11.1 Bypass Indication for Atherosclerotic Occlusive Diseases

Atherosclerosis is a common disease that leads to the progressive stenosis and occlusion of cerebral vessels. Patients with transient ischemic attacks (TIAs) and cerebral infarctions due to the atherosclerotic stenosis of the internal carotid artery (ICA) and its branches usually present with general atherosclerosis. Studies on the natural history of ICA stenosis indicate that the annual stroke rate after diagnosis may vary from 3 to 27% per year. ¹ Extracranial-intracranial (EC-IC) bypass aims to revascularize the affected hemisphere. New approaches for measuring brain blood flow and metabolism facilitate the selection of candidates in whom bypass surgery would probably improve outcome. Measurements of cerebral blood flow (CBF) and cerebrovascular resistance (CVR) by single-photon emission computed tomography (SPECT) (Fig. 11.1) were unified using stereotactic brain coordinates and three-dimensional stereotactic surface projections by Mizumura et al. ²

Hemodynamic compromise of ipsilateral artery occlusion is divided into three stages (stages 0–2) ³ based on CVR calculated from the CBF values at rest and during Diamox challenge (Table 11.1).

Stage 2, or misery perfusion, ⁴ is considered to serve as criteria for the indication for revascularization. In symptomatic major cerebral artery disease, misery perfusion remains a predictor of subsequent stroke. ⁵ However, certain quantitative determinations of misery perfusion by different approaches (e.g., arterial spin labeling, magnetic resonance imaging [MRI], SPECT, and positron emission tomography [PET]) are still being debated. Patients with atherosclerotic occlusion of main brain arteries who satisfy the following eligibility categories can be candidates for bypass surgery according to the Carotid Occlusion Surgery Study ⁶ and the Japanese EC-IC Bypass Trial (JET) ⁷ :

1. 
   

   Symptomatic ICA occlusion

   
   
2. 
   

   Symptomatic middle cerebral artery (MCA) occlusion or severe stenosis

   
   
3. 
   

   Age less than 73 years

   
   
4. 
   

   Rankin disability scale 1 or 2

   
   
5. 
   

   CBF less than 80% and CVR less than 10% (Fig. 11.1) (or PET criteria: contralateral oxygen extraction fraction [OEF] ratio in the MCA territory > 1.130)

   
   
6. 
   

   Angiographic confirmation of the ICA occlusion and presence of suitable intra- and extracranial vessels for anastomosis

Nevertheless, superficial temporal artery (STA) to MCA bypass plus best medical care failed to show more benefit than best medical care alone for the treatment of symptomatic intracranial occlusion in the JET ⁷ and the Carotid Occlusion Surgery Study. ⁶ The results of these studies have been interpreted by some authors as the end of the role for EC-IC bypass in the management of stroke. Although a general expansion of EC-IC bypass application in this population would not be supported by the results of trials, a selective subset of patients with medically refractory hemodynamic symptoms may obtain benefit from surgery with sufficiently low perioperative morbidity. ⁸

11.2 Illustrative Case 1: Atherosclerotic Internal Carotid Artery Occlusion

11.2.2 Examination

MRI showed old ischemic changes in the left hemisphere (Fig. 11.2). PET (O¹⁵ gas) before surgery showed stage 1 vasodilatory changes in the left cerebral hemisphere (Table 11.2).

Table 11.2 O¹⁵ gas and water PET brain examination in case 1

MCA cortical territory	Normal	Preoperative		Postoperative
		Left	Right	Left	Right
CBF (mL/100 g/min)	> 32	41.2	47.0	40.9	46.0
CMRO2 (mL/100 g/min)	> 2.3	2.98	3.10	2.75	2.77
OEF (%)	< 52	50.6	46.1	55.2	49.3
CBV (mL/100 g)	…	4.86	4.09	4.99	4.27
CBF/CBV	…	8.77	12.1	8.65	11.1
Diamox-activated CBF (mL/100 g/min)	…	36.4	54.9	43.0	55.1
CVR (%)	> 10.5	–11.7	16.8	5.0	19.7
Abbreviations: CBF, cerebral blood flow; CBV, cerebral blood volume; CMRO2, cerebral metabolic rate of oxygen; CVR, cerebrovascular reserve; MCA, middle cerebral artery; OEF, oxygen extraction fraction; PET, positron emission tomography. Note: Significant decrease in CVR was revealed on preoperative examination. Postoperative data showed increase of global OEF, probably due to anemia and improvement of CVR in left MCA territory. The abnormal left preoperative CVR value and the improved postoperative value are shown in bold for comparison.

11.3 Indications of Bypass for Moyamoya Disease and Moyamoya Syndrome

Moyamoya is a unique cerebrovascular disease of progressive stenosis of the bilateral terminal ICAs with development of rich arterial collaterals at the base of the brain. Moyamoya disease should be distinguished from moyamoya syndrome according to the diagnostic criteria. ⁹ Bypass surgery is indicated for both conditions.

