Detailed description of the anterior cerebral artery anomalies observed in a cadaver population

Accepted Manuscript Title: Detailed Description of the Anterior Cerebral Artery Anomalies Observed in a Cadaver Population Author: K. Cilliers B.J. Page PII: DOI: Reference:

S0940-9602(16)30096-6 http://dx.doi.org/doi:10.1016/j.aanat.2016.04.036 AANAT 51049

To appear in: Received date: Revised date: Accepted date:

25-3-2016 22-4-2016 23-4-2016

Please cite this article as: Cilliers, K., Page, B.J.,Detailed Description of the Anterior Cerebral Artery Anomalies Observed in a Cadaver Population, Annals of Anatomy (2016), http://dx.doi.org/10.1016/j.aanat.2016.04.036 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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K. Cilliers (1), BJ. Page (1) (1) Anatomy and Histology, Faculty of Medicine and Health Sciences, Stellenbosch University, Cape Town, Western Cape, South Africa

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Title: Detailed Description of the Anterior Cerebral Artery Anomalies Observed in a Cadaver Population ABSTRACT Anomalies of the anterior cerebral artery (ACA) include the median ACA (MedACA), bihemispheric

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ACA (BihemACA) and the azygos ACA. Knowledge of these anomalies can be crucial to clinicians and neurosurgeons, especially during surgeries involving the interhemispheric region and in the

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interpretation of the clinical signs of a stroke. Since few reports exist on the origin, area supplied, diameter and length of the ACA anomalies, the aim of this study is to give a detailed description on the

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anatomy of the ACA anomalies.

The ACAs of 60 brains were injected with a colored silicone. When an anomaly was observed,

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a detailed illustration of the course and pattern of the ACA and cortical branches were made. The origins and the areas supplied by the anomalous arteries were noted. The external diameter was measured using a digital micrometer and the length was measured using string and a ruler.

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There were seven cases (11.7%) of a MedACA and 12 cases (20.0%) of a BihemACA. The MedACA originated mostly from the anterior communicating artery, and from the A2 segment in one

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case. The MedACA was bilateral in four cases and unilateral in three cases. Excluding Case 5 and 9,

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the BihemACA cases can be divided into two groups; one branch to the left hemisphere (n=3), and one branch to the right hemisphere (n=7). The average diameter of both the BihemACA and MedACA was

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1.8 mm.

Studies rarely provide additional information on these anomalies. Therefore, the present study elaborated on the origin, diameter, length and the area supplied by these anomalies. The definitions are described in the literature, although additional criteria were still lacking and this was provided in the present study. Since information on these aspects of the ACA anomalies is scarce, future research should give detailed descriptions on the ACA anomalies. Keywords: Anomaly; bihemispheric anterior cerebral artery; median anterior cerebral artery; origin. Abbreviations: (ACA) Anterior cerebral artery; (AcoA) Anterior communicating artery; (AIFA) Anterior internal frontal artery; (BihemACA) Bihemispheric anterior cerebral artery; (IIPA) Inferior internal parietal artery; (MedACA) Median anterior cerebral artery; (MIFA) Middle internal frontal artery; (PIFA) Posterior

internal

frontal

artery;

and

(PLA)

Paracentral

lobule

artery. Page 2 of 29

2 1.

INTRODUCTION

Anomalies of the anterior cerebral artery (ACA) that are occasionally observed can be divided into three main groups. These anomalies include a median ACA (MedACA), bihemispheric ACA (BihemACA) and an azygos ACA (Jinkins, 2000). These anomalies are often mentioned in the

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literature, although very few studies give more information on the origin, area supplied, diameter and

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length. The definitions and criteria of these anomalies can be very similar and even overlap.

When the right and left A2 segments fuse, a single A2 segment is formed which is referred to as an

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azygos ACA (Critchley, 1930; Ozaki et al., 1977; Katz et al., 1978; Perlmutter and Rhoton, 1978; Krayenbuhl et al., 1982; Lemos, 1984; Milenković et al., 1985; Gomes et al., 1986; Cinnamon et al.,

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1992; Hashizume et al., 1992; Baykal et al., 1996; Ladziński et al., 1997; Jinkins, 2000). Descriptions of the azygos ACA in the literature are very rare, although it has been observed in several studies

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(Table 1).

