ec - ic , extracranial - intracranial imax , internal maxillary artery mca , middle cerebral artery sc - ic , subcranial - intracranial sta , superficial temporal artery
we recently treated 4 patients with sc - ic bypass who required cerebral bypasses to effectively treat various cerebrovascular pathologies . the decision to treat the patient with a bypass and the feasibility of the sc - ic bypass
was made in a multidisciplinary fashion by the neurovascular , neuroradiology , and cranial base teams .
our multidisciplinary team performed cadaveric dissection to better assess the subcranial approach for exposure of the imax in the infratemporal fossa . in this dissection ,
subsequently , a lateral rectangle craniectomy of the temporal fossa floor was created up to a point that was 2 mm lateral to a virtual line connecting the foramen rotundum and foramen ovale ( figures 1 - 4 ) .
the deep temporal arteries on the medial aspect of the temporalis muscle were then identified and followed to the imax .
drawing of an elevated skin flap and temporalis , after osteotomy ; the line indicates the craniotomy site .
the red area indicates the contemplated craniectomy of the middle cranial fossa floor to unroof the infratemporal fossa .
the  corridor  craniectomy will reach a line 2 mm lateral to the virtual line between the foramen ovale and foramen rotundum . a right - sided cadaveric dissection demonstrates an orbitozygomatic osteotomy and frontotemporal craniotomy .
the craniectomy ( thick red arrow ) is done up to the virtual line 2 mm lateral to v2 and v3 entering foramen rotundum and foramen ovale , respectively ( thin arrows ) .
the internal maxillary artery is dissected in the infratemporal fossa ( large gray arrow ) .
zygomatic osteotomy ( with or without orbital osteotomy ) was used followed by frontotemporal craniotomy and subsequently temporal fossa craniectomy reaching its medial border designated by the same virtual line connecting the foramen rotundum and foramen ovale ( figures 4 and 5 ) .
we use computed tomography angiography  based neuronavigation and micro doppler probe ( mizuho inc .
tokyo , japan ) . to identify the imax artery in the pterygoid muscles ( figures 6 and 7 ) .
anatomically , the deep temporal arteries in the medial aspect of the temporalis muscle were followed proximally to allow definitive identification of the imax artery .
the first patient 's proximal anastomosis was performed in an end - to - side fashion , whereas the proximal anastomoses in the subsequent 3 patients were end to end ( figures 8 - 10 ) .
the end - to - end anastomoses were technically less demanding than the end to side .
in the 3 end - to - end cases , reversed subcutaneous brachiocephalic veins were used rather than the radial artery .
this vessel was consistently an excellent diameter  match  with the donor imax . in our experience ,
the brachiocephalic vein was consistently reliably free of valves and had a paucity of branches .
intraoperative flow measurements using the charbel microflow probe ( transonic systems inc . , ithaca , new york ) was performed in all patients .
intraoperative angiography and indocyanine green videoangiography were obtained to evaluate bypass patency in all patients .
all patients also underwent postoperative angiography to further assess the flow within the bypass and to further treat the aneurysms with endovascular techniques , as deemed necessary . left side intraoperative craniectomy of the middle cranial fossa floor , similar in view to the cadaveric dissection shown in figure 4 .
a screen shot from the stryker neuronavigation system ( stryker instruments , kalamazoo , michigan ) shows the localization of the internal maxillary artery ( red arrows ) . a left - sided intraoperative image of the internal maxillary artery ( blue arrow ) dissected in the infratemporal fossa .
drawing of the donor internal maxillary artery and the recipient m3 in the opened sylvian fissure .
drawing of the proximal end - to - end anastomosis and a permanent clip on the distal internal maxillary artery and distal end - to - side anastomosis to the m3 .
zygomatic osteotomy ( with or without orbital osteotomy ) was used followed by frontotemporal craniotomy and subsequently temporal fossa craniectomy reaching its medial border designated by the same virtual line connecting the foramen rotundum and foramen ovale ( figures 4 and 5 ) .
we use computed tomography angiography  based neuronavigation and micro doppler probe ( mizuho inc .
tokyo , japan ) . to identify the imax artery in the pterygoid muscles ( figures 6 and 7 ) .