Moyamoya disease is found mostly among Japanese and other Asian populations, with an annual prevalence of 6.03 to 10.5 cases per 100,000 individuals in Japan. ¹⁰ The distribution of the age of ischemic onset demonstrates two peaks, one at 5 to 9 years of age and a lower peak at 35 to 39 years of age, whereas distribution of the age of hemorrhagic onset demonstrates a peak at 25 to 50 years of age. ¹⁰ Moyamoya disease is clinically progressive in most cases with childhood onset and is also progressive in many adult-onset cases. The common clinical scenario is repeated TIAs, cerebral infarctions, and brain atrophy in children and intracerebral hemorrhages from abnormal dilated lenticulostriate arteries or microaneurysms of abnormal moyamoya vessels or saccular aneurysms in adults. The explanation for such clinical presentations can be obtained from Suzuki’s six-stage angiographic system of moyamoya disease. ¹¹ Moyamoya disease shows more rapid clinical and angiographic progression in children than in adults, so it should be treated as soon as possible. In pediatric patients, surgery is indicated even for the asymptomatic hemispheres because of a strong possibility that it will become symptomatic in the near future. In adults, however, close follow-up observation is recommended, because asymptomatic adults usually have a good prognosis without bypass. ¹² From the clinical point of view, many cases with stenosis of the arteries that form the circle of Willis can be difficult to distinguish from cases of moyamoya disease, so the term moyamoya syndrome was introduced. ¹³

Medical treatments have not been found to be effective in reversing the progression of arterial stenosis seen in moyamoya disease. Surgical treatment of moyamoya disease began in the mid-1970s when Yaşargil proposed anastomosis of the STA to a branch of the MCA. ¹⁴ EC-IC bypass can reverse the progression of ischemia when the ischemic state of the brain remains in a recoverable state. Surgical treatment is based on the clinical characteristics; anatomical findings on MRI, magnetic resonance angiography (MRA), computed tomography (CT), and angiography; and functional assessment of CBF with SPECT, PET, and acetazolamide challenge test. It is still controversial whether direct bypass is necessary for the treatment of moyamoya disease, because indirect revascularization is effective. Indeed, direct bypass between a small STA and a small MCA, especially in children, is not always easy and carries risk of perioperative complications. However, direct bypass is more reliable in reducing hemodynamic stress to the moyamoya vessels, and it is an indispensable procedure for adult patients. In fact, some authors reported no significant reduction of the rebleeding rate after bypass surgery, ¹⁵ so surgical treatment in adult hemorrhagic patients remains controversial. In rare cases with pronounced ischemia in anterior cerebral artery (ACA) territory, direct STA-ACA anastomosis is essential.

The treatment guidelines, published in 2009 ¹⁶ and 2012, ¹⁷ stated the effectiveness of direct bypass for both pediatric and adult cases. Optimal treatment of moyamoya disease is now widely accepted to require collateral formation in both the MCA and either ACA or posterior cerebral artery (PCA) territories. Multiple treatment choices that include combined direct and indirect bypass surgery are applied for most pediatric cases of moyamoya disease. ¹⁸

During the first month after bypass, approximately 30% of patients exhibit TIA. However, symptoms usually improve thereafter. ^{19 ,​ 20}

11.4 Illustrative Case 2: Moyamoya Disease

11.4.2 Examination

On examination, the patient had mild weakness of the left arm and leg (4/5 on the Medical Research Council Scale for Muscle Strength). Imaging revealed evidence of right cerebral vascular accidents, severe hypoperfusion of the right cerebral hemisphere, and stenosis of the right internal carotid artery consistent with moyamoya disease (Fig. 11.3). ²¹

11.5 Indications for Bypass in Complex and Giant Aneurysms

Arterial intracranial aneurysms are lesions with potentially devastating consequences. The goal of treating any aneurysm is to prevent bleeding by exclusion of the aneurysm from circulation. The most common treatment strategies for intracranial arterial aneurysms include endovascular occlusion and microsurgical clipping. Both treatments have their pros and cons. In certain situations, such as giant blister-like ²² or dissecting aneurysms, proximal occlusion or trapping of the parent artery is required. If a dramatic decrease in blood flow after trapping is suspected, or if the balloon test occlusion documents that the patient may not tolerate permanent parent artery occlusion, bypass surgery should be considered prior to trapping to prevent ischemia. Patients with such complicated aneurysms who need vascular reconstruction are rare. ^{23 ,​ 24 ,​ 25 ,​ 26} Attempts of bypass application for treatment of difficult cerebral aneurysms have increased since Yaşargil introduced microvascular techniques in neurosurgery, but the first “high-flow” bypass was performed without a microscope and was reported by Lougheed et al ^{27 ,​ 28} in 1971. Sato and Kadoya ²⁹ mentioned application of saphenous vein grafts beginning in 1974 for occlusive disease, traumatic occlusion of the ICA, and intracranial aneurysms. In 1979, Iwabuchi et al ³⁰ reported a case of a giant ICA aneurysm treated with a long-vein bypass graft and trapping of the ICA. Many different techniques and nuances in high-flow bypass exist throughout the neurosurgical centers in the world. In recent published articles on EC-IC bypass application for the treatment of patients with complex intracranial aneurysms, good graft patency rates were achieved with low surgical morbidity and mortality. ^{23 ,​ 31}

11.6 Illustrative Case 3: Giant Arterial Aneurysm

11.6.1 History

A 7-year-old boy presented with headache and lethargy. His medical history was unremarkable, and he was otherwise healthy (Fig. 11.4).

Related posts:

1 The Philosophy of Microsurgical Practice: Four Founding Principles Inherited from the Great Thinkers 2 Day 1: The Organization of the Microsurgical Laboratory: Necessary Tools and Equipment 8 Day 7: Models for Microneurosurgical Training and Schedules for Training 3 Day 2: Dry-Laboratory Microsurgical Training: Techniques and Manual Skills 7 Day 6: Exercises: Kidney Autotransplantation, Supermicrosurgery, and Aneurysm Clipping 10 Translation of Laboratory Skills: Indications for Bypass in Neurosurgery

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