ANATOMICAL STUDY
Bypass of the Maxillary Artery to Proximal Middle Cerebral Artery Lin Ma, MD, He-cheng Ren, PhD, and Ying Huang, PhD Objective: The objective of this work was to explore the feasibility of bypass between the maxillary artery (MA) and proximity of middle cerebral artery (MCA). Methods: Ten fixed and perfused adult cadaver heads were dissected bilaterally, 20 sides in total. The superficial temporal artery and its 2 branches were dissected, and outer diameters were measured. The MA and its branch were exposed as well as deep temporal artery; outer diameter of MA was measured. The lengths between the external carotid artery, internal carotid artery, maxillary artery, and proximal middle cerebral artery were measured. Ten healthy adults as targets (20 sides), inner diameter and blood flow dynamic parameters of the common carotid artery, external carotid artery, internal carotid artery, maxillary artery, superficial temporal artery, and its 2 branches were done with ultrasound examination. Results: The mean outer diameter of MA (2.60 ± 0.20 mm) was larger than that of the temporal artery trunk (1.70 ± 0.30 mm). The mean lengths of graft vessels between the internal carotid artery, external carotid artery, and the bifurcation section of MCA (171.00 ± 2.70 and 162.40 ± 2.60 mm) were longer than the mean lengths of graft vessels between MA and MCA bifurcation section (61.70 ±1.50 mm). In adults, the mean blood flow of the second part of MA (62.70 ± 13.30 mL/min) was more than that of the 2 branches of the superficial temporal artery (15.90 ± 3.70 mL/min and 17.70 ± 4.10 ml/min). Conclusion: Bypass between the maxillary artery and proximity of middle cerebral artery is feasible. It is a kind of effective high flow bypass with which the graft vessel is shorter and straighter than the bypass between internal carotid artery or external carotid artery and proximity of middle cerebral artery. Key Words: Maxillary artery, middle cerebral artery, bypass, anatomy, blood flow (J Craniofac Surg 2015;26: 544–547)
I
n modern surgery of skull base, such as in vascular diseases and tumors closely related to basilar artery, autogenous saphenous vein, radial artery, and other arteries, which are similar in diameter, are usually anastomosed with the normal arteries beyond the region of lesion through microsurgery. This kind of surgery is called vascular bypass grafting and is one of the effective methods to ensure intracranial blood supply.1–3 However, some limitations still exist such as low
From the Department of Neurosurgery, Tianjin Huanhu Hospital, Tianjin, China. Received November 26, 2014. Accepted for publication December 23, 2014. Address correspondence and reprint requests to Ying Huang, PhD, Department of Neurosurgery, Tianjin Huanhu Hospital, No. 122 Qixiangtai Rd, Hexi District, 300060, Tianjin, PR China; E-mail: [email protected] The authors report no conflicts of interest. Copyright © 2015 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000001521
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blood flow, long grafting blood vessels, low unobstructed rate, and vascular diameter mismatch in all kinds of intracranial and extracranial vascular bypass surgeries. Recently, many scholars have been trying to study a new bypass method that can produce higher blood flow, shorter grafting blood vessels through bypass of the maxillary artery (MA) with intracranial artery.4–6 This study was aimed to prove the feasibility of bypass between MA and proximal high blood flow vessels of middle cerebral artery.
MATERIALS AND METHODS Materials Cadaver Heads Ten cadaver heads were fixed with 10% of formaldehyde and immersed in 75% alcohol to restore tissue color and to reduce formaldehyde stimulus (Department of Anatomy, Tianjin Huanhu Hospital), rinsed routinely, and arteries and veins were perfused with red and blue rubber, respectively. Each cadaveric head was dissected bilaterally. This study was approved by the ethics committee of Tianjin Huanhu Hospital.
Healthy Adults Ten healthy adults (20 sides) were selected, and their mean age was 38 years (age older than 40 years, 6 patients, 12 sides; age younger than 40 years, 4 cases, 8 sides).
Anatomy of Cadaver Heads Superficial Temporal Artery. Cadaver heads were positioned supine, rotated 20–30 degrees toward the contralateral side of surgical site, and placed on the head holder. Incision was made in the frontotemporal skin followed by a line of 1–2 cm under zygomatic arch and 0.5 cm in front of ear. Scalp was dissected along the layer of epicranial aponeurosis. The top end and the temporal branches of superficial temporal artery were dissected, and the external diameter of the superficial temporal artery and its branches were measured (Fig. 1A).
