J Cerebrovasc Endovasc Neurosurg > Volume 26(1); 2024 > Article
Degollado-García, Casas-Martínez, Mejia, Balcázar-Padrón, Rodríguez-Rubio, and Nathal: Internal maxillary artery (IMax) - middle cerebral artery bypass in a patient with bilateral atherosclerotic carotid occlusion: A technical case report

Abstract

Since the first description of the possible utilization of the internal maxillary artery for bypass surgery, there are some reports of its use in aneurysm cases; however, there is no information about the possible advantages of this type of bypass for cerebral ischemic disease.
We present a 77-year-old man with a history of diabetes, hypertension, systemic atherosclerosis, and two acute myocardial infarctions with left hemiparesis. Imaging studies reported total occlusion of the right internal carotid artery and 75% occlusion on the left side, with an old opercular infarction and repeated transient ischemic attacks in the right middle cerebral artery territory despite medical treatment. After a consensus, we decided to perform a bypass from the internal maxillary artery to the M2 segment of the middle cerebral artery using a radial artery graft. After performing the proximal anastomosis, the calculated graft’s free flow was 216 ml/min. Subsequently, after completing the bypass, the patency was confirmed with fluorescein videoangiography and intraoperative Doppler. Postoperatively, imaging studies showed improvement in the perfusion values and the hemiparesis from 3/5 to 4+/5. The patient was discharged one week after the operation, with a modified Rankin scale of 1, without added deficits.
The use of revascularization techniques in steno-occlusive disease indicates a select group of patients that may benefit from this procedure. In addition, internal maxillary artery bypass has provided a safe option for large areas of ischemia that cannot be supplied with a superficial temporal artery - middle cerebral artery bypass.

INTRODUCTION

Yasargil was the first to report the use of an extracranial-intracranial (EC-IC) bypass in 1967 for cerebral atherosclerotic disease [21]. After this report, flow augmentation through an EC-IC bypass in occlusive disease increased until the results of the EC-IC Bypass Study [2], and the COSS (Carotid Occlusion Surgery Study) showed no apparent advantage of the procedure when compared with medical treatment [11]. However, it has been demonstrated that a group of patients may still benefit from bypass if they meet criteria such as symptomatic steno-occlusive disease with an impaired perfusion image study with recurrent symptoms or stroke despite best medical treatment (BMT) [19,22].
The Internal Maxillary artery (IMax) as a donor for EC-IC bypass was first described by Vrionis [16]. After this report, many studies have reported variations of the surgical technique to reach the IMax, mainly for revascularization in aneurysm cases [1,3,10,13,18]. However, to our knowledge, only one article uses IMax as a donor artery for occlusive disease [22]. In these cases, the goal is to reestablish the regional blood flow and glucose metabolism and restore the functional state caused by the chronic ischemia favoring the regression of the hibernating brain [4].
This report shows the utility of the IMax - middle cerebral artery (MCA) bypass to increase the cerebral blood flow in a patient with bilateral internal carotid artery occlusion and repetitive transient ischemic attacks (TIAs) despite BMT.

CASE DESCRIPTION

Presentation

The Institutional Vascular Review Board approved this study. A 77-year-old man with a history of diabetes, hypertension, systemic atherosclerosis, and two acute myocardial infarctions sought medical attention due to repeated TIAs. The image workout showed almost total occlusion of the right internal carotid artery (ICA) with 75% occlusion of the left ICA and a minor stroke at the right MCA territory. Physical examination revealed a left hemiparesis of 3/5. The patient was classified as grade 2 of the modified Rankin scale (mRS). Medical treatment included antiplatelet drugs, control of glucose levels, blood pressure, and the use of statins. However, the patient continued with recurrent TIAs despite this treatment. Magnetic resonance imaging (MRI) with perfusion sequence showed an increase in the time to peak (TTP), mean transit time (MTT), and a decrease in the regional cerebral blood flow (rCBF) at the right ICA territory (Fig. 1A-D). A superficial temporal artery (STA) - MCA bypass was considered; however, this patient had a very small-caliber STA.

