Computed tomographic perfusion in assessing postoperative revascularization in moyamoya disease

1. Introduction 

Moyamoya is a cerebrovascular disease causing progressive occlusion of the supraclinoid internal carotid arteries and subsequently, the proximal middle and anterior cerebral arteries [1], [2], [9], [13]. In the United States and Korea, there appears to be a bimodal distribution with one pediatric group in the first decade of life and another adult group with patients in their 30s and 40s [4], [10], [17]. Once the diagnosis of moyamoya has been made, the goal is for prompt treatment to prevent an ischemic or hemorrhagic event via a direct or indirect procedure [2]. At our institution, we use a direct anastomosis via superficial temporal artery (STA) to middle cerebral artery (MCA) bypass for moyamoya in adults to provide additional collateral blood flow to hypoperfused areas [1], [5].

Although there is no standard treatment of moyamoya, there is also no standard method for assessing cerebral blood flow (CBF) postoperatively or even bypass patency. Many modalities can be used as follows: single photon emission computed tomography (SPECT) [6], [7], [8], [11], positron emission tomography (PET) [3], xenon computed tomography, cerebral angiography [6], [18], computed tomographic perfusion (CTP) [9], and magnetic resonance brain perfusion (MRP). Our purpose in this study is to evaluate the use of CTP as an imaging modality to assess revascularization after STA to MCA bypass; a more expeditious and less expensive alternative to the aforementioned imaging techniques.

2. Methods 

We received institutional review board approval to perform a retrospective review of the charts of a series of 5 female patients (mean age, 35; range, 20-50) who underwent STA-MCA bypass for ischemic stroke or transient ischemic attack (TIA).

Preoperatively, all patients showed clinically significant hypoperfusion in the MCA territory. Indications for surgery included history of stroke or TIA and MCA hypoperfusion on CTP. All of the patients also had moyamoya disease. All surgeries were performed by the senior author and there were no periprocedural complications. Preoperative computed tomographic angiography (CTA) was done initially to identify moyamoya disease; cerebral angiography was done to assess STA size and patency and to confirm the diagnosis of moyamoya. Preoperative and postoperative CTP was performed to assess improvement after the bypass. Computed tomographic angiography was done postoperatively with the CTP to assess bypass patency as well. Cerebral angiography was done in one patient postoperatively.

Although there can be disease within the posterior circulation in moyamoya patients, previous studies have recommended the use of vessels of the posterior circulation as a reference point to prevent greater error in the data sets [9]. As such, we used the posterior circulation as reference points in this study when reading the CTP. Mean transit time (MTT), cerebral blood volume (CBV), and CBF were calculated. In addition, a comparison of the absolute values before and after treatment was made using a paired t test. P < .05 was considered a statistically significant difference.

3. Results 

Table 1 gives an overview of all patients characteristics and revascularization procedures. Clinically, all patients did well postoperatively. During the follow-up period (mean, 18 months), 3 patients continued to be asymptomatic, 1 patient's hemiparesis improved, and another patient's hemiparesis improved but she remained aphasic (mean GOS, 4.5). To date, no MCA strokes or TIAs were observed or reported.

Table 1. Patient characteristics and revascularization procedures

	Patient	Age/sex	Preoperative symptoms	Postoperative symptoms	Anastomosis	Postoperative perfusion	Postoperative stroke
	1	33/female	Left hemiparesis	Improved left-sided strength	Right STA-MCA bypass	Improved	No
	2	50/female	Minimal sensory changes	Unchanged	Left STA-MCA bypass	Improved	No
	3	36/female	Asymptomatic, history of stroke	Unchanged	Right STA-MCA bypass	Improved	No
	4	38/female	Asymptomatic, history of stroke	Unchanged	Left STA-MCA bypass	Improved	No
	5	20/female	Right hemiparesis, aphasia	Hemiparesis improved, aphasia unchanged	Left STA-MCA bypass	Improved	No

