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Improvement in cognitive decline after indirect bypass surgery in adult moyamoya disease: implication of 15O-gas positron emission tomography

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Abstract

Purpose

To investigate the characteristics of patients with moyamoya disease (MMD) who show improvement in their cognitive decline after bypass surgery by analyzing the hemodynamic and metabolic parameters of 15O-gas positron emission tomography (PET).

Materials and methods

We retrospectively analyzed adult patients with MMD who were evaluated with PET and cognitive tests before and approximately one year after indirect bypass surgery. The PET parameters of the left Rolandic area were compared between patients who did and did not show improvement in their cognitive decline.

Results

Of the 19 patients analyzed, fourteen (74%) showed improvement in either the verbal or performance intelligence quotient (VIQ or PIQ). Three out of four patients with perioperative infarction experienced significant cognitive decline. The preoperative oxygen extraction fraction (OEF) was significantly higher in patients who showed improvement in their cognitive decline in terms of the PIQ than in those patients who did not (P = 0.03). The postoperative increase in the cerebral metabolic rate of oxygen (CMRO2) was significantly higher in patients who showed improvement in their cognitive decline in terms of the VIQ than in those who did not (P = 0.02).

Conclusion

Adult patients with MMD might show improvement in their cognitive decline after successful indirect bypass surgery if they have a severely increased regional OEF before the surgery and an increased regional CMRO2 after the surgery.

Clinical trial registration

URL: https://www.umin.ac.jp/ctr/. Unique identifier: UMIN000027949.

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References

  1. Kuroda S, Houkin K. Moyamoya disease: current concepts and future perspectives. Lancet Neurol. 2008;7(11):1056–66.

    Article  Google Scholar 

  2. Piao R, Oku N, Kitagawa K, Imaizumi M, Matsushita K, Yoshikawa T, et al. Cerebral hemodynamics and metabolism in adult moyamoya disease: comparison of angiographic collateral circulation. Ann Nucl Med. 2004;18(2):115.

    Article  Google Scholar 

  3. Weinberg DG, Rahme RJ, Aoun SG, Batjer HH, Bendok BR. Moyamoya disease: functional and neurocognitive outcomes in the pediatric and adult populations. Neurosurg Focus. 2011;30(6):E21.

    Article  Google Scholar 

  4. Festa JR, Schwarz LR, Pliskin N, Cullum CM, Lacritz L, Charbel FT, et al. Neurocognitive dysfunction in adult moyamoya disease. J Neurol. 2010;257(5):806–15.

    Article  Google Scholar 

  5. Kazumata K, Tha KK, Narita H, Kusumi I, Shichinohe H, Ito M, et al. Chronic ischemia alters brain microstructural integrity and cognitive performance in adult moyamoya disease. Stroke. 2015;46(2):354–60.

    Article  CAS  Google Scholar 

  6. Hara S, Hori M, Murata S, Ueda R, Tanaka Y, Inaji M, et al. Microstructural damage in normal-appearing brain parenchyma and neurocognitive dysfunction in adult moyamoya disease. Stroke. 2018;49:2504–7.

    Article  Google Scholar 

  7. Hosoda C, Nariai T, Ishiwata K, Ishii K, Matsushima Y, Ohno K. Correlation between focal brain metabolism and higher brain function in patients with Moyamoya disease. Int J Stroke. 2010;5(5):367–73.

    Article  Google Scholar 

  8. Zeifert PD, Karzmark P, Bell-Stephens TE, Steinberg GK, Dorfman LJ. Neurocognitive performance after cerebral revascularization in adult moyamoya disease. Stroke. 2017;48(6):1514–7.

    Article  Google Scholar 

  9. Lee JY, Phi JH, Wang KC, Cho BK, Shin MS, Kim SK. Neurocognitive profiles of children with moyamoya disease before and after surgical intervention. Cerebrovasc Dis. 2011;31(3):230–7.