Surgical approach (see supplementary Video 1)

To identify the IMax, we used the technique described by Peto et al. [10], consisting of a pterional approach with interfascial dissection of the temporal muscle (TM) and zygomatic osteotomy; the TM was cut, leaving a muscle cuff in the superior temporal line for the reconstruction. Next, the muscle was mobilized to the gap created by the zygomatic osteotomy. Next, the superior head of the lateral pterygoid muscle was identified and, if necessary, transected to discover the IMax. Afterward, a retrograde dissection was made to expose the whole pterygoid segment of the artery.
A radial artery graft (RAG) was obtained from the left side (after a negative Allen test) in a length of 12 cm. Then, a frontotemporal craniotomy was completed, with the temporal extension flush with the floor of the middle fossa. The Sylvian fissure was opened widely to identify M1-M2 segments of the MCA; the superior trunk was dissected and was left ready for distal anastomosis. Next, proximal and distal temporary clips were placed at the dissected segment of the IMax. The artery was divided after the alveolar nerve crossed it and was mobilized for an end-to-end anastomosis with the RAG. The anastomosis was completed with an 8-0 suture, using a separated suture technique; after the proximal anastomosis finished, the calculated graft’s free flow was 216 ml/min. Then, the anastomosis with the superior trunk of M2 was completed with a 10-0 suture with an interrupted suture technique. The temporary clips were released, and the patency was corroborated with fluorescein video angiography and intraoperative Doppler. The dura mater was closed, leaving a dural opening for the RAG, and the rest of the surgical layers were closed and reconstructed as usual (Fig. 2).

Postoperative course

Postoperative computed tomography angiography (CT-Angio) showed patency of the bypass and adequate irrigation of the MCA territory. Diffusion-weighted imaging showed no areas of new ischemic events. Perfusion sequence showed a decrease in the TTP and MTT and an increase in the regional cerebral blood flow (rCBF) in the MCA territory, with hypoperfusion in the posterior cerebral artery (PCA) territory included the watershed area between MCA and PCA (Fig. 1E-H, Fig. 3). In addition, the patient’s hemiparesis improved to 4+/5. The patient was discharged one week after the operation with an mRS of 1 without additional motor deficit to continue rehabilitation in a physical therapy facility.

DISCUSSION

Atherosclerosis of the ICA is a common pathology that leads to complete occlusion in 15,000-20,000 patients annually. These patients are still susceptible to TIAs and may also experience an increased risk of cerebral hypoperfusion that could lead to brain atrophy, reduced corticospinal excitability, cognitive impairment, and dementia [4]. The first response against the hypoperfusion is dilatation to the maximal capacity to increase cerebral perfusion; when this mechanism fails, the vascular insufficiency leads to an increase in oxygen extraction, and this compensatory mechanism reduces the reserve for additional functional demands, which leads to neurologic symptoms and a fluctuation between oligemia and ischemia [6,8,20]. Reynolds et al. classified cerebral hemodynamics failure into three stages: I, II, and III. Our patient presented stage III (true ischemia), meaning that cerebral perfusion pressure decreased below a critical point with a reduction of the volume and cerebral blood flow, prolonged TTP and MTT, and decreased brain metabolism, with an annual stroke rate of 31% [12].
The indication for bypass in atherosclerosis and chronic ischemia is controversial, but when done under strict criteria, the goal is flow augmentation via a new donor artery that provides blood supply to the affected territory. The JET trial showed, for the first time, the preventive effect of EC-IC bypass on stroke recurrence, which has been proved in other series in selected patients [5,9,14,19,22].

Treatment strategy

The patient, in this case, as previously mentioned, continued with neurologic symptoms regardless of BMT, and the perfusion studies showed the whole right MCA territory with hypoperfusion that worsened with his daily activities, meaning that the patient alternated between oligemia and ischemia. So then, it was decided to perform the bypass in agreement with the Institutional Vascular Review Board.
The IMax was selected as a donor’s vessel because of the small size of the STA and the need to revascularize the whole MCA territory, meaning that the blood supply needed to be higher than 15-40 ml/100g/min. According to previous reports, IMax provides between 60-95 ml/min/100g [23]. To localize the IMax artery, we selected the technique described by Peto et al. [10] because of the short time needed to expose the artery. The radial artery was selected as a graft because it has some advantages; 1) more appropriate diameter similar to the M2 segment of the MCA, avoiding a type- 2b error [14], 2) the lack of valves, 3) less possibility of kinking and 4), adequate length from the temporal fossa to the Sylvian fissure. In this case, the final length of the graft was 7 cm [14,17,18]. We decided to perform the bypass to the superior trunk of M2 to prioritize the flow to the precentral and central arteries, which were the ones that irrigated the motor and supplementary motor cortex.