anatomically , the deep temporal arteries in the medial aspect of the temporalis muscle were followed proximally to allow definitive identification of the imax artery .
the first patient 's proximal anastomosis was performed in an end - to - side fashion , whereas the proximal anastomoses in the subsequent 3 patients were end to end ( figures 8 - 10 ) .
the end - to - end anastomoses were technically less demanding than the end to side .
in the 3 end - to - end cases , reversed subcutaneous brachiocephalic veins were used rather than the radial artery .
this vessel was consistently an excellent diameter  match  with the donor imax . in our experience ,
the brachiocephalic vein was consistently reliably free of valves and had a paucity of branches .
intraoperative angiography and indocyanine green videoangiography were obtained to evaluate bypass patency in all patients .
all patients also underwent postoperative angiography to further assess the flow within the bypass and to further treat the aneurysms with endovascular techniques , as deemed necessary . left side intraoperative craniectomy of the middle cranial fossa floor , similar in view to the cadaveric dissection shown in figure 4 .
a screen shot from the stryker neuronavigation system ( stryker instruments , kalamazoo , michigan ) shows the localization of the internal maxillary artery ( red arrows ) . a left - sided intraoperative image of the internal maxillary artery ( blue arrow ) dissected in the infratemporal fossa .
drawing of the donor internal maxillary artery and the recipient m3 in the opened sylvian fissure .
drawing of the proximal end - to - end anastomosis and a permanent clip on the distal internal maxillary artery and distal end - to - side anastomosis to the m3 .
one case was a flow augmentation bypass for a hypoperfused hemisphere in a patient with neurofibromatosis type 2 who underwent cervical surgery for resection of a cervical neurofibroma that resulted in occlusion of the internal carotid artery .
this patient also had a very small - caliber superficial temporal artery ( sta ) .
two patients have a diagnosis of a giant mca aneurysm not amendable to endovascular treatment or direct microsurgical clipping ( figures 11 and 12 ) .
one of these patients had undergone a previous craniotomy in which the ipsilateral sta had been sacrificed .
this patient experienced major recanalization of her aneurysm after endovascular coiling and presented with severe brain edema .
subsequent to sc - ic bypass , the distal m1 segment was clipped , and the patient was subsequently treated by trapping of her proximal m1 segment using coil embolization . a , computed tomography angiography of a patient with enlarging serpentine m2 aneurysm .
b , magnetic resonance angiography demonstrates the thrombosed aneurysm and the flow into the aneurysm .
patient had had a previous frontotemporal craniotomy for meningioma and had no superficial temporal artery . in the first patient ,
the imax was identified in the infratemporal fossa by neuronavigation coupled with micro doppler confirmation ( figure 6 ) . in the subsequent patients , anatomic landmarks formed by the virtual line between the foramen rotundum and foramen ovale ( which marks the medial border of the craniectomy ) , as well as the deep temporalis arteries that lead to the imax ,
the position of the imax was then confirmed by micro doppler . in our last case ,
intraoperative flow measurements , in the graft , using the charbel flow probe ( transonic systems inc ) , ranged from 20 to 60 ml / min . in the cases of end - to - end anastomosis ( figure 13 )
retrograde filling of distal imax territory by external carotid artery collaterals was demonstrated on all postoperative angiograms . a left - sided intraoperative image of the proximal end - to - end anastomosis of the internal maxillary artery ( imax ) and the vein graft ( orange arrow ) .
postoperative angiography demonstrated good filling of the graft with robust distal flow in all cases ( figures 14 and 15 ) .
this plan allows early flow demand to be placed on the transplanted graft with real - time angiographic flow assessment before aneurysm deconstruction .
in addition , by eliminating surgical exposure of the aneurysm , less surgical dissection is required , limiting surgical morbidity to the construction of the bypass itself .
the last case underwent distal microsurgical m1 segment sacrifice with the residual aneurysm coiled and completely occluded postoperatively .
retrograde filling was demonstrated from the sc - ic anastomosis into the m1 segment up to the clip , allowing flow into the lateral lenticulostriate arteries arising from this portion of the m1 segment .