Maxillary Artery Zygomatic arch was exposed and sawed with drill and end mill grinder. The masseter muscles attaching to the zygomatic arch and its lower edge were turned down. Then, the temporal muscles were dissected from skull surface with a periosteal elevator and pulled in forward and lateral direction. Mandible-anchored site, both of sigmoid notch and mandibular fossa located between the zygomatic process and coronoid process of mandible were exposed. Then, the mandibular artery and its branch-deep temporal artery were carefully dissected in the mandibular fossa (Fig. 1B), and the external diameter of the MA in infratemporal fossa was measured.
The Journal of Craniofacial Surgery • Volume 26, Number 2, March 2015
Copyright © 2015 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
The Journal of Craniofacial Surgery • Volume 26, Number 2, March 2015
An Anatomical and Technical Study
Statistical Analysis Data were presented as mean ± SD, and t test was performed by using SPSS17.0 software. P = 0.05 or less was considered statistically significant.
RESULTS Cadaver Anatomy The mean diameter of MA (2.60 ± 0.20 mm) in infratemporal fossa was larger than that of bifurcation of superficial temporal artery (1.70 ± 0.3 mm) and had significant difference (t test, P < 0.05). The mean length of grafting vessels between internal carotid artery and bifurcation of the middle cerebral artery (171.00 ± 2.70 mm), and external carotid artery and bifurcation of the middle cerebral artery (162.40 ± 2.60 mm) were too long, whereas the mean length of grafting vessels between MA and bifurcation of the middle cerebral artery were relatively shorter (61.70 ± 1.50 mm). FIGURE 1. Anatomies of cadaver heads. A, Frontal and top branches of superficial temporal artery. B, Infratemporal fossa and the maxillary artery. C, Bifurcation of the middle cerebral artery. D, Bifurcation of common carotid artery, initial part of the internal and external carotid artery.
Bifurcation of the Middle Cerebral Artery Temporalis muscle was pulled in forward and lateral direction. Skull was opened with wire saws. Dissection was performed through lateral sulcus and finally the bifurcation of the middle cerebral artery was exposed (Fig. 1C).
Bifurcation of Common Carotid Artery Skin incision was made along the anterior edge of the sternocleidomastoid, and the sternocleidomastoid was isolated, then the carotid sheath was freed and the bifurcation of common carotid artery, beginning parts of the internal and external carotid artery, were exposed (Fig. 1D). Then, the length from the initial parts of internal carotid artery, external carotid artery, and the MA up to the bifurcation of the middle cerebral artery were measured.
Vascular Flow Measurements in Healthy Adults The persons undergoing examination were positioned supine with head tilted to the back and slightly rotated toward the left or right to expose the neck completely. We then examined the sites up to 1.0 cm from under enlargement of common carotid artery and 1.0 cm from bifurcation of common carotid artery, and measured inner diameters and hemodynamic parameters of common carotid artery, internal carotid artery, and external carotid artery by performing ultrasonography. We also examined the superficial temporal artery, maxillary artery, frontal and top branches of superficial temporal artery. We selected the arteries in front of ear, in infratemporal fossa, and frontal and top branches of superficial temporal artery. Then, we measured inner diameters and hemodynamic parameters of common carotid artery, maxillary artery, and frontal and top branches of superficial temporal artery through ultrasonography. We measured inner diameters through 2-dimensional mode and gained the vascular intimal pitch after zooming; we measured hemodynamic parameters through the mode of Doppler. The volume of samples coincided with the size of inner diameter, and angle correction was made. Hemodynamic parameters included peak systolic velocity (Vs), end-diastolic velocity (Ved), mean velocity (Vmean), and pulsatility index (PI). Quantity of blood flow was calculated through the following formula: Q = Vmean A; A7 = [(diameters/2)2 PI] ∏.
Vascular Flow Measurements in Healthy Adults Ten cases (20 sides) of healthy adults were examined by vascular color Doppler methods, and we obtained the clear images from the test and collected the related data (Fig. 2; Table 1). The mean volume of blood flow in the second part of MA (62.70 ± 13.30 mL/min) was more than that of frontal (15.90 ± 3.70 mL/min) and top branches of superficial temporal artery (17.70 ± 4.10 mL/min) and statistically significant difference was observed between the two (t test, P < 0.05).