Cut flow calculation

In addition, the cut flow was calculated before discharge using transcranial Doppler measurements. The calculated flow at the RAG was 334 ml/min, and the flow of the MCA was 288 ml/ml. According to Jonathan and Charbel [15], these values provide a cut flow index of 0.86, meaning that the bypass has an 83.1% long-term patency rate.
To our knowledge, this is the first case published using an IMax bypass to treat a complex systemic steno-occlusive disease with improved perfusion parameters (TTP, MTT, and rCBF). Although we are waiting for new results of clinical trials such as Carotid and Middle cerebral artery Occlusion Surgery Study (CMOSS) [7], this procedure has a physiologic and logical foundation, so it should not be discarded as an option for treatment.

CONCLUSIONS

The revascularization in steno-occlusive disease is indicated in carefully selected patients as the last bullet we can offer as treatment. The IMax bypass has proved to be a safe option in cases where total revascularization is needed and the ischemic area to treat is too large for the STA-MCA bypass.

NOTES

Disclosure

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Supplementary Video 1

The online-only data supplement is available with this article at https://doi.org/10.7461/jcen.2023.E2022.11.003
Supplementary Video 1

Fig. 1.
Imaging studies. (A-C) Preoperative time to peak (TTP), mean transit time (MTT), and regional cerebral blood volume (rCBV) perfusion MRI shows low perfusion in the right hemisphere. (D) MRI shows an area of a previous infarction in the right opercular area. (E-G) Postoperative TTP, MTT, and rCBV perfusion image without areas of hypoperfusion. (H) CT-angio shows the IMax-radial artery graft (RAG) end-to-end anastomosis (yellow arrow) and the end-to-side M2 anastomosis (white arrow). CT-angio, computed tomography angiography; IMax, internal maxillary artery
jcen-2023-e2022-11-003f1.jpg
Fig. 2.
Illustrative case. (A) Surgical planning for a pterional and transzygomatic approach. (B and C) Incision and dissection of the radial artery. (D) IMax to radial artery graft end-to-end anastomosis. (E) Radial artery to M2 end-to-side anastomosis. (F) Intraoperative fluorescein video angiography shows the IMax-M2 anastomosis with radial artery graft (white arrows) with adequate perfusion of the cerebral hemisphere. IMax, internal maxillary artery
jcen-2023-e2022-11-003f2.jpg
Fig. 3.
Sagittal view shows the IMax-radial artery graft (RAG) end-to-end anastomosis (yellow arrow) and the end-to-side M2 anastomosis (white arrow). IMax, internal maxillary artery
jcen-2023-e2022-11-003f3.jpg