Preoperatively, all patients showed clinically significant hypoperfusion in the MCA territory on CTP. The postoperative CTA images clearly demonstrate patency of the bypass and restoration of flow, particularly in the MCA distribution. The CTPs were typically performed at greater than 6 months postoperatively (range, 6-24 months; mean, 12 months). In the actual perfusion parameters, the CTP showed some significant differences in the symptomatic hemisphere. In particular, the CBF increased from 67.6 ± 4.9 (mL/100 g per minute) before to 92.3 ± 13.3 (mL/100 g per minute) after surgical revascularization (P < .05). In addition, the MTT decreased from 6.53 ± 0.75 seconds before to 4.16 ± 1.0 seconds after treatment (P < .05). There were no other significant differences in the absolute perfusion parameters (P > .05) (see Table 2).

Table 2. Absolute CT perfusion data (mean, SD, and P Value) for the symptomatic hemisphere

	Time of measurement	MTT (s)	CBV(mL/100 g)	CBF(mL/100g per minute)
	Before treatment	6.53 ± .075	4.53 ± .55	67.6 ± 4.93
	After treatment	4.16 ± 1.0	2.96 ± .92	92.3 ± 13.2
	P	.03	.065	.039

3.1. Illustrative case 

A 33-year-old female with a history of moyamoya, multiple strokes refractory to medication, and left hemiparesis underwent a right STA-MCA bypass. Fig. 1 is the patient's lateral cerebral angiogram preoperatively which shows an occlusion of the right internal carotid artery at approximately the ophthalmic segment as well as the characteristic “puff of smoke” seen in moyamoya patients. Fig. 2 is the patient's CTP preoperatively which shows a perfusion deficit of the right hemisphere demonstrated by diminished CBF and prolonged MTT with relatively symmetric CBV. Please note that the patient did have a history of bifrontal strokes which is illustrated by the decreased CBV in these areas. Fig. 3, Fig. 4 demonstrate the CTA 1 week postoperative; both views show a patent bypass. The postoperative cerebral angiogram can be seen in Fig. 5A and B. These angiograms were done at the patient's 1-year follow-up and show good revascularization within the MCA distribution from 2 branches of the STA. And most important, Fig. 6 shows the improvement in the perfusion postoperatively with hemispheric symmetry in the CBV, CBF, and MTT. Neurologically, the patient's hemiparesis improved with no new evidence of stroke.

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Fig. 1. Preoperative lateral cerebral angiogram. A 33-year-old female with history of moyamoya, multiple strokes refractory to medication, and left hemiparesis. Note the occlusion of the right internal carotid artery at approximately the ophthalmic segment (straight arrow) as well as the characteristic “puff of smoke” seen in moyamoya patients (curved arrow).

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Fig. 2. Preoperative CTP. Same patient's CTP shows diminished CBF (bottom left) and prolonged MTT (bottom right) with relatively symmetric CBV (top right) consistent with a perfusion deficit of the right hemisphere. Please note that the patient did have a history of bifrontal strokes illustrated by the diminished CBV in the frontal regions.

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Fig. 3. Postoperative CTA. Imaging of the same patient after right STA-MCA bypass at 1 week postoperative demonstrating patent bypass from STA to MCA (arrow) from superficial view.

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Fig. 4. Postoperative CTA. Same patient's CTA illustrating patent STA-MCA bypass (arrow) from deep view at 1 week postoperative.

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Fig. 5. A: Postoperative lateral cerebral angiogram. Imaging of the same patient postoperatively demonstrating patent bypass (arrows) during early arterial phase. B: Postoperative lateral cerebral angiogram. Imaging of the same patient postoperatively demonstrating patent bypass (arrow) during second half of arterial phase.

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Fig. 6. Postoperative CTP. Same patient's imaging representing patent bypass. Note the hemispheric symmetry in the CBV (top right), CBF (bottom left), and MTT (bottom right) consistent with improvement of perfusion. More pronounced is the poor perfusion in the bifrontal regions from the patient's old strokes. Neurologically, the patient's hemiparesis improved with no new evidence of stroke.