a , an internal carotid artery injection demonstrates complete occlusion ( no distal flow ) of the aneurysm by coil mass .
b , an external carotid artery injection demonstrates a patent bypass that fills the middle cerebral artery territory .
anteroposterior ( a ) and lateral ( b ) projections of a common carotid artery injection demonstrate a patent bypass and filling of the entire hemisphere .
one of the aneurysm patients in our series experienced postoperative swelling of the hemisphere after aneurysm embolization and underwent decompressive craniectomy .
one case was a flow augmentation bypass for a hypoperfused hemisphere in a patient with neurofibromatosis type 2 who underwent cervical surgery for resection of a cervical neurofibroma that resulted in occlusion of the internal carotid artery .
this patient also had a very small - caliber superficial temporal artery ( sta ) .
two patients have a diagnosis of a giant mca aneurysm not amendable to endovascular treatment or direct microsurgical clipping ( figures 11 and 12 ) .
one of these patients had undergone a previous craniotomy in which the ipsilateral sta had been sacrificed .
this patient experienced major recanalization of her aneurysm after endovascular coiling and presented with severe brain edema .
subsequent to sc - ic bypass , the distal m1 segment was clipped , and the patient was subsequently treated by trapping of her proximal m1 segment using coil embolization . a , computed tomography angiography of a patient with enlarging serpentine m2 aneurysm .
b , magnetic resonance angiography demonstrates the thrombosed aneurysm and the flow into the aneurysm .
patient had had a previous frontotemporal craniotomy for meningioma and had no superficial temporal artery .
in the first patient , the imax was identified in the infratemporal fossa by neuronavigation coupled with micro doppler confirmation ( figure 6 ) . in the subsequent patients , anatomic landmarks formed by the virtual line between the foramen rotundum and foramen ovale ( which marks the medial border of the craniectomy ) , as well as the deep temporalis arteries that lead to the imax ,
the position of the imax was then confirmed by micro doppler . in our last case ,
intraoperative flow measurements , in the graft , using the charbel flow probe ( transonic systems inc ) , ranged from 20 to 60 ml / min . in the cases of end - to - end anastomosis ( figure 13 )
retrograde filling of distal imax territory by external carotid artery collaterals was demonstrated on all postoperative angiograms . a left - sided intraoperative image of the proximal end - to - end anastomosis of the internal maxillary artery ( imax ) and the vein graft ( orange arrow ) .
all patients tolerated the imax sc - ic bypass well . postoperative angiography demonstrated good filling of the graft with robust distal flow in all cases ( figures 14 and 15 ) .
this plan allows early flow demand to be placed on the transplanted graft with real - time angiographic flow assessment before aneurysm deconstruction .
in addition , by eliminating surgical exposure of the aneurysm , less surgical dissection is required , limiting surgical morbidity to the construction of the bypass itself .
the last case underwent distal microsurgical m1 segment sacrifice with the residual aneurysm coiled and completely occluded postoperatively .
retrograde filling was demonstrated from the sc - ic anastomosis into the m1 segment up to the clip , allowing flow into the lateral lenticulostriate arteries arising from this portion of the m1 segment .
a , an internal carotid artery injection demonstrates complete occlusion ( no distal flow ) of the aneurysm by coil mass .
b , an external carotid artery injection demonstrates a patent bypass that fills the middle cerebral artery territory .
anteroposterior ( a ) and lateral ( b ) projections of a common carotid artery injection demonstrate a patent bypass and filling of the entire hemisphere .
one of the aneurysm patients in our series experienced postoperative swelling of the hemisphere after aneurysm embolization and underwent decompressive craniectomy .
cerebral bypass has been used for many years for the treatment of cranial base tumors and giant aneurysms as well as for flow augmentation into hypoperfused cerebral hemispheres.1 - 4,10 the 2 basic modalities of bypass are either ec - ic bypass or ic - ic ( in situ ) bypass.11 - 13 the most common ec - ic bypass is the sta - mca bypass . in cases in which the target of the bypass is flow replacement ,
a higher flow bypass graft is often required.14,15 in these cases , the cervical carotid artery is typically used as the donor site , using either a saphenous vein or radial artery as a graft vessel , which is then anastomosed to an appropriate recipient mca branch.1,2,14,16 this technique typically requires a graft in excess of 20 cm , which can be prone to kinking and subcutaneous compression .