REFERENCES

1. Abdulrauf SI, Sweeney JM, Mohan YS, Palejwala SK. Short segment internal maxillary artery to middle cerebral artery bypass: A novel technique for extracranial-to-intracranial bypass. Neurosurgery. 2011 Mar;68(3):804-8; discussion 808-9.
crossref pmid pdf
2. EC/IC Bypass Study Group. Results of an international randomized trial. N Engl J Med. 1985 Nov;313(19):1191-200.
crossref pmid
3. Feng X, Lawton MT, Rincon-Torroella J, El-Sayed IH, Meybodi AT, Benet A. The lateral triangle of the middle fossa: Surgical anatomy and a novel technique for transcranial exposure of the internal maxillary artery. Oper Neurosurg (Hagerstown). 2016 Jun;12(2):106-11.
pmid
4. Flaherty ML, Flemming KD, McClelland R, Jorgensen NW, Brown RD Jr. Population-based study of symptomatic internal carotid artery occlusion: Incidence and long-term follow-up. Stroke. 2004 Aug;35(8):e349-52.
pmid
5. JET Study Group. Japanese EC-IC bypass trial (JET study): The second interim analysis. Surg Cereb Stroke. 2002 30(6):434-7.
crossref
6. Jussen D, Zdunczyk A, Schmidt S, Rösler J, Buchert R, Julkunen P, et al. Motor plasticity after extra-intracranial bypass surgery in occlusive cerebrovascular disease. Neurology. 2016 Jul;87(1):27-35.
crossref pmid
7. Ma Y, Gu Y, Tong X, Wang J, Kuai D, Wang D, et al. The Carotid and Middle cerebral artery Occlusion Surgery Study (CMOSS): A study protocol for a randomised controlled trial. Trials. 2016 17(1):544.
crossref pmid pmc pdf
8. McKetton L, Venkatraghavan L, Rosen C, Mandell DM, Sam K, Sobczyk O, et al. Improved white matter cerebrovascular reactivity after revascularization in patients with steno-occlusive disease. AJNR Am J Neuroradiol. 2019 Jan;40(1):45-50.
crossref pmid pmc
9. Ning XJ, Gao Q, Chen C, Ling C, Liang JJ, Li ZY, et al. Effects of superficial temporal artery-middle cerebral artery bypass on hemodynamics and clinical outcomes in the patients with atherosclerotic stenosis in the intracranial segment of internal carotid artery and middle cerebral artery. Clin Neurol Neurosurg. 2019 Nov;186:105510.
crossref pmid
10. Peto I, Nouri M, Agazzi S, Langer D, Dehdashti AR. Pterygo-maxillary fissure as a landmark for localization of internal maxillary artery for use in extracranial-intracranial bypass. Oper Neurosurg (Hagerstown). 2020 Oct;19(5):e480-6.
crossref pmid pdf
11. Powers WJ, Clarke WR, Grubb RL Jr, Videen TO, Adams HP Jr, Derdeyn CP, et al. Extracranial-intracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia: The Carotid Occlusion Surgery Study randomized trial. JAMA. 2011 Nov;306(18):1983-92.
crossref pmid pmc
12. Reynolds MR, Derdeyn CP, Grubb RL Jr, Powers WJ, Zipfel GJ. Extracranial-intracranial bypass for ischemic cerebrovascular disease: What have we learned from the Carotid Occlusion Surgery Study? Neurosurg Focus. 2014 Jan;36(1):e9.
crossref pmid
13. Rodriguez Rubio R, Kola O, Tayebi Meybodi A, Tabani H, Feng X, Burkhardt JK, et al. Minimally invasive exposure of the maxillary artery at the anteromedial infratemporal fossa. Oper Neurosurg (Hagerstown). 2019 Jan;16(1):79-85.
pmid
14. See AP, Charbel FT. Bypass for flow-augmentation in atherosclerotic carotid occlusion: A review of the literature and career experience. J Neurosurg Sci. 2021 Jun;65(3):305-21.
crossref pmid
15. Stapleton CJ, Atwal GS, Hussein AE, Amin-Hanjani S, Charbel FT. The cut flow index revisited: Utility of intraoperative blood flow measurements in extracranial-intracranial bypass surgery for ischemic cerebrovascular disease. J Neurosurg Sci. 2019 Sep;1-5.
crossref pmid
16. Vrionis FD, Cano WG, Heilman CB. Microsurgical anatomy of the infratemporal fossa as viewed laterally and superiorly. Neurosurgery. 1996 Oct;39(4):777-85; discussion 785-6.
crossref pmid
17. Wang L, Cai L, Qian H, Song J, Tanikawa R, Lawton M, et al. Intracranial-intracranial bypass with a graft vessel: A comprehensive review of technical characteristics and surgical experience. World Neurosurg. 2019 May;125:285-98.
crossref pmid
18. Wang L, Lu S, Cai L, Qian H, Tanikawa R, Shi X. Internal maxillary artery bypass for the treatment of complex middle cerebral artery aneurysms. Neurosurg Focus. 2019 Feb;46(2):e10.
crossref pmid
19. Wessels L, Hecht N, Vajkoczy P. Patients receiving extracranial to intracranial bypass for atherosclerotic vessel occlusion today differ significantly from the COSS population. Stroke. 2021 Oct;52(10):e599-604.
crossref pmid
20. Wu L, Wu W, Tali ET, Yuh WT. Oligemia, penumbra, infarction: Understanding hypoperfusion with neuroimaging. Neuroimaging Clin N Am. 2018 Nov;28(4):599-609.
pmid
21. Yasargil MG, Yonekawa Y. Results of microsurgical extra-intracranial arterial bypass in the treatment of cerebral ischemia. Neurosurgery. 1977 Jul-Aug;1(1):22-4.
crossref pmid
22. Yu Z, Shi X, Qian H, Liu F, Zhou Z, Sun Y, et al. Internal maxillary artery to intracranial artery bypass: A case series of 31 patients with chronic internal carotid/middle cerebral arterial-sclerotic steno-occlusive disease. Neurol Res. 2016 May;38(5):420-8.
crossref pmid
23. Zaki Ghali MG, Srinivasan VM, Britz GW. Maxillary artery to intracranial bypass. World Neurosurg. 2019 Aug;128:532-40.
crossref pmid


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