4. Discussion 

A successful bypass in the treatment of moyamoya can prevent neurologic deficits and TIAs that will burden these patients [5], [9], [11]. The postoperative evaluation of the STA-MCA bypass has evolved for the last several years. Wanebo et al [15] recommend following 4 key areas: functional neurologic status, neurocognitive status, bypass patency, and status of CBF and perfusion, with the first two being the most important from a clinical standpoint. At the same time, assessment of the latter two serves to ensure technical success and continued patient improvement or stability [15].

Although others have advocated the use of PET, xenon CT, or SPECT for evaluating CBF after bypass surgery [6], [11], their lack of availability and inadequate data have limited their use. In addition, studies have shown good correlation between CTP and the data provided by these more difficult studies [9]. Our article focuses on assessment of cerebral flow and perfusion with CTP that is much more available and provides quantitative data. In cost, Table 3 clearly demonstrates a reduced cost of CTP relative to MRP and cerebral angiography at our institution. All of the above illustrate the benefits of using CTP over other modalities.

Table 3. Cost of various perfusion modalities

		Totalbilled	Proceduretime (min)	Contrast media used
	CTP(noncontrast CT + CTP)	$6500	25	150 mL Omnipaque350
	MRP(MRI + MRA + MRP)	$9000	105	20 mL gadolinium
	3-Vessel catheter angiography	$8000	60	100 mL Omnipaque300

Using the proper technique, CTP can also be used as a CTA to assess bypass patency. Although this is easily done intraoperatively via various modalities such as Doppler, ultrasound, fluorescent videoangiography, or cerebral angiography, the latter is considered to be the gold standard [16]. Angiography has been done in the past, although some have recommended physical examination and Doppler ultrasonography to be as effective [12]. The 3-dimensional imaging that can be obtained via CTA may be a less invasive replacement to conventional angiography while still allowing follow-up of bypass patency. In addition, in moyamoya patients where a simple burr hole or dural opening could enhance collateral flow, improvement in the CTP may in itself be an indication of improved bypass patency although it would be difficult to see on conventional CTA. This is especially important in the pediatric population where indirect approaches such as encephaloduroarteriosynangiosis (EDAS), encephalomyosynangiosis (EMS), encephalomyoarteriosynangiosis (EMAS), burr holes with anastomosis, and dural splitting are often used due to the small caliber of the pediatric cerebral vasculature [10].

One limitation of the study is the optimal method to interpret the data. The CTP data calculates CBV and MTT and then uses this data to calculate CBF (CBF = CBV/MTT). The question is whether to use the absolute data or relative data. Absolute data represent the numerical value given for the above values. Relative data represent the symptomatic hemisphere data compared to the asymptomatic hemisphere data. Waaijer et al [14] performed a study that answered this question after carotid endarterectomies that stated that the relative data produced a more statistically significant change, but whether this can be transferred to the STA-MCA bypass remains to be seen.

Other limitations to the study are the possibility of variability in physiology, contrast timing, and postprocessing. Also, there is no definitive reference data with which to compare our absolute values. In addition, the variable timing of the postoperative CTP may have affected our results. Moyamoya disease is a progressive disease, even in adult cases, and therefore, progression of the disease even postoperatively may affect later perfusion studies. Whether the improvement in perfusion due to synangiosis outweighs the progression of disease and how these will be reflected in CTP done several years postoperatively remain to be seen. And finally, given the relatively short follow-up—the mean CTP was done at 1 year—it is difficult to determine the true long-term changes seen with this procedure. Given that all patients are continuing to do well, it is safe to assume that their cerebral perfusion has not diminished.

5. Conclusion 

This study demonstrates that CTP, a more convenient and less expensive imaging test than other available options, can provide an assessment of CBF after cerebral bypass that appears to correlate with postoperative clinical and angiographic findings. In addition, in this small series of moyamoya patients, STA-MCA bypass appeared to prevent recurrent TIAs and strokes.