When one of the A2 segments is hypoplastic or terminates early, the contralateral ACA can divide and

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supply both hemispheres. This is referred to as a bihemispheric ACA (Ring and Waddington, 1968;

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Perlmutter and Rhoton, 1978; Okahara et al., 2002; Rhoton, 2002). Descriptions of the BihemACA are

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particularly rare, although it has been observed in selected studies (Table 1). A third ACA branch can be observed supplying the medial surface of either one or both hemispheres. This is referred to as a median ACA. (Baptista, 1963; Krayenbuhl et al., 1982; Stefani et al., 2000. The third branch can originate from the anterior communicating artery (AcoA), as well as from the A1 or A2 segments (Fawcett and Blachford, 1905; Critchley, 1930; Tulleken, 1978; Okahara et al., 2002; Rhoton, 2002; Hussain et al., 2005; Kahilogullari et al., 2008; Kapoor et al., 2008; Pekcevik et al., 2012; Makowicz et al., 2013). The MedACA is rarely described in the literature, although it has been observed in numerous studies (Table 3). The prevalence of the azygos, bihemispheric and median anterior cerebral arteries is shown in Table 1. Table 1 The knowledge of these anomalies can be crucial to clinicians and neurosurgeons, especially during surgeries involving the interhemispheric region and in the interpretation of the clinical signs of a stroke Page 3 of 29

3 (Gunnal et al., 2013). These anomalies may be associated with aneurysm formation and, occlusion of certain anomalies can lead to cerebral ischemia in both hemispheres (Kovač et al., 2014). Since few reports exist on the origin, area supplied, diameter and length of the ACA anomalies, the aim of this study is to give a detailed description on the anatomy of the ACA anomalies as observed in a cadaveric

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population.

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4 2.

METHODOLOGY

Sixty-three brains (126 hemispheres), obtained from the Department of Anatomy and Histology, were examined and five hemispheres were excluded due to failure of perfusion, or damage to the hemisphere. Since these anomalies affect both hemispheres, three brains were excluded. Consequently,

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60 brains were used for this study. The anterior cerebral artery was injected with a colored silicone (MM922 Silicone, ACC Silicone Concepts). The course of the ACA and its cortical branches were

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followed and dissected. If an azygos, BihemACA or a MedACA were observed, a detailed illustration of the course and pattern of the ACA and cortical branches was made. The origins and the areas

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supplied by the anomalous arteries were noted. The external diameter was measured using a digital micrometer and the length was measured using string and a ruler. Ethical clearance was obtained from

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the Health Research Ethics Committee (HREC).

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5 3.

RESULTS

In the 60 brains examined, the azygos ACA was not observed. A MedACA (Fig. 1 and Fig. 2) was observed in seven cases (11.7%) and a bihemispheric ACA (Fig. 3 and Fig. 4) in 12 cases (20.0%). Median anterior cerebral artery

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3.1.

A median ACA was observed in seven cases and a line diagram of each case is given in Figure 1. The

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area supplied by the MedACA is indicated in green. The MedACA originated from the AcoA in six

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cases (85.7%) and from the A2 segment in one case (14.3%). Figure 1

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Figure 2

The median ACA supplied only one hemisphere in three cases (unilateral MedACA) and both

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hemispheres in four cases (bilateral MedACA). The superior internal parietal artery (SIPA), paracentral lobule artery (PLA) and inferior internal parietal artery (IIPA) were the only cortical

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branches originating from the MedACA. When the SIPA was present it always originated from the

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MedACA. In the bilateral MedACAs, the SIPA also supplied both hemispheres. The paracentral lobule

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artery was originated from the MedACA in six cases and the IIPA in three cases. 3.1.1. Unilateral median anterior cerebral artery In Case 1 (Fig. 1), the MedACA originated from the left A2 segment (proximal to the origin of the first cortical branch), and only gave rise to cortical branches on the right (SIPA and paracentral lobule artery). The second and third cases both arose from the AcoA, giving rise to only the SIPA in the second case, and the parietal arteries in the third case. 3.1.2. Bilateral median anterior cerebral artery The MedACA gave rise to the same cortical branches bilaterally in Case 4 and 6. The SIPA and paracentral lobule artery were supplied on both sides in Case 4, and the SIPA was supplied on both sides in Case 6. In Case 5 two cortical arteries were supplied on the left and three on the right. In the last case (Case 7), the MedACA gave rise to the SIPA and paracentral lobule artery on the left and the parietal arteries on the right.

