ANATOMICAL CONSIDERATION OF THE INTRACRANIAL PORTION OF MIDDLE MENIGEAL ARTERY IN THAIS

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1 ANATOMICAL CONSIDERATION OF THE INTRACRANIAL PORTION OF MIDDLE MENIGEAL ARTERY IN THAIS Kritsana Namonta, 1 Lanaprai Kwathai, 1 Thanaporn Rungruang, 1 Vipavadee Chaisuksunt, 2 Wandee Apinhasmit, 3 Supin Chompoopong, 1, * 1 Department of Anatomy, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok 10700, Thailand 2 Department of Anatomy, Faculty of Medicine, Chiang Mai University, Chiang Mai 50200, Thailand 3 Department of Anatomy, Faculty of Dentistry, Chulalongkorn University, Bangkok 10330, Thailand * siscm@mahidol.ac.th Abstract: The knowledge of variations of the origin, course and branching pattern of the middle meningeal artery (MMA) is of great importance in surgery and radiological examinations. Therefore, the present study was aimed to determine the course of the MMA and confined mainly to its intracranial portion as follows: 1) type of branching, 2) point of division of the main trunk and 3) length and diameters of the starting and ending of main trunk.the investigations made consisted of the examination of the course of the MMA on both sides of 103 Thai dry skulls (66 males and 37 females) and 26 dissections upon the cadaveric skulls (14 males and 12 females) with known sex and age. The type of branching and point of division of the MMA were classified into 5 types. The length was measured from its appearing at the FS to the point of division to anterior and posterior branches. Two diameters of the main trunk were measured; D1 at the starting stem of the MMA from the FS and D2 at the point of division of the MMA. The branching of MMA, in cadaveric skulls was mostly found as type D, the anterior and middle branches branching from the same stem at the pterion region (28.80%). In dry skulls, it was mostly found as type E, the anterior and middle branches branching from the same stem at the pterion region and the middle and posterior branches branching from the same stem at temporal bone or parietal bone region (30.36%). The length of the main trunk of the MMA was longer in males (18.41±8.29 mm) than females (10.07±2.86 mm) significantly at P < There was no significant difference of the length between side and age groups. The average diameter only at the ending of main trunk (D2) between age groups, years and more than 59 years, were 2.04±0.23 mm and 2.34±0.30 mm, respectively, it was significant difference at P < The information on the anatomical variations in the type of branching, the length and diameters of the intracranial portion of MMA is of surgical importance and is also needed to support useful hypotheses in bypass procedures to manage skull base vascular lesions. Introduction: The middle meningeal artery (MMA) is the branch supplying the dura mater covering the parietal, temporal and part of the frontal meningeal regions. Its usual course arises from the maxillary artery, branch of the external carotid artery and enters the middle cranial fossa through the foramen spinosum (FS). Generally, the intracranial portion of MMA divides into two main branches, the anterior and posterior branches after pass through the FS, some classifications consider the third branch or middle branch which may originate from the anterior or posterior branches. The anterior and posterior branches starts from the FS and passes into the meningeal layers and divides in two principal branches and further to be minor vessels which form a complex vascular network between the brain surface and endocranial wall. 1 Several anatomical studies suggest that the MMA shows a high anatomical variability both origin and branching patterns. 2-6 The knowledge of its variations is of great 37 th Congress on Science and Technology of Thailand 1

2 importance in surgery and radiological examinations. But no such study in Thais has been reported. Therefore, the present study was aimed to determine the course of the MMA and confined mainly to its intracranial portion as follows: 1) type of branching, 2) point of division of the main trunk and 3) length and diameters (start and end) of main trunk. Methology: The examination of the course of the MMA was performed on both sides of 103 Thai dry skulls and of 26 cadaveric skulls dissected obtained from Department of Anatomy, Faculty of Medicine Siriraj Hospital, Mahidol University. All skulls were from adults with known sex and age. An approval of the study protocol was exempted from the Ethics Committee, the Siriraj Institutional Review Board (SIRB), Mahidol University, Thailand, Protocol No.: 657/2553. The types of the intracranial portion branches of MMA were determined in all skulls according to some modifications of Adachi and Giuffrida-Ruggeri's classifications. 7 The MMA branching types were identified by considering the location on the bone of the point of division and the common stem of the anterior and middle branches or of the posterior and middle branches (Table 1). Based on these criteria, a total of 5 types of MMA branching was classified. The point of division of the MMA was also determined according to Plummer (1896) 8 as follows: 1) the temporal bone or 2) the greater wing of sphenoid bone or pterion region, Table 1. Classification of the branching types of the MMA identified by the location of the point of division and the origin of the middle branch. Point of division Pterion Temporal bone Type A / / Type B / / Type C / / Type D / / Type E / / / Origin of middle branch From anterior From posterior branch branch The length and diameters of the main trunk of the MMA were measured using Image Tool 3.0 Program (UTHSCSA, The University of Texas Health Science Center in San Antonio, USA). The length of the main trunk was measured from the point of its emerging from the FS to the point of division to anterior and posterior branches (Fig. 1A). Two diameters of the main trunk were measured; D1, at the initial part of the stem of the MMA coming out from the FS, and D2, at the point of division of the MMA (Fig. 1B). Statistical Package for the Social Science (version 16) software (SPSS; Chicago, IL, USA) was used for the analysis. A comparison of values between groups was made using the unpaired t-test. The level of significant difference was P-value < Results, Discussion and Conclusion: In this study, 103 Thai dry skulls (66 males and 37 females) and 26 dissections upon the cadaveric skulls (14 males and 12 females) were studied. An average age of analyzed dry skulls was 65.07±17.05 years (range years) and of the cadaveric skulls was ± years (range years). All 5 types of the intracranial branching of MMA were identified as follows: Type A: the anterior and middle branches arising from a common stem at the pterion region, 2) Type B: the middle and the posterior branches branching from a common stem at the pterion region, 3)Type C: the posterior and middle branches branching from a common stem at the temporal bone region, 4) Type D: the anterior and middle branches branching from a common stem at the pterion region and 5) Type E: the anterior and middle branches branching from a stem at the pterion 37 th Congress on Science and Technology of Thailand 2

