Chronological evaluation of Cerebral Hemodynamics by Dynamic Susceptibility Contrast Magnetic Resonance Imaging after Indirect Bypass Surgery for Moyamoya Disease
Yosuke Ishii1,2, Tadashi Nariai1, Yoji Tanaka1, HIroshi Aihara2, Yoshio Suyama2, Shinichi Wakabayashi2, and Taketoshi Maehara1

1Neurosurgery, Tokyo Medial and Dental University, Tokyo, Japan, 2Neurosurgery, Suiseikai Kajikawa Hospital, Hiroshima, Japan

Synopsis

We used dynamic susceptibility contrast (DSC)-MRI to evaluate the chronological changes in hemodynamics after indirect bypass surgery for moyamoya disease. Twenty five patients who underwent indirect bypass surgery and repeated DSC–MRI measurement within the first 6 postoperative months were included. We analyzed mean transit time (MTT) delay using the cerebellum as control. Mean MTT delay in the anterior circulation area gradually decreased soon after surgery and stabilized after 3 postoperative months. Postoperative MTT delay values were significantly decreased compared with preoperative values from 1 to 2 weeks onwards. These results suggested DSC–MRI detected angiogenesis during the early postoperative stages.

Purpose

Indirect bypass surgery has been demonstrated to be an effective method for treating moyamoya disease of ischemia onset. To date, however, the chronological hemodynamic changes after indirect bypass surgery have not been clarified. At our department, we previously have reported the cerebral hemodynamics of patients with moyamoya disease using Xe-CT, PET and DSC-MRI.1-4 On performing dynamic susceptibility contrast magnetic resonance imaging (DSC–MRI), in one of these papers, we reported the area with PET measured abnormally elevated oxygen extraction fraction corresponded well the that prolonged mean transit time (MTT) of more than 2 seconds in comparison to control region.3 In the present study, we used DSC–MRI to evaluate the chronological changes in hemodynamics after indirect bypass surgery.

Methods

A total of 57 patients with moyamoya disease underwent indirect bypass surgery at our department from April 2005 and to March 2009; of them, 25 patients (38 surgical sites; mean age, 14.7 ± 11.1 years; 16 females) who underwent repeated DSC–MRI measurement within the first 6 postoperative months were analyzed in the present study. DSC–MRI was performed with a Magnetom Vision 1.5-T MR unit (Siemens Medical System, Erlangen, Germany). The DSC–MRI data were evaluated by pixel-based numerical integration analysis, and the measured data were used to calculate the relative MTT. The relative MTT was calculated directly from the time-ΔR2*curve. The ROIs were placed on the cortical rim (frontal, temporal, parietal, and rolandic areas) that are perfused by internal carotid arteries and upper cortex of the cerebellum, away from the infarcted areas. We called the difference of MTT between the target regions and the control region (cerebellum) the MTT delay and investigated its chronological change .

Results

Mean MTT delay in the anterior circulation area gradually decreased soon after surgery and stabilized after 3 postoperative months (Fig. 1A). The preoperative mean MTT delay was 2.1 ± 1.0 s; the postoperative mean MTT delay was 1.8 ± 1.2 s at week 1, 1.6 ± 1.0 s at weeks 1–2, 1.6 ± 0.7 s at weeks 2–4, 1.3 ± 0.7 s at months 1–2, 0.88 ± 0.38 s at months 2–3, and 0.87 ± 0.50 s at months 3–6. Therefore, on analyzing the abovementioned values, postoperative mean MTT delay values significantly decreased compared with preoperative values from 1 to 2 weeks onwards (Fig. 1B). On comparing local MTT delay among several sites, MTT delay that occurred significantly earlier was markedly decreased in the rolandic area, where the indirect bypass was commonly applied (Fig. 2). Next, we compared a group of subjects in whom preoperative MTT delay was prolonged by at least 2 s with a group of patients in whom preoperative MTT delay was prolonged by less than 2 s (Fig. 3); postoperative MTT delay more markedly decreased in the former group. No significant difference was noted between the two groups after 3 postoperative months. Although decreases in MTT delay were slightly less marked in adult cases than in pediatric cases, no significant differences were noted between the two age groups at any of the time periods (Fig. 4).