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6 3.2.

Bihemispheric anterior cerebral artery

A bihemispheric ACA was observed in 12 cases and a line diagram of each case is given in Figure 3. The arteries arising from the bihemispheric branch are indicated in red on the figure. The most common origin of these bihemispheric branches included origin between two paracentral lobule arteries (three cases), between a PLA and the posterior internal frontal artery (PIFA) (three cases) and

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between the anterior (AIFA) and middle internal frontal arteries (MIFA) (three cases). The most frequent arteries arising from a bihemispheric branch were the SIPA in 11 cases, and the IIPA and

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paracentral lobule artery in eight cases each.

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Figure 3

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Excluding Case 5 and Case 9, the remaining 10 cases can be divided into two subgroups depending on the hemisphere supplied. Three cases supplied the left hemisphere (with two or three branches), and seven cases supplied the right hemisphere (with one to five branches). In all 10 cases, there was only

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one bihemispheric branch. The bihemispheric branch in Case 5 supplied both hemispheres and in Case

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9 there were two branches supplying the left hemisphere.

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An anastomosis was observed between the bihemispheric branch in Case 7 and the left SIPA. The diameter and length of the anastomosis was 0.9 mm and 2.0 mm, respectively. There was only one

Figure 4

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case (Case 8) where the bihemispheric branch only gave rise to one cortical branch.

The cortical branches originating from the BihemACA and MedACA as well as the diameter and length of these anomalies are shown in Table 2. The diameters were measured at the origin of the ACA anomaly and Length 1 refers to the distance between the origin (of the ACA anomaly) and the AcoA. The MedACA originated from the AcoA in six cases; therefore the only measurement for Length 1 was when the MedACA arose from the A2 segment (Case 1). For the BihemACA, Length 2 refers to the length of the crossing branch, and for the MedACA it refers to the length before the division into cortical branches. These measurements are illustrated in Figure 5. Figure 5 Table 2 Page 7 of 29

7 Both the BihemACA and MedACA had an average diameter of 1.8 mm (SD 0.4 and 0.3, respectively). Branches supplying the right side were larger (2.0 mm ± 0.3) compared to branches supplying the left (1.5 mm ± 0.4). The average diameter of both the unilateral and the bilateral MedACA was 1.8 mm (SD 0.2 and 0.5, respectively). The average distance of Length 1 (BihemACA) was 43.8 mm on the

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right, and 56.0 mm on the left. The average Length 2 of the MedACA was 88.4 mm (excluding Case

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2), and the average Length 2 of the BihemACA was 21.2 mm (excluding Case 5 and 8).

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8 4.

DISCUSSION

This study presents descriptions of ACA anomalies observed in 60 brains. The azygos ACA was not observed in this study and this supports the notion of scarcity (Huber et al., 1980; Sanders et al., 1993; Bharatha et al., 2008). Selected studies have confused the azygos ACA with the MedACA (Kapoor et

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al., 2008; Gunnal et al., 2013). This can be due to the fact that both the azygos ACA and MedACA can develop due to persistence of the median artery of the corpus callosum. Therefore, if the results of

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different studies are compared, the definitions of the anomalies should be noted.

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Seven cases (11.7%) of the MedACA were observed. This is in accordance with the range indicated in the literature (Table 1, 0.9%-33.3%). In six of the seven cases, the MedACA originated from the AcoA

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which is consistent with reports by previous authors (Fawcett and Blachford, 1905; Critchley, 1930; Tulleken, 1978; Okahara et al., 2002; Rhoton, 2002; Hussain et al., 2005; Kahilogullari et al., 2008; Kapoor et al., 2008; Pekcevik et al., 2012; Makowicz et al., 2013). Few studies comment on the

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regions that are supplied by the MedACA, although comments have been made on whether one or both hemispheres are supplied (Baptista, 1963). The MedACA supplied only one hemisphere in three cases;

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therefore, the MedACA is not always bilateral. Baptista (1963) observed the unilateral MedACA in 27

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cases, and the bilateral MedACA in 23 cases (in a sample size of 381). The region most commonly supplied by the MedACA was the precuneus (area supplied by the SIPA). The average diameter of the