DISCUSSION Among the vascular bypass surgeries of anterior cerebral circulation, the most commonly used methods are as follows: vascular bypass of superficial temporal artery and cortical branch of middle cerebral artery; bypass of superficial temporal artery and the proximal middle cerebral artery; bypass of the external carotid artery and the intracranial carotid artery or middle cerebral artery through long vein grafts; bypass of proximal superficial temporal artery and the middle cerebral artery through short vein grafts; bypass of occipital artery or middle meningeal artery and the temporal or angular gyrus branches of middle cerebral artery, and so on.8–11 The other graft vessels, such as radial artery, are also used for vascular bypass. Among the methods of vascular bypass, the safest and most commonly used one is the bypass of superficial temporal artery and middle cerebral artery cortical branch. However, it was observed that although the anastomotic site was not blocked, only less than 25 mL/min of additional blood flow was provided through bypass of the newly created superficial temporal artery and middle cerebral artery cortical branch, which was far from enough to avoid the occurrence of cerebral ischemia.6,12,13 According to the reports, compared with bypass of superficial temporal artery and middle cerebral artery cortical branch, the
FIGURE 2. Doppler imaging of the maxillary artery.
© 2015 Mutaz B. Habal, MD
Copyright © 2015 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
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The Journal of Craniofacial Surgery • Volume 26, Number 2, March 2015
Ma and Huang
TABLE 1. Inner Diameters and Hemodynamic Parameters Vessels Frontal branch of STA Top branch of STA STA MA ECA ICA CCA
Vs (cm/s)
Ved (cm/s)
Vmean (cm/s)
PI
D (mm)
Q (mL/min)
71.50 ± 18.00 60.80 ± 15.00 68.50 ± 17.00 45.60 ± 11.00 70.80 ± 17.00 61.50 ± 16.00 86.60 ± 21.00
12.90 ± 4.30 11.30 ± 3.90 11.70 ± 4.00 7.70 ± 2.80 8.40 ± 3.00 24.70 ± 8.40 26.30 ± 8.70
21.70 ± 6.70 19.10 ± 5.90 23.40 ± 6.90 15.70 ± 5.50 15.50 ± 5.60 33.60 ± 7.10 35.40 ± 7.60
2.29 ± 0.50 2.33 ± 0.50 2.54 ± 0.60 2.50 ± 0.50 2.62 ± 0.60 1.08 ± 0.30 1.81 ± 0.50
0.80 ± 0.08 0.90 ± 0.09 1.50 ± 0.14 2.00 ± 0.19 3.80 ± 0.37 4.70 ± 0.45 6.30 ± 0.58
15.90 ± 3.70 17.70 ± 4.10 43.00 ± 9.70 62.70 ± 13.30 170.00 ± 33.70 271.00 ± 53.30 478.00 ± 105.00
Vs, peak systolic velocity; Ved, end-diastolic velocity; Vmean, mean velocity; PI, pulsatility index; D, inner diameter; Q, blood flow quantity; STA, superficial temporal artery; ECA, external carotid artery; ICA, internal carotid artery; CCA, common carotid artery.
bypass, which considered the internal carotid artery or proximal cerebral middle artery as accepting blood vessels, could provide more powerful protection.8–10 Therefore, the scholars began to study anatomy of the maxillary artery and tried to perform the vascular bypass of the MA and the proximal middle cerebral artery.4–6 Currently, there have been few clinical reports about the bypass through the MA to treat ischemic cerebral diseases and giant aneurysms.6 In this research, we discovered that the diameters of the maxillary artery, the radial artery, and M2 part of cerebral middle artery matched with each other. Because the diameter of all 3 arteries were more than 2 mm and the volume of blood flow of the second part of the MA (62.70 ± 13.30 mL/min) was more than that of frontal (15.90 ± 3.70 mL/min) and top branches of superficial temporal artery (17.70 ± 4.10 mL/min), this bypass could provide more blood flow for brain. We discovered that the diameter of every branch of middle cerebral artery was consistent with the report from Umansky et al.14 We selected the thickest branch of middle cerebral artery as recipient vessels, which were middle and infra-branches in 20 sides of samples. If middle and infra-branches were regarded as recipient vessels, there were extra advantages such as avoiding lenticulostriate artery. Although the blood flow was blocked for a long time during the bypass surgeries, motor dysfunction was not induced. The advantages of vascular bypass of the MA and proximal site of the second part of middle cerebral artery are as follows: (1) Because the diameter of superficial temporal artery is less than 2 mm, bypass of the MA and proximal site of the second part of middle cerebral artery can provide more blood flow compared with bypass of superficial temporal artery and middle cerebral artery cortical branch. (2) Since the grafts are shorter, the higher rate of patency is shown in bypass of the MA and proximal site of the second part of middle cerebral artery. According to report,15 shorter vein or artery had a higher patency rates (80%–90%). Although bypass of external