Discussion

In the previous report that analyzed the development of collateral circulation after indirect bypass surgery using cerebral angiography or magnetic resonance angiography (MRA), authors discussed that it takes approximately 3 months before collateral circulation is established.5 However, in an experimental study that was conducted on pigs cerebral ischemia model, angiogenesis at the operated field was established on week after surgery, and arteriogenesis to anastomose between external carotid artery and arterioles on the brain surface was established 1 month after surgery.6 From these reports, it was suggested that minimal angiogenesis started soon after surgery, which was consistent with the process of developing into arteriogenesis that could be confirmed by macroscopic evaluation modalities such as angiography or MRA. In the present investigation using DSC–MRI, hemodynamic changes after indirect bypass surgery gradually progressed soon after surgery and continued for approximately 3 months, rather than progressing rapidly during a particular time period. Taken the previous reports and the present results, it was suggested that DSC-MRI detected the minimal change of cerebral hemodynamics by angiogenesis at the early time point after surgery. And also, DSC-MRI could evaluate the temporal changes of cerebral hemodynamics, which could contribute to manage the patients who have indirect bypass surgery.

Conclusion

Although it may take 3–4 months after indirect bypass surgery, till angiographically detectable collateral flow develop, amelioration of cerebral hemodynamic begin as early as 1–2 weeks postoperatively and gradually improve for approximately 3 months thereafter. These results suggested that DSC–MRI detected angiogenesis and arteriogenesis that occurred in early postoperative stages.

Acknowledgements

No acknowledgement found.

References

1.Nariai T, Suzuki R, Matsushima Y, et al. Surgically induced angiogenesis to compensate for hemodynamic cerebral ischemia. Stroke. 1994;25(5):1014-1021.

2. Nariai T, Matsushima Y, Imae S, et al. Severe haemodynamic stress in selected subtypes of patients with moyamoya disease: a positron emission tomography study. J Neurology Neurosurg Psychiatry. 2005;76(5):663-669.

3. Tanaka Y, Nariai T, Nagaoka T, et al. Quantitative evaluation of cerebral hemodynamics in patients with moyamoya disease by dynamic susceptibility contrast magnetic resonance imaging--comparison with positron emission tomography. J Cerebral Blood Flow Metab. 2006;26(2):291-300.

4. Ishii Y, Nariai T, Tanaka Y, et al. Practical clinical use of dynamic susceptibility contrast magnetic resonance imaging for the surgical treatment of moyamoya disease. Neurosurgery. 2014;74(3):302-309.

5. Houkin K, Nakayama N, Kuroda S, et al. How does angiogenesis develop in pediatric moyamoya disease after surgery? A prospective study with MR angiography. Childs Nerv Syst. 2004;20(10):734-741.

6. Nakamura M, Imai H, Konno K, et al. Experimental investigation of encephalomyosynangiosis using gyrencephalic brain of the miniature pig: histopathological evaluation of dynamic reconstruction of vessels for functional anastomosis. Laboratory investigation. J Neurosurg Pediatr. 2009;3(6):488-495.

Figures

Fig.1

(A) Chronologic changes in mean MTT delay in the anterior circulation area.

(B) Mean MTT delay in the anterior circulation area at each time period.

*: Decreased significantly compared with preoperative values (p < 0.05)


Fig.2

(A) Chronological changes in local MTT delay.

(B) Local MTT delay at each time period.


Fig.3

(A) Comparison of chronologic changes in postoperative MTT delay between the two groups using the preoperative MTT delay.

(B) Comparison of postoperative MTT delay at different time periods between the two groups using the preoperative MTT delay.

*: significant difference noted between the two groups (p < 0.05).


Fig.4

(A) Comparison of chronological changes in postoperative MTT delay according to age.

(B) Comparison of postoperative MTT delay with regard to time period and age. No significant differences were noted between the two groups at any of the time periods.




Proc. Intl. Soc. Mag. Reson. Med. 24 (2016)
0606