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MedACA was 1.8 mm (± 0.3), which is larger compared to previous reports (0.9 mm (Türe et al., 1996) and 1.28 mm (Kahilogullari et al., 2008)). There were 12 cases (20.0%) of the BihemACA. This is in accordance with the range indicated in the literature (Table 1, 0.9%-64.0%). Unfortunately, studies rarely elaborate on the origin of these bihemispheric branches. In the present study, these branches most commonly originated between two paracentral lobule arteries, between a PLA and the PIFA, and between the AIFA and middle internal frontal artery. Few studies comment on the regions that are supplied by the BihemACA, although comments have been made on which hemisphere is supplied. Bihemispheric branches supplied the right hemisphere in seven cases, and the reverse in five cases. Baptista (1963) observed branches supplying the right hemisphere in 25 cases, and the reverse in 20 cases (in a sample size of 381). The region most commonly supplied by the BihemACA in the present study was the precuneus (area supplied by the SIPA). There have been no reports on the length of the branches crossing from one hemisphere to the other. Therefore the distance from the AcoA to the origin of the branch (Length 1), Page 9 of 29

9 and the distance before division (Length 2) were measured. This information can be useful during interhemispheric surgery. The definitions of the BihemACA and MedACA can overlap. The definition for the BihemACA is the presence of a branch supplying the contralateral hemisphere, while the ipsilateral ACA terminates

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early or is hypoplastic (Ring and Waddington, 1968; Perlmutter and Rhoton, 1978; Okahara et al., 2002; Rhoton, 2002; Parmar et al., 2005; Lehecka et al., 2008; Dimmick and Faulder, 2009; Bradac,

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2011; Hamidi et al., 2013). The definition for the MedACA is the presence of an additional branch, while the right and left ACA are still present and not hypoplastic (Baptista, 1963; Krayenbuhl et al.,

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1982; Stefani et al., 2000; Parmar et al., 2005; Kapoor et al., 2008; Dimmick and Faulder, 2009; Niederberger et al., 2010; Pekcevik et al., 2012). Additional criteria are needed for these ACA

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anomalies. In the case of the BihemACA, the hemisphere receiving the bihemispheric branch, has been described as being hypoplastic or terminating early. This was not always the case in the present study. The ACA could terminate at the level of the SIPA (two cases), PLA (five cases), PIFA (one case),

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MIFA (three cases) or the AIFA (one case). Therefore the ACA is not always hypoplastic or terminates early, since it could extend to the internal parietal arteries. This indicates that the BihemACA

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definition is not necessarily precise and extended criteria are needed. The following criteria are suggested and illustrated in Figure 6. Firstly, if the atypical artery originates

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proximal to the first cortical artery, it should be considered a MedACA (which can supply only one cortical artery, or several on one or both hemispheres). Secondly, if the atypical cortical artery originates distal to the first cortical artery and supplies the contralateral hemisphere, it should be considered a BihemACA. Lastly, if the atypical artery originates distal to the first cortical artery and supplies the ipsilateral hemisphere, it should be considered a cortical artery with an unusual origin. Figure 6

These extended criteria can be illustrated by comparing Case 2, Case 7 and Case 8 (Fig. 6). In Case 2, the atypical artery originates proximal to the first cortical artery. Thus, the atypical branch was termed a MedACA. In case 7, the atypical artery originates distal to the first cortical branch, and supplies the ipsilateral hemisphere. Therefore, the atypical branch was termed an unusual cortical artery. In Case 8, the atypical artery originates distal to the first cortical branch and supplies the contralateral

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10 hemisphere. Therefore, the atypical branch was termed a BihemACA. A BihemACA and a MedACA can be observed in the same specimen, although this was not observed in the present study. Case 1 (MedACA) (Fig. 1) was also similar to Case 11 (BihemACA) (Fig. 3). In Case 1, the atypical artery originates proximal to the first cortical artery. Therefore, the atypical branch was termed a

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MedACA. In Case 11, the atypical artery originates distal to the first cortical branch and supplies the

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contralateral hemisphere. Therefore, the atypical branch was termed a BihemACA.

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11 5.