carotid artery and proximal site of the second part of middle cerebral artery can provide more quantity of blood flow, its patency rate is lower (70%–80%). (3) The technique of bypass of the MA and proximal site of the second part of middle cerebral artery is simpler than bypass of external carotid artery and proximal site of the second part of middle cerebral artery, and the neck incision is also not needed. (4) The graft vessel that is used for bypass of external carotid artery and proximal site of the second part of middle cerebral artery will form a curve when entering the lateral fissure, but there is no curve when bypass of the MA and proximal site of the second part of middle cerebral artery is performed, meaning that bypass travels in nearly a straight line, which is a very important factor for governing patency of graft. Bending or twisting of grafts can reduce blood flow velocity and result in graft occlusion. In our study, none of the cases had occurrence of bending or twisting of grafting vessels. According to study of cadaver head dissection from Hanel et al,12 the bypass was testified between the MA and bed salient segment of the internal carotid artery. However, it required
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a broader anatomy, deeper operative site, and more skilled micromanipulation techniques. (5) Because the position of blood vessels was deep, outside temperature had little effect. The second segment of MA located in infratemporal fossa and grafts was also deep in the temporal muscle, so the grafts in deep position provided blood flow from MA to brain, which had few possibilities of harmful impact induced by outside temperature, and intracranial vascular stimulation was also weaker compared with graft vessels through subcutaneous tunnel to the brain. (6) In our study, most parts of graft vessels were intracranial and were not influenced by movement of head. However, the traditional grafts traveled subcutaneously and could be easily twisted and pressed, resulting in blockage. However, there are also some limitations for bypass of the MA and proximal site of the second part of middle cerebral artery such as the following: (1) as the site of anastomosis is located in the lateral fissure, it requires dissection through more anatomical structures of subarachnoid compared with bypass of superficial temporal artery and middle cerebral artery cortical branch; (2) it requires graft vessels and 2 sites of anastomosis, which extends the operation duration and might decrease patency rate as compared to single anastomosis; (3) it requires removal of the zygomatic arch, although it is not a difficult procedure. Bone connecting piece makes the zygomatic arch reset easier; (4) if preoperative angiography shows that there are important intracranial and extracranial lateral branches anastomosing with maxillary artery, another way of bypass should be chosen.
CONCLUSIONS Bypass between the MA and proximity of middle cerebral artery is feasible. It is a kind of effective high-flow bypass with which the graft vessel is shorter and straighter than the bypass between internal carotid artery or external carotid artery and proximity of middle cerebral artery.
REFERENCES 1. Sekhar LN, Natarajan SK, Ellenbogen RG, et al. Cerebral revascularization for ischemia, aneurysms, and cranial base tumors. Neurosurgery 2008;62:1373–1408 2. Ramanathan D, Temkin N, Kim LJ, et al. Cerebral bypasses for complex aneurysms and tumors: long-term results and graft management strategies. Neurosurgery 2012;70:1442–1457 3. Sekhar LN, Kalavakonda C. Cerebral revascularization for aneurysms and tumors. Neurosurgery 2002;50:321–331 4. Ustun ME, Buyukmumcu M, Ulku CH, et al. Radial artery graft for bypass of the maxillary to proximal middle cerebral artery: an anatomic and technical study. Neurosurgery 2004;54:667–671 5. Ulku CH, Ustun ME, Buyukmumcu M, et al. Radial artery graft for bypass of the maxillary to proximal posterior cerebral artery: an anatomical and technical study. Acta Otolaryngol 2004;124:858–862
© 2015 Mutaz B. Habal, MD
Copyright © 2015 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
The Journal of Craniofacial Surgery • Volume 26, Number 2, March 2015 6. Shi X, Qian H, KC KI, et al. Bypass of the maxillary to proximal middle cerebral artery or proximal posterior cerebral artery with radial artery graft. Acta Neurochir (Wien) 2011;153:1649–1655 7. Smith HJ. Quantitative Doppler flowmetry. I. Construction and testing of a duplex scanning system. Acta Radiol Diagn (Stockh) 1984;25:305–312 8. Sekhar LN, Sen CN, Jho HD. Saphenous vein graft bypass of the cavernous internal carotid artery. J Neurosurg 1990;72:35–41 9. Sekhar LN, Burgess J, Akin O. Anatomical study of the cavernous sinus emphasizing operative approaches and related vascular and neural reconstruction. Neurosurgery 1987;21:806–816 10. Spetzler RF, Fukushima T, Martin N, et al. Petrous carotid-to-intradural carotid saphenous vein graft for intracavernous giant aneurysm, tumor, and occlusive cerebrovascular disease. J Neurosurg 1990;73:496–501