3 region and the middle and posterior branches branching from the other stem at temporal bone or parietal bone region (Table 1). The points of division of type A and B found in this study are at the pterion region but type C, D and E are at the temporal bone (Table 1). As shown in Table 2, the type of the MMA branches in cadaveric skulls was mostly type D (28.80% in 52 sides) whereas in dry skulls, it was mostly type E, (30.36% in 206 sides). Table 2. The percentage of the branching types of the MMA in cadaveric and dry skulls. Type Cadaveric skulls Dry skulls N (sides) % N (sides) % Type A % % Type B % % Type C % % Type D % % Type E % % Total % % Figure 1. The MMA and its branches in the right middle cranial fossa of a cadaveric skull. The two-head arrows demonstrate the sites for the measurements of length (A) and diameters D1 and D2 (B) at the main trunk. Ant. br, anterior branch; Post. br, posterior branch; MMA, middle meningeal artery; CN.V, trigeminal nerve; CN.II, optic nerve; CN.VI, abducens nerve; F. magnum, foramen magnum. Table 3. The length and diameters (D1 and D2) of the main trunk of the intracranial portion of the MMA. Group Diameter (mm) Length (mm) N (sides) D1 D2 Average Male (26) 18.41±8.29* ( ) 2.62±0.37 ( ) 2.33±0.36 ( ) 2.48±0.39 ( ) Female (18) 10.07±2.86* ( ) 2.37±0.27 ( ) 2.16±0.20 ( ) 2.26±0.25 ( ) Right (24) 13.27±7.84 ( ) 2.59±0.29 ( ) 2.33±0.28 ( ) 2.60±0.29 ( ) Left (20) 17.20±7.59 ( ) 2.42±0.64 ( ) 2.72±0.35 ( ) 2.42±0.40 ( ) years(12) 13.04± ± ±0.23* 2.18±0.32 ( ) ( ) >59 years(32) 15.89± ±0.33 ( ) ( ) The values were expressed as mean ± SD (range). *Significant difference at P value<0.05 ( ) 2.34±0.30* ( ) ( ) 2.46±0.34 ( ) 37 th Congress on Science and Technology of Thailand 3