    Article  Google Scholar 

  10. Wityk RJ, Hillis A, Beauchamp N, Barker PB, Rigamonti D. Perfusion-weighted magnetic resonance imaging in adult moyamoya syndrome: characteristic patterns and change after surgical intervention: case report. Neurosurgery. 2002;51(6):1499–506.

    Article  Google Scholar 

  11. Kazumata K, Tha KK, Tokairin K, Ito M, Uchino H, Kawabori M, et al. Brain structure, connectivity, and cognitive changes following revascularization surgery in adult moyamoya disease. Neurosurgery. 2019

  12. Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo) 2012;52(5):245–66.

  13. Matsushima Y, Fukai N, Tanaka K, Tsuruoka S, Inaba Y, Aoyagi M, et al. A new surgical treatment of moyamoya disease in children: a preliminary report. Surg Neurol. 1981;15(4):313–20.

    Article  CAS  Google Scholar 

  14. Aoyagi M, Tanaka Y, Tamura K, Maehara T, Nariai T, Ohno K. Vasculrrized flap with multiple small dural opening in patients with Moyamoya disease with hemodynamic impariments in the posterior circulation. Video J Neurosurg. 2007;15(4).

  15. Nariai T. Treatment of moyamoya disease using indirect bypass surgery. In: Saito N, editor. Prime neurosurgery 2. Miwa: Cerebral Ischemia; 2017. p. 81–87.

    Google Scholar 

  16. Nariai T, Suzuki R, Matsushima Y, Ichimura K, Hirakawa K, Ishii K, et al. Surgically induced angiogenesis to compensate for hemodynamic cerebral ischemia. Stroke. 1994;25(5):1014–21.

    Article  CAS  Google Scholar 

  17. Hara S, Tanaka Y, Ueda Y, Hayashi S, Inaji M, Ishiwata K, et al. Noninvasive evaluation of CBF and perfusion delay of moyamoya disease using arterial spin-labeling MRI with multiple postlabeling delays: comparison with 15O-gas PET and DSC-MRI. AJNR Am J Neuroradiol. 2017;38(4):696–702.

    Article  CAS  Google Scholar 

  18. Ishii Y, Tanaka Y, Momose T, Yamashina M, Sato A, Wakabayashi S, et al. Chronologic evaluation of cerebral hemodynamics by dynamic susceptibility contrast magnetic resonance imaging after indirect bypass surgery for moyamoya disease. World Neurosurg. 2017;108:427–35.

    Article  Google Scholar 

  19. Hosoda C, Nariai T, Kawasaki K, Ishiwata K, Ishii K, Inaji M, et al. Altered correlation between intelligence quotient and PET measured cerebral metabolism induced by surgical revascularization in patients with Moyamoya disease, In: Abstracts of the 13th Annual Meeting of the Organization for Human Brain Mapping (2007). Neuroimage. 2007;36(Supplement 1):e1.

  20. Fujita K, Maekawa H, Dairoku H, Yamanaka K. Assessment cases and clinical researches using Japanese version of WAIS-III: Nihon Bunka Kagakusha; 2011. iv, 278 pp.

  21. Dairoku H. Secular change in: Assesment case series using WISC-III: theory and practice. Kazuhiro F, Kazuhiko U, Hisao M, Toshiyuki I, Hitoshi D, editors: Nihon Bunka Kagakusya; 2005. v, 362 pp.

  22. Senda M, Buxton RB, Alpert NM, Correia JA, Mackay BC, Weise SB, et al. The 15O steady-state method: correction for variation in arterial concentration. J Cereb Blood Flow Metab. 1988;8(5):681–90.

    Article  CAS  Google Scholar 

  23. Sadato N, Yonekura Y, Senda M, Iwasaki Y, Matoba N, Tamaki N, et al. PET and the autoradiographic method with continuous inhalation of oxygen-15-gas: theoretical analysis and comparison with conventional steady-state methods. J Nucl Med. 1993;34(10):1672–80.