An Anatomical and Technical Study
11. Ausman JI, Nicoloff DM, Chou SN. Posterior fossa revascularization: anastomosis of vertebral artery to PICA with interposed radial artery graft. Surg Neurol 1978;9:281–286 12. Hanel RA, Spetzler RF. Surgical treatment of complex intracranial aneurysms. Neurosurgery 2008;62:1289–1299 13. Mura J, Malogo-Tavares W, Figueiredo EG. Basic aspects of high-flow extracranial-intracranial bypass: part I. Contemp Neurosurg 2010;32:1–4 14. Umansky F, Juarez SM, Dujovny M, et al. Microsurgical anatomy of the proximal segments of the middle cerebral artery. J Neurosurg 1984;61:458–467 15. Vrionis FD, Cano WG, Heilman CB. Microsurgical anatomy of the infratemporal fossa as viewed laterally and superiorly. Neurosurgery 1996;39:777–786
© 2015 Mutaz B. Habal, MD
Copyright © 2015 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
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Bypass of the Maxillary Artery to Proximal Middle Cerebral Artery Lin Ma, MD, He-cheng Ren, PhD, and Ying Huang, PhD Objective: The objective of this work was to explore the feasibility of bypass between the maxillary artery (MA) and proximity of middle cerebral artery (MCA). Methods: Ten fixed and perfused adult cadaver heads were dissected bilaterally, 20 sides in total. The superficial temporal artery and its 2 branches were dissected, and outer diameters were measured. The MA and its branch were exposed as well as deep temporal artery; outer diameter of MA was measured. The lengths between the external carotid artery, internal carotid artery, maxillary artery, and proximal middle cerebral artery were measured. Ten healthy adults as targets (20 sides), inner diameter and blood flow dynamic parameters of the common carotid artery, external carotid artery, internal carotid artery, maxillary artery, superficial temporal artery, and its 2 branches were done with ultrasound examination. Results: The mean outer diameter of MA (2.60 ± 0.20 mm) was larger than that of the temporal artery trunk (1.70 ± 0.30 mm). The mean lengths of graft vessels between the internal carotid artery, external carotid artery, and the bifurcation section of MCA (171.00 ± 2.70 and 162.40 ± 2.60 mm) were longer than the mean lengths of graft vessels between MA and MCA bifurcation section (61.70 ±1.50 mm). In adults, the mean blood flow of the second part of MA (62.70 ± 13.30 mL/min) was more than that of the 2 branches of the superficial temporal artery (15.90 ± 3.70 mL/min and 17.70 ± 4.10 ml/min). Conclusion: Bypass between the maxillary artery and proximity of middle cerebral artery is feasible. It is a kind of effective high flow bypass with which the graft vessel is shorter and straighter than the bypass between internal carotid artery or external carotid artery and proximity of middle cerebral artery. Key Words: Maxillary artery, middle cerebral artery, bypass, anatomy, blood flow (J Craniofac Surg 2015;26: 544–547)
I
n modern surgery of skull base, such as in vascular diseases and tumors closely related to basilar artery, autogenous saphenous vein, radial artery, and other arteries, which are similar in diameter, are usually anastomosed with the normal arteries beyond the region of lesion through microsurgery. This kind of surgery is called vascular bypass grafting and is one of the effective methods to ensure intracranial blood supply.1–3 However, some limitations still exist such as low
From the Department of Neurosurgery, Tianjin Huanhu Hospital, Tianjin, China. Received November 26, 2014. Accepted for publication December 23, 2014. Address correspondence and reprint requests to Ying Huang, PhD, Department of Neurosurgery, Tianjin Huanhu Hospital, No. 122 Qixiangtai Rd, Hexi District, 300060, Tianjin, PR China; E-mail: [email protected] The authors report no conflicts of interest. Copyright © 2015 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000001521
544
blood flow, long grafting blood vessels, low unobstructed rate, and vascular diameter mismatch in all kinds of intracranial and extracranial vascular bypass surgeries. Recently, many scholars have been trying to study a new bypass method that can produce higher blood flow, shorter grafting blood vessels through bypass of the maxillary artery (MA) with intracranial artery.4–6 This study was aimed to prove the feasibility of bypass between MA and proximal high blood flow vessels of middle cerebral artery.