CONCLUSION

Information on the anatomy of the anterior cerebral arteries and its anomalies is necessary in certain vascular procedures (aneurysm and arteriovenous malformation surgery) (Kahilogullari et al., 2012) as well as for the interpretation of clinical signs of a stroke (Umansky et al., 1984; Kakou et al., 2000).

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Studies usually only mention the ACA anomalies and do not provide additional information on these anomalous branches. Therefore, the present study provides additional information on the origin,

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diameter, length and the area supplied by these anomalous arteries. The definitions for these ACA anomalies are described in the literature, although additional criteria were still lacking and this has

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been provided in the present study. Since information on these aspects of the ACA anomalies is scarce,

6.

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future research should give detailed descriptions on the ACA anomalies. ACKNOWLEDGEMENTS

The author’s would like to thank the Harry Crossley Foundation for financial support, and Mr RP

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Williams and Ms Jacklynn Walters for technical assistance with perfusion.

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16 Ozaki, T., Handa, H., Tomimoto, K., Hazama, F., 1977. Anatomical variations of the arterial system of the base of the brain. Archiv für Japanische Chirurgie. 46, 3-17. Parmar, H., Sitoh, Y.Y., Hui, F., 2005. Normal variants of the intracranial circulation demonstrated by MR angiography at 3T. European Journal of Radiology. 56(2), 220-228. Paul, S., Mishra, S., 2004. Variations of the anterior cerebral artery in human cadavers: a dissection

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18 Zurada, A., Gielecki, J., Tubbs, R.S., Loukas, M., Cohen-Gadol, A.A., Chlebiej, M., Maksymowicz, W., Nowak, D., Zawiliński, J., Michalak, M., 2010. Three-dimensional morphometry of the A2 segment of the anterior cerebral artery with neurosurgical relevance.

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Clinical Anatomy. 23(7), 759-769.

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19 Figures: Figure 1: Illustrations of the seven median anterior cerebral arteries observed in the present study. Figure 2: The origin and course of a median anterior cerebral artery.

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Green indicates the area supplied by the anomalous branch.

study. Red indicates the area supplied by the anomalous branch.

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Figure 3: Illustrations of the twelve bihemispheric anterior cerebral arteries observed in the present Figure 4: The origin and course of a bihemispheric anterior cerebral artery. A) Left hemisphere

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receiving branch from the right; B) Bihemispheric branch from the right to the left hemisphere; and C) Superior view.

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Figure 5: Measuring the length of the bihemispheric and median anterior cerebral arteries. Figure 6: Clarification on the criteria of the median anterior cerebral artery, unusual origin of a cortical

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artery, and the bihemispheric anterior cerebral artery.

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Tables:

Table 1: The prevalence of the azygos, bihemispheric, and median anterior cerebral arteries.

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Table 2: The diameter (mm), length (mm) and cortical arteries originating from the bihemispheric and median anterior cerebral artery.

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20 Table 1: The prevalence of the azygos, bihemispheric, and median anterior cerebral arteries.

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Cases 9 23 50 26 21 8 13 10 1 2 27 5 9 2 3 1 1 1 27 10 23 4 3 3 1 5 1 5 1 1 10 -

MedACA % 4.5% 3.3% 13.1% 8.7% 14.2% 10.7% 4.4% 22.7% 3.3% 9.1% 13.1% 3.7% 9.0% 6.7% 7.9% 4.0% 1.0% 2.2% 3.0% 33.3% 2.3% 4.0% 2.6% 6.0% 1.4% 12.8% 0.9% 1.0% 6.7% 3.3% 2.2% -

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BihemACA Cases % 45 11.8% 2 8.0% 16 64.0% 2 8.0% 1 2.0% 1 5.0% 15 14.9% 4 5.6% 7 6.3% 9 1.8% 1 6.7% 2 6.7% 4 0.9% -

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200 700 381 300 414 107 291 25 20 146 25 75 7782 296 44 30 22 206 134 25 5190 100 30 38 25 100 50 20 45 891 50 504 30 1000 101 72 115 50 70 39 112 500 15 30 455 3572