    CAS  PubMed  Google Scholar 

  24. Iida H, Kanno I, Miura S, Murakami M, Takahashi K, Uemura K. Error analysis of a quantitative cerebral blood flow measurement using H2(15)O autoradiography and positron emission tomography, with respect to the dispersion of the input function. J Cereb Blood Flow Metab. 1986;6:536–45.

    Article  CAS  Google Scholar 

  25. Lammertsma AA, Jones T. Correction for the presence of intravascular oxygen-15 in the steady-state technique for measuring regional oxygen extraction ratio in the brain: 1. Description of the method. J Cereb Blood Flow Metab. 1983;3(4):416–24.

    Article  CAS  Google Scholar 

  26. Mintun MA, Raichle ME, Martin WR, Herscovitch P. Brain oxygen utilization measured with O-15 radiotracers and positron emission tomography. J Nucl Med. 1984;25(2):177–87.

    CAS  PubMed  Google Scholar 

  27. Nariai T, Matsushima Y, Imae S, Tanaka Y, Ishii K, Senda M, et al. Severe haemodynamic stress in selected subtypes of patients with moyamoya disease: a positron emission tomography study. J Neurol Neurosurg Psychiatry. 2005;76(5):663–9.

    Article  CAS  Google Scholar 

  28. Tanaka Y, Nariai T, Nagaoka T, Akimoto H, Ishiwata K, Ishii K, 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 Cereb Blood Flow Metab. 2006;26(2):291–300.

    Article  Google Scholar 

  29. Baek HJ, Chung SY, Park MS, Kim SM, Park KS, Son HU. Preliminary study of neurocognitive dysfunction in adult moyamoya disease and improvement after superficial temporal artery-middle cerebral artery bypass. J Korean Neurosurg Soc. 2014;56(3):188–93.

    Article  CAS  Google Scholar 

  30. Yanagihara W, Chida K, Kobayashi M, Kubo Y, Yoshida K, Terasaki K, et al. Impact of cerebral blood flow changes due to arterial bypass surgery on cognitive function in adult patients with symptomatic ischemic moyamoya disease. J Neurosurg. 2018:1–9.

  31. Karzmark P, Zeifert PD, Bell-Stephens TE, Steinberg GK, Dorfman LJ. Neurocognitive impairment in adults with moyamoya disease without stroke. Neurosurgery. 2012;70(3):634–8.

    Article  Google Scholar 

  32. Karzmark P, Zeifert PD, Tan S, Dorfman LJ, Bell-Stephens TE, Steinberg GK. Effect of moyamoya disease on neuropsychological functioning in adults. Neurosurgery. 2008;62(5):1048–51.

    Article  Google Scholar 

  33. Calviere L, Yan Kai G, Catalaa I, Marlats F, Bonneville F, Larrue V. Executive dysfunction in adults with moyamoya disease is associated with increased diffusion in frontal white matter. J Neurol Neurosurg Psychiatry. 2012;83(6):591–3.

    Article  Google Scholar 

  34. Kazumata K, Tha KK, Uchino H, Ito M, Nakayama N, Abumiya T. Mapping altered brain connectivity and its clinical associations in adult moyamoya disease: a resting-state functional MRI study. PLoS ONE. 2017;12(8):e0182759.

    Article  Google Scholar 

  35. Powers WJ. Cerebral hemodynamics in ischemic cerebrovascular disease. Ann Neurol. 1991;29(3):231–40.

    Article  CAS  Google Scholar 

  36. Fujimura M, Mugikura S, Kaneta T, Shimizu H, Tominaga T. Incidence and risk factors for symptomatic cerebral hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in patients with moyamoya disease. Surg Neurol. 2009;71(4):442–7.

    Article  Google Scholar 

  37. Kazumata K, Tha KK, Uchino H, Shiga T, Shichinohe H, Ito M, et al. Topographic changes in cerebral blