis completo de este tipo de aneurismas en la ACoA. Del punto de vista diagnóstico, en este tipo de casos es fundamental el estudio 3D. La angiotomografia tiene la ventaja sobre el estudio angiográfico convencional 31) que muestra todo el árbol vascular, no existiendo el problema que ocurre en el estudio por cateterismo en que la inyección en una carótida muchas veces no logra mostrar la imagen completa necesaria para tratar un aneurisma de esta localización, es decir los 7 vasos del complejo comunicante anterior: Al ipsilateral, A2 ipsilateral, ACoA, Recurrente Heubner ipsilateral, Al contralateral, A2 contralateral, Recurrente Heubner contralateral. Estos mismos vasos deben verse SIEMPRE en cirugía. En mi experiencia personal de 508 aneurismas (marzo 1999-abril 2008), me ha correspondido tratar varios casos de aneurismas múltiples de ACoA, que son muy complejos y que requieren de técnicas de clipaje múltiple. Del punto de vista técnico lo ideal es usar la mínima cantidad de clips posibles, es decir excluir todos los aneurismas que comparten el mismo eje con un solo clip, comenzando siempre por el aneurisma entre las dos A2 (superior y posterior) y luego los de orientación inferior. En el caso de aneurismas de Al distal contralateral, se debe considerar la presencia de más aneurismas contralaterales y realizar una cirugía bilateral, que es de mucho menor riesgo. El otro aspecto relevante es la craneotomía. Nosotros actualmente en el Equipo Vascular del INC, estamos preconizando las osteotomías orbitaria y orbitozigomática, sólo para aneurismas grandes o gigantes, o aquellos aneurismas de dirección superior o posterior en pacientes jóvenes, para evitar la retracción cerebral y la resección del gyrus recto. En pacientes de más de 50 años, una craneotomía pterional interfascial basal y con una exposición generosa de la porción temporal es suficiente junto con la apertura completa del valle silviano, siempre que las venas lo permitan, para tratar cualquier aneurisma del complejo comunicante anterior. Este es un trabajo muy bien escrito, analizado e ilustrado y sin duda viene a enriquecer nuestra revista.

Dr. Jorge Mura Castro

Coordinador Capítulo Vascular

Sociedad de Neurocirugía de Chile

Recibido: 29.11.07

Aceptado: 15.04.08

REFERENCES

(1-) Chen L, Kato Y, Sano H, Watanabe S, Yoneda M, Hayakawa M, Sadato A, Irie K, Negoro M, Karagiozov KL, Kanno T. Management of complex, surgically intractable intracranial aneurysms: the option for intentional reconstruction of aneurysm neck followed by endovascular coiling. Cerebrovasc Dis. 2007; 23:381-387.

(2-) Debono B, Proust F, Langlois O, Clavier E, Douvrin F, Derrey S, Freger P.. Ruptured anterior communicating artery aneurysm. Therapeutic options in 119 consecutive cases. Neurochirurgie. 2004; 50:21-32.

(3-) Frosen J, Piipo A, Paeteau A, Kangasniemi M, Niemelä M, Hernesniemi J, Jääskeläinen J. Growth factor receptor expression and remodeling of saccular cerebral artery aneurysms walls: implications for biological therapy preventing rupture. Neurosurgery 2006; 58:534-541.

(4-) Hayakawa M, Katada K, Anno H, Imizu S, Hayashi J, Irie K, Negoro M, Kato Y, Kanno T, Sano H.CT angiography with electrocardiographically gated reconstruction for visualizing pulsation of intracranial aneurysms: identification of aneurysmal protuberance presumably associated with wall thinning. AJNR Am J Nemoradiol. 2005; 26:1366-1369.

(5-) Inci S, Ozgen T. Multiple aneurysms of the anterior communicating artery: radiological and neurosurgical difficulties. J Neurosurg 2005; 102:495-502.