these grafts need to be safely tunneled from the neck to the cranial insertion site ; alternatively , a long skin incision from the craniotomy site down to the cervical carotid is required . additionally , the 2 operative fields are not well visualized through a single operative microscopic view
. the surgeon must move from neck to cranial exposure when performing the 2 anastomoses , and any graft complication is therefore managed with only a partial view of the totality of the graft length .
imax - mca ( sc - ic ) bypass as a high - flow ec - ic bypass option has been described in both cadaveric studies6 - 9,17 and clinical microsurgical practice.5 this bypass option is efficacious in cases that require high flow where the use of the cervical carotid as a donor is contraindicated ( ie , after neck surgery or in the setting of occlusion of the common carotid artery ) . the imax - mca bypass technique and the important modifications that we propose carry a number of distinct advantages over the conventional ec - ic bypass in which the cervical carotid artery is used as a donor .
first , the sc - ic graft is significantly shorter ( 7 - 9 cm ) than the typical length required when using the cervical carotid artery as a proximal anastomosis site .
although bypass length has not been described as a prognostic factor for bypass longevity , longer grafts are theoretically more prone to mechanical disruption such as kinking and compression .
short graft length permits the use of a brachiocephalic rather than a saphenous vein , and graft size can then be tailored more effectively to recipient size .
the brachiocephalic vein has few , if any , valves , which improves overall donor quality .
additionally , potential upper extremity arterial complications that can be associated with radial artery are then avoided.1,18,19 an additional benefit of the sc - ic bypass technique is that the entire intracranial graft  both the proximal and distal anastomoses  is visualized within the same microsurgical field ( figures 16 and 17 ) .
this allows for immediate inspection of the graft , the proximal anastomosis site , and the distal anastomosis site simultaneously and thus improves the safety and efficiency of the operation .
a postoperative computed tomography 3-dimensional reconstruction of the cranium ( from a second patient ) that demonstrates the vein graft bypassing through the floor of the middle cranial fossa .
note the craniectomy at the base of the middle cranial fossa overlying the infratemporal fossa .
the final result demonstrates the vein graft ( blue arrow ) emerging from the infratemporal fossa ( black arrow ) into the sylvian fissure ( green arrow ) in the same operative field .
our modification of the previously described imax bypass technique , in which the imax was identified through a small middle cranial fossa floor window , represents a distinct technical improvement.5 this original technique is highly demanding , requiring drilling in the anterior aspect of the floor of the middle cranial fossa and the subsequent end - to - side anastomosis through this small , constricted middle cranial fossa craniectomy . precise localization and manipulation of the imax through this small window
our sc - ic technique modification used either a zygomatic osteotomy or orbitozygomatic osteotomy followed by a lateral rectangular craniectomy of the middle fossa .
this modification allowed the imax to be reliably anatomically identified over a considerable length of 15 to 20 mm . in cadaver dissections , we localized the imax just anterior and parallel to the line between the foramen rotundum and foramen ovale .
this experience allowed us to execute the craniectomy in situ up to this same line and then readily identify the vessel within the infratemporal fossa ; this exposure then allowed for the performance of the anastomosis in an end - to - end fashion , ultimately , we found that the completion of proximal anastomosis could be performed in a straightforward manner , with wide exposure and illumination of the imax in the infratemporal fossa . there was no need for retractors throughout the procedure .
the imax - mca ( sc - ic ) bypass is safe and effective and has a number of advantages over the conventional ec - ic bypass using the cervical carotid .
these advantages include ( 1 ) shorter graft length , ( 2 ) avoidance of a cervical carotid artery dissection and its attendant complications , ( 3 ) a microsurgical view of the entirety of the intracranial graft and both the proximal and distal anastomoses within the same field , ( 4 ) minimization of the risk of graft kinking and compression , ( 5 ) the ability to use a subcutaneous vein with easier graft sizing rather than the radial artery with its known risks , and ( 6 ) the use of a lateral temporal fossa rectangular craniectomy technique combined with a zygomatic osteotomy .