MATERIALS AND METHODS Materials Cadaver Heads Ten cadaver heads were fixed with 10% of formaldehyde and immersed in 75% alcohol to restore tissue color and to reduce formaldehyde stimulus (Department of Anatomy, Tianjin Huanhu Hospital), rinsed routinely, and arteries and veins were perfused with red and blue rubber, respectively. Each cadaveric head was dissected bilaterally. This study was approved by the ethics committee of Tianjin Huanhu Hospital.
Healthy Adults Ten healthy adults (20 sides) were selected, and their mean age was 38 years (age older than 40 years, 6 patients, 12 sides; age younger than 40 years, 4 cases, 8 sides).
Anatomy of Cadaver Heads Superficial Temporal Artery. Cadaver heads were positioned supine, rotated 20–30 degrees toward the contralateral side of surgical site, and placed on the head holder. Incision was made in the frontotemporal skin followed by a line of 1–2 cm under zygomatic arch and 0.5 cm in front of ear. Scalp was dissected along the layer of epicranial aponeurosis. The top end and the temporal branches of superficial temporal artery were dissected, and the external diameter of the superficial temporal artery and its branches were measured (Fig. 1A).
Maxillary Artery Zygomatic arch was exposed and sawed with drill and end mill grinder. The masseter muscles attaching to the zygomatic arch and its lower edge were turned down. Then, the temporal muscles were dissected from skull surface with a periosteal elevator and pulled in forward and lateral direction. Mandible-anchored site, both of sigmoid notch and mandibular fossa located between the zygomatic process and coronoid process of mandible were exposed. Then, the mandibular artery and its branch-deep temporal artery were carefully dissected in the mandibular fossa (Fig. 1B), and the external diameter of the MA in infratemporal fossa was measured.
The Journal of Craniofacial Surgery • Volume 26, Number 2, March 2015
Copyright © 2015 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
The Journal of Craniofacial Surgery • Volume 26, Number 2, March 2015
An Anatomical and Technical Study
Statistical Analysis Data were presented as mean ± SD, and t test was performed by using SPSS17.0 software. P = 0.05 or less was considered statistically significant.
RESULTS Cadaver Anatomy The mean diameter of MA (2.60 ± 0.20 mm) in infratemporal fossa was larger than that of bifurcation of superficial temporal artery (1.70 ± 0.3 mm) and had significant difference (t test, P < 0.05). The mean length of grafting vessels between internal carotid artery and bifurcation of the middle cerebral artery (171.00 ± 2.70 mm), and external carotid artery and bifurcation of the middle cerebral artery (162.40 ± 2.60 mm) were too long, whereas the mean length of grafting vessels between MA and bifurcation of the middle cerebral artery were relatively shorter (61.70 ± 1.50 mm). FIGURE 1. Anatomies of cadaver heads. A, Frontal and top branches of superficial temporal artery. B, Infratemporal fossa and the maxillary artery. C, Bifurcation of the middle cerebral artery. D, Bifurcation of common carotid artery, initial part of the internal and external carotid artery.
Bifurcation of the Middle Cerebral Artery Temporalis muscle was pulled in forward and lateral direction. Skull was opened with wire saws. Dissection was performed through lateral sulcus and finally the bifurcation of the middle cerebral artery was exposed (Fig. 1C).
Bifurcation of Common Carotid Artery Skin incision was made along the anterior edge of the sternocleidomastoid, and the sternocleidomastoid was isolated, then the carotid sheath was freed and the bifurcation of common carotid artery, beginning parts of the internal and external carotid artery, were exposed (Fig. 1D). Then, the length from the initial parts of internal carotid artery, external carotid artery, and the MA up to the bifurcation of the middle cerebral artery were measured.