(6-) Kato Y, Hayakawa M, Sano H, Sunil MV, Imizu S, Yoneda M, Watanabe S, Abe M, Kanno T. Prediction of impending rupture in aneurysms using 4D-CTA: histopathological verification of a real-time minimally invasive tool in unruptured aneurysms. Minim Invasive Neurosurg. 2004;47:131-135.

(7-) Kato Y, Sano H, Dindorkar K, Abe M, Nagahisa S, Iwata S, Yoshida K, Kanno T. Treatment of umuptured intracranial aneurysms--a clinicopathological correlation. Acta Neurochir (Wien). 2001;143:681-686.

(8-) Kato Y, Sano H, Abe M, Hayakawa M, Yoshida K, Yoshimoto J, Kanno T. Newly developed aneurysm increased and ruptured 1 month after clipping of first aneurysm where the parent artery was abnormal. Acta Neurochir (Wien). 2001;143(2):187-195.

(9-) Kato Y, Sano H, Kanaoka N, Hayakawa M, Iritani K, Katada K, Kanno T, Abe M. Mechanism and prevention of enlargement or new development of aneurysm following treatment by clipping or coiling. Neurol Res. 2000; 22: 692-698.

(10-) Khandelwal P, Kato Y, Sano H, Yoneda M, Kanno T.Treatment of ruptured intracranial aneurysms: our approach. Minim Invasive Neurosurg. 2005 Dee; 48(6):325-329.

(11-) Kerber CW, Imbesi SG, Knox K. Flow dynamics in a lethal communicating artery aneurysm. AJNR Am J Nemoradiol 1999; 20:2000-2003.

(12-) Kiyosue H, Tanoue S, Okahar M, Hori Y, Nakamura T, Nagatomi H, Mori H. Anatomic Features Predictive of Complete Aneurysm Occlusion Can Be Determined with Three-Dimensional Digital Subtraction Angiography. AJNR Am J Neuroradiol 2002;23:1206-1213.

(13-) Sekhar L, Raso JL. Anterior communicating complex aneurysms. In: Cranial Microsurgery. Approaches and techniques. Sekhar LN, De Oliveira E (eds), Thieme, New York 1999, Chapter 12, p 91-108.

(14-) Wanifuchi W, Shimizu T, Higa T, Nakaya K. Kissing mirror image anterior communicating artery aneurysms. Case report. Neurol Med Chir (Tokyo) 2001; 41: 1,29-32.

(15-) Yasargil MG, Fox JL, Ray MW. The operative approach to aneurysms of the anterior communicating artery. In: Advances and technical standards in Neurosurgery. Krayenbfhl(ed), Springer Verlag Wien, 1975, vol 2, p 113-170.

PAULO HENRIQUE PIRES AGUIAR, MARCOS VINICIUS MALDAUN, ALEXANDROS PANAGOPOULOS, ADRIANA TAHARA, LUCAS SUGUIKAWA, DENISE NAKANISHI, RENATA SIMM, LAURO MARUBAYASHI

* Clinica de Neurologia e Neurocirurgia Pinheiros, SP, Brazil Hospital São Camilo, Hospital Santa Paula, SP, Brazil

Corresponding author:

Adriana Tahara

Av. Henrique Broseghini, 243

Osasco, SP, Brazil

Postal code 06030-340

Phone number 55 14 81113178

Table 1--Characteristics of 3 patients with multiple ACOA aneurysms
and 1 patient with a multi-lobular aneurysm.

Case    Age         Sex           Fisher    Hunt     Number
                                  Grade     Hess     of
                                            Grade    aneurysms

1       55          F             IV        II       2
2       55          F             I         I        3
3       72          F             0         0        2
4       57          F             IV        III      1 *

Case    Size of     Size of       GOS       Type
        ruptured    unruptured
        aneurysm    aneurysm
        [mm]        [mm]

1       22          4             G         C
2       10          10 and 4      G         C
3       11          10            G         C
4       18                        P         NA

GOS--Glasgow Outcome Scale

P--Poor

G--Good

F--Female

NA--not applicable

*--multi-lobular

Source Citation

Source Citation   

Gale Document Number: GALE|A186862464