4 The results of the measurements of the length and diameters, D1 and D2, of the main trunk of the intracranial portion of MMA were shown in Table 3. The length of the main trunk of the MMA was longer in males (18.41 ± 8.29 mm) than in females (10.07 ± 2.86 mm) significantly at P < There was no significant difference in the length between side and age groups. The diameters of D1 and D2 were 2.62 ± 0.37 mm and 2.33 ± 0.36 mm respectively in male and were 2.37 ± 0.27 mm and 2.16 ± 0.20 mm respectively in female. However, there was no significant difference either in the diameters of D1 and D2 or in the average mean of both diameters between sex and sides. Interestingly, even though there were insignificant differences in D1 and the average mean of D1 and D2 between two age groups (29-59 years and over 59 years), the mean diameter of D2 of the old age group was significantly greater than that found in the young group (P < 0.05). Generally, the branches of the MMA and vein accompany one another, the vein lying external to the artery. Therefore, the grooves on the skull are made by the veins but indicate the position of both vein and artery and can be used to study the course of MMA. 1 Previous studies have dealt with either bony or cadaver specimens, whereas this study is carried out on both Thai cadaveric skulls and dry skulls for considering the type of branching of MMA.(Figure 2) Figure 2. The intracranial surface of a dry skull showing the imprints of the MMA and its branches on each sides of the middle cranial fossa (A). The area of the right middle cranial fossa in the rectangle frame in A was enlarged in B showing a clearer view of the groove for the MMA starting at the FS, and then dividing into the anterior branch and the common stem of the posterior and middle branches. The MMA branching pattern seen in B was identified as type C. The white labels: A, anterior branch; M, middle branch; P, posterior branch; FS, foramen spinosum,; FO, foramen ovale; MMA, middle meningeal artery. The black labels: F, frontal bone; O, occipital bone; P, parietal bone; S, greater wing of sphenoid bone; T, temporal bone. The anterior branch of MMA is clinically important because it is overlaid with the pterion and lies close to the motor area of the cerebral cortex of the brain. 9 Many previous studies have been reported concerning the clinical correlation of the MMA The torn MMA in temporal bone fracture or trauma usually presents with extradural hemorrhage 11. The similar injury in skull fracture that needs operation is the lesions associate with lesions of MMA such as the aneurysm of the MMA and the rupture of entire vessel wall layer of the MMA which can cause intracerebral hemorrhage 11, 12. Therefore, the consideration of type of branching could help surgeon to gain a practical understanding of the surgical relationship of clinical structure such as the MMA in these cases. Otherwise, the lesions about cerebral revascularization 13 and high cervical vascular lesion could be treated with the bypass procedures using the MMA as the graft or donor. 14 Ustun et al reported the simpler bypass procedure between the MMA and P2 segment of the posterior cerebral artery for the correction of vertebrobasilar insufficiency. In their study, the length and diameter of the main 37 th Congress on Science and Technology of Thailand 4

5 trunk of MMA, 39.5±4.4 mm and 2.1±0.25 mm, respectively were suitable to provide sufficient blood flow. 15 In this study, the length of the main trunk of MMA were shorter because the type of branching of MMA mostly found as type D and E (Table 2). In both types, the point of division was on the temporal bone not the pterion region which was shorter and not suitable as the graft or donor for bypass procedure as previous report. 14 Previous study also reported that the diameter of the main trunk of MMA at the point of division was 2.33±0.36 mm in males and 2.16±0.20 mm in females. Furthermore, the mean diameter of MMA in Thais was more than 2 mm. Therefore, it was suitable to provide sufficient blood flow if its length was long enough or the point of division was on the pterion. 14 In conclusion, the information on the anatomical variations in the type of branching of the MMA is of surgical importance such as concerning extradural hemorrhage. The length and diameters of the intracranial portion of MMA is also needed to support useful hypotheses in bypass procedures to manage skull base vascular lesions such as the MMA-to-branches of internal carotid artery bypass. References: 1. Snell, R.S. Clinical anatomy by Regions 8 th Edn.2008, Lippincott Williams & Wilkins, Philadelphia, pp. 673, 683 and Chandler, S.B., Derezinski, C.F. Anatomical Record. 1935, 62 (3), Royle, G., Motson, R. J Neurol Neurosurg Psychiatry. 1973, 36 (5), Manjunath, K.Y. J Anat Soc India. 2001,50 (2), Kawai, K., Yoshinaga, K., Koizumi, M., Honma, S., Tokiyoshi, A., Kodama, K. Ann Anat. 2006, 188 (1), Yoshioka, N., Rhoton, A.L., Jr., Abe, H. Neurosurgery. 2006, 58 (1 Suppl):ONS123-6; discussion ONS Rothman, D. Am. J. Phys. Anthropol. 1937, 22, Plummer, S.C. Ann Surg. 1896, 23 (5), Apinhasmit, W., Chompoopong, S., Chaisuksunt, V., Thiraphatthanavong, P., Phasukdee, N. J Med Assoc Thai. 2011, 94 (2), Cengiz, S.L., Ozturk, K., Cicekcibasi, A.E., Salbacak, A., Ustun, M.E. Neurosurg Rev. 2008, 31 (3), Paiva, W.S., de Andrade, A.F., Amorim, R.L., Figueiredo, E.G., Teixeira, M.J. Case Report, 2010, Auld, A.W., Aronson, H.A., Gargano, F. Arch Neurol. 1965, 13 (4), Miller, C.F., 2nd, Spetzler, R.F., Kopaniky, D.J.J Neurosurg. 1979, 50 (6), Ustun, M.E., Buyukmumcu, M., Ulku, C.H., Guney, O., Salbacak, A. Skull Base. 2006, 16 (1), Acknowledgements: This study was supported by a grant from the Siriraj Graduate Thesis Scholarship, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok 10700, Thailand. We gratefully acknowledge the Department of Anatomy, Faculty of Medicine Siriraj Hospital, Mahidol University. Special thanks are expressed to Professor Dr Sanjai Sangvivhien for his valuable advice for this study. Key words: Middle meningeal artery, Pterion, Middle cranial fossa, Base of skull, Trigeminal nerve 37 th Congress on Science and Technology of Thailand 5