Vascular Flow Measurements in Healthy Adults The persons undergoing examination were positioned supine with head tilted to the back and slightly rotated toward the left or right to expose the neck completely. We then examined the sites up to 1.0 cm from under enlargement of common carotid artery and 1.0 cm from bifurcation of common carotid artery, and measured inner diameters and hemodynamic parameters of common carotid artery, internal carotid artery, and external carotid artery by performing ultrasonography. We also examined the superficial temporal artery, maxillary artery, frontal and top branches of superficial temporal artery. We selected the arteries in front of ear, in infratemporal fossa, and frontal and top branches of superficial temporal artery. Then, we measured inner diameters and hemodynamic parameters of common carotid artery, maxillary artery, and frontal and top branches of superficial temporal artery through ultrasonography. We measured inner diameters through 2-dimensional mode and gained the vascular intimal pitch after zooming; we measured hemodynamic parameters through the mode of Doppler. The volume of samples coincided with the size of inner diameter, and angle correction was made. Hemodynamic parameters included peak systolic velocity (Vs), end-diastolic velocity (Ved), mean velocity (Vmean), and pulsatility index (PI). Quantity of blood flow was calculated through the following formula: Q = Vmean A; A7 = [(diameters/2)2 PI] ∏.
Vascular Flow Measurements in Healthy Adults Ten cases (20 sides) of healthy adults were examined by vascular color Doppler methods, and we obtained the clear images from the test and collected the related data (Fig. 2; Table 1). The mean volume of blood flow in the second part of MA (62.70 ± 13.30 mL/min) was more than that of frontal (15.90 ± 3.70 mL/min) and top branches of superficial temporal artery (17.70 ± 4.10 mL/min) and statistically significant difference was observed between the two (t test, P < 0.05).
DISCUSSION Among the vascular bypass surgeries of anterior cerebral circulation, the most commonly used methods are as follows: vascular bypass of superficial temporal artery and cortical branch of middle cerebral artery; bypass of superficial temporal artery and the proximal middle cerebral artery; bypass of the external carotid artery and the intracranial carotid artery or middle cerebral artery through long vein grafts; bypass of proximal superficial temporal artery and the middle cerebral artery through short vein grafts; bypass of occipital artery or middle meningeal artery and the temporal or angular gyrus branches of middle cerebral artery, and so on.8–11 The other graft vessels, such as radial artery, are also used for vascular bypass. Among the methods of vascular bypass, the safest and most commonly used one is the bypass of superficial temporal artery and middle cerebral artery cortical branch. However, it was observed that although the anastomotic site was not blocked, only less than 25 mL/min of additional blood flow was provided through bypass of the newly created superficial temporal artery and middle cerebral artery cortical branch, which was far from enough to avoid the occurrence of cerebral ischemia.6,12,13 According to the reports, compared with bypass of superficial temporal artery and middle cerebral artery cortical branch, the
FIGURE 2. Doppler imaging of the maxillary artery.
© 2015 Mutaz B. Habal, MD
Copyright © 2015 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
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Ma and Huang
TABLE 1. Inner Diameters and Hemodynamic Parameters Vessels Frontal branch of STA Top branch of STA STA MA ECA ICA CCA
Vs (cm/s)
Ved (cm/s)
Vmean (cm/s)
PI
D (mm)
Q (mL/min)
71.50 ± 18.00 60.80 ± 15.00 68.50 ± 17.00 45.60 ± 11.00 70.80 ± 17.00 61.50 ± 16.00 86.60 ± 21.00
12.90 ± 4.30 11.30 ± 3.90 11.70 ± 4.00 7.70 ± 2.80 8.40 ± 3.00 24.70 ± 8.40 26.30 ± 8.70
21.70 ± 6.70 19.10 ± 5.90 23.40 ± 6.90 15.70 ± 5.50 15.50 ± 5.60 33.60 ± 7.10 35.40 ± 7.60
2.29 ± 0.50 2.33 ± 0.50 2.54 ± 0.60 2.50 ± 0.50 2.62 ± 0.60 1.08 ± 0.30 1.81 ± 0.50
0.80 ± 0.08 0.90 ± 0.09 1.50 ± 0.14 2.00 ± 0.19 3.80 ± 0.37 4.70 ± 0.45 6.30 ± 0.58
15.90 ± 3.70 17.70 ± 4.10 43.00 ± 9.70 62.70 ± 13.30 170.00 ± 33.70 271.00 ± 53.30 478.00 ± 105.00
Vs, peak systolic velocity; Ved, end-diastolic velocity; Vmean, mean velocity; PI, pulsatility index; D, inner diameter; Q, blood flow quantity; STA, superficial temporal artery; ECA, external carotid artery; ICA, internal carotid artery; CCA, common carotid artery.