this craniectomy was found to significantly improve the previously described anastomotic technique by allowing the imax to be reliably identified , accessed , and then used as a proximal blood flow source without the need for significant drilling .
we believe that this technique should be considered as a first choice for an ec - ic bypass in which the sta is either unavailable or inadequate relative to the flow required .
we strongly advocate preparatory cadaveric dissection by the multidisciplinary team before microsurgical in vivo sc - ic bypass using the imax .
the authors have no personal financial or institutional interest in any of the drugs , materials , or devices described in this article .
the authors have no personal financial or institutional interest in any of the drugs , materials , or devices described in this article .
this is an interesting small technical case series with nice illustrations . for the open vascular subspecialist
, it highlights an important nuance to a newer option for an extracranial - intracranial bypass , the internal maxillary  middle cerebral artery ( imax - mca ) bypass . although the overall technique is not novel and the patient number is small , the authors demonstrate the feasibility of , and rationale for , using this modification . as originally described , the imax - mca bypass provides access to the donor artery through only a small opening in the middle fossa floor , which presents technical challenges .
the nuance provided allows for better exposure and control of the donor artery and for end - to - end as well as end - to - side anastomosis .
slick  alternative to more traditional methods , indications for using it are probably very limited .
when available , the superficial temporal artery ( sta ) is a technically easier bypass that does not require a separate graft harvest and can be used even for  high - flow  indications .
i have advocated double - barrel sta - mca bypass whenever feasible , and when both branches are used ( one for the superior division and one for the inferior division ) , flows approaching 100 ml / min are possible in patients with robust arteries .
intracranial - intracranial bypass is also emerging as an attractive option in many cases and shares the benefits of short graft length and the lack of a cervical incision with the currently described technique .
microvascular anastomosis , in whatever form it takes , remains an important skill for cranial neurosurgeons and should continue to be taught to our trainees . in the laboratory ,
synthetic kits , turkey wings , and rats are good models for early experience , and although a high level of trust is required , i have found that senior residents can safely participate in bypass surgery in the operating room .
 background : internal maxillary artery ( imax)middle cerebral artery ( mca ) bypass has been recently described as an alternative to cervical extracranial - intracranial bypass . 
 this technique uses a  keyhole  
 craniectomy in the temporal fossa that requires a technically challenging end - to - side anastomosis.objective:to describe a lateral subtemporal craniectomy of the middle cranial fossa floor to facilitate wide exposure of the imax to facilitate bypass.methods:orbitozygomatic osteotomy is used followed by frontotemporal craniotomy and subsequently laterotemporal fossa craniectomy , reaching its medial border at a virtual line connecting the foramen rotundum and foramen ovale . 
 the imax was identified by using established anatomic landmarks , neuronavigation , and micro doppler probe ( mizuho inc . 
 tokyo , japan ) . additionally , we studied the approach in a cadaveric specimen in preparation for microsurgical bypass.results:there were 4 cases in which the technique was used . 
 one bypass was performed for flow augmentation in a hypoperfused hemisphere . 
 the other 3 were performed as part of treatment paradigms for giant middle cerebral artery aneurysms . 
 vein grafts were used in all patients . the proximal anastomosis was performed in an end - to - side fashion in 1 patient and end - to - end in 3 patients . 
 intraoperative graft flow measured with the transonic flow probe ranged from 20 to 60 ml / min . 
 postoperative angiography demonstrated good filling of the graft with robust distal flow in all cases . 
 all patients tolerated the procedure well.conclusion:imax to middle cerebral artery subcranial - intracranial bypass is safe and efficacious . 
 the laterotemporal fossa craniectomy technique resulted in reliable identification and wide exposure of the imax , facilitating the proximal anastomosis.abbreviations:ec-ic , extracranial - intracranialimax , internal maxillary arterymca , middle cerebral arterysc - ic , subcranial - intracranialsta , superficial temporal artery 
ABBREVIATIONS:
METHODS
Intraoperative Technique
RESULTS
Patients
Anastomoses
Outcome
DISCUSSION
CONCLUSION
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