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Windle (1888) Fawcett and Blachford (1905) Baptista (1963) Jain (1964) Fisher (1965) Lemay and Gooding (1966) Wollschlaeger et al. (1967) Ring and Waddington (1968) Dunker and Harris (1976) Ozaki et al. (1977) Perlmutter and Rhoton (1978) Tulleken (1978) Huber et al. (1980) Kwak et al. (1980) Kayembe et al. (1984) Gomes et al. (1986) Marinković et al. (1990) Ogawa et al. (1990) Nathal et al. (1992) van der Zwan et al. (1992) Sanders et al. (1993) Macchi et al. (1996) Serizawa et al. (1997) Stefani et al. (2000) Avci et al. (2001) Kulenović et al. (2003) Paul and Mishra (2004) Ugur et al. (2005) Tao et al. (2006) Uchino et al. (2006) Ugur et al. (2006) Bharatha et al. (2008) Kahilogullari et al. (2008) Kapoor et al. (2008) Lehecka et al. (2008) Saidi et al. (2008) Nowinski et al. (2009) Zurada et al. (2010) Nordon and Rodrigues (2012) Swetha (2012) Cilliers et al. (2013) Gunnal et al. (2013) Hamidi et al. (2013) Kedia et al. (2013) Stefani et al. (2013) Kovač et al. (2014) Wan-Yin et al. (2014)

Azygos ACA Cases % 6 3.0% 1 0.3% 7 1.7% 4 3.7% 3 1.0% 2 10.0% 1 1.3% 17 0.2% 1 3.3% 2 0.04% 2 2.0% 1 3.3% 1 2.6% 1 4.0% 1 5.0% 18 2.0% 2 4.0% 1 0.2% 9 0.9% 4 4.0% 3.7% 2 1.7% 5 4.4% 9 1.8% 7 1.5% 14 0.4%

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Total

(ACA) Anterior cerebral artery; (BihemACA) Bihemispheric anterior cerebral artery; and (MedACA) Median anterior cerebral artery.

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21 Table 2: The diameter (mm), length (mm) and cortical arteries originating from the bihemispheric and median anterior cerebral artery.

BihemACA 1.8

57.0

41.5

Right side SIPA, IIPA

BihemACA 2.1

36.0

13.0

-

BihemACA 1.8

32.5

8.0

PIFA, PLA, SIPA

BihemACA 1.8

42.7

25.0

PLA, SIPA

BihemACA 2.4

36.7

5.7

IIPA

36.7

18.7

-

BihemACA 2.2

40.0

33.0

BihemACA 1.9

64.7

19.0

BihemACA 1.7

62.2

-

BihemACA 1.1 1.4 BihemACA 1.2

Case 10 Case 11 Case 12 Case 1 Case 2 Case 3 Case 4 Case 5

63.0 69.0 66.4

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Branch 1: Branch 2:

Left side PLA, PLA, SIPA -

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PIFA, PLA, SIPA, IIPA -

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Case 6 Case 7 Case 8 Case 9

Cortical Arteries

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Diameter Length Length 2 1

-

MIFA, PIFA, PLA, SIPA SIPA, IIPA

IIPA

-

13.0 22.5

-

PLA SIPA, IIPA SIPA, IIPA -

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Case 1 Case 2 Case 3 Case 4 Case 5

Variation

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Case

BihemACA 2.0

26.0

17.5

BihemACA 2.4

53.2

19.0

MIFA, PIFA, PLA, SIPA, IIPA PLA, SIPA

MedACA

2.0

7.5

60.0

PLA, SIPA

-

MedACA

1.8

-

-

-

SIPA

MedACA

1.7

-

95.0

SIPA, IIPA

-

MedACA

1.7

-

Right: 100.7 Left: 102.7 Right: 75.7 Left: 71.5

PLA, PLA

-

-

PLA, PLA

IIPA, PLA, SIPA

-

-

PLA, SIPA

MedACA

2.4

-

-

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22 Case 6 Case 7

MedACA

1.3

-

MedACA

1.9

-

72.5

SIPA

SIPA

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Right: SIPA, IIPA 111.7 Left: PLA, SIPA 105.9 (BihemACA) Bihemispheric anterior cerebral artery; (IIPA) Inferior internal parietal artery; (MedACA) Median anterior cerebral artery; (MIFA) Middle internal frontal artery; (PIFA) Posterior internal frontal artery; (PLA) Paracentral lobule artery; and (SIPA) Superior internal parietal artery.

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Figure 1

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Figure 2

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Figure 3

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Figure 4

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Figure 5

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Figure 6

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