bypass, which considered the internal carotid artery or proximal cerebral middle artery as accepting blood vessels, could provide more powerful protection.8–10 Therefore, the scholars began to study anatomy of the maxillary artery and tried to perform the vascular bypass of the MA and the proximal middle cerebral artery.4–6 Currently, there have been few clinical reports about the bypass through the MA to treat ischemic cerebral diseases and giant aneurysms.6 In this research, we discovered that the diameters of the maxillary artery, the radial artery, and M2 part of cerebral middle artery matched with each other. Because the diameter of all 3 arteries were more than 2 mm and the volume of blood flow of the second part of the MA (62.70 ± 13.30 mL/min) was more than that of frontal (15.90 ± 3.70 mL/min) and top branches of superficial temporal artery (17.70 ± 4.10 mL/min), this bypass could provide more blood flow for brain. We discovered that the diameter of every branch of middle cerebral artery was consistent with the report from Umansky et al.14 We selected the thickest branch of middle cerebral artery as recipient vessels, which were middle and infra-branches in 20 sides of samples. If middle and infra-branches were regarded as recipient vessels, there were extra advantages such as avoiding lenticulostriate artery. Although the blood flow was blocked for a long time during the bypass surgeries, motor dysfunction was not induced. The advantages of vascular bypass of the MA and proximal site of the second part of middle cerebral artery are as follows: (1) Because the diameter of superficial temporal artery is less than 2 mm, bypass of the MA and proximal site of the second part of middle cerebral artery can provide more blood flow compared with bypass of superficial temporal artery and middle cerebral artery cortical branch. (2) Since the grafts are shorter, the higher rate of patency is shown in bypass of the MA and proximal site of the second part of middle cerebral artery. According to report,15 shorter vein or artery had a higher patency rates (80%–90%). Although bypass of external carotid artery and proximal site of the second part of middle cerebral artery can provide more quantity of blood flow, its patency rate is lower (70%–80%). (3) The technique of bypass of the MA and proximal site of the second part of middle cerebral artery is simpler than bypass of external carotid artery and proximal site of the second part of middle cerebral artery, and the neck incision is also not needed. (4) The graft vessel that is used for bypass of external carotid artery and proximal site of the second part of middle cerebral artery will form a curve when entering the lateral fissure, but there is no curve when bypass of the MA and proximal site of the second part of middle cerebral artery is performed, meaning that bypass travels in nearly a straight line, which is a very important factor for governing patency of graft. Bending or twisting of grafts can reduce blood flow velocity and result in graft occlusion. In our study, none of the cases had occurrence of bending or twisting of grafting vessels. According to study of cadaver head dissection from Hanel et al,12 the bypass was testified between the MA and bed salient segment of the internal carotid artery. However, it required
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a broader anatomy, deeper operative site, and more skilled micromanipulation techniques. (5) Because the position of blood vessels was deep, outside temperature had little effect. The second segment of MA located in infratemporal fossa and grafts was also deep in the temporal muscle, so the grafts in deep position provided blood flow from MA to brain, which had few possibilities of harmful impact induced by outside temperature, and intracranial vascular stimulation was also weaker compared with graft vessels through subcutaneous tunnel to the brain. (6) In our study, most parts of graft vessels were intracranial and were not influenced by movement of head. However, the traditional grafts traveled subcutaneously and could be easily twisted and pressed, resulting in blockage. However, there are also some limitations for bypass of the MA and proximal site of the second part of middle cerebral artery such as the following: (1) as the site of anastomosis is located in the lateral fissure, it requires dissection through more anatomical structures of subarachnoid compared with bypass of superficial temporal artery and middle cerebral artery cortical branch; (2) it requires graft vessels and 2 sites of anastomosis, which extends the operation duration and might decrease patency rate as compared to single anastomosis; (3) it requires removal of the zygomatic arch, although it is not a difficult procedure. Bone connecting piece makes the zygomatic arch reset easier; (4) if preoperative angiography shows that there are important intracranial and extracranial lateral branches anastomosing with maxillary artery, another way of bypass should be chosen.
CONCLUSIONS Bypass between the MA and proximity of middle cerebral artery is feasible. It is a kind of effective high-flow bypass with which the graft vessel is shorter and straighter than the bypass between internal carotid artery or external carotid artery and proximity of middle cerebral artery.
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© 2015 Mutaz B. Habal, MD
Copyright © 2015 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
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An Anatomical and Technical Study
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Copyright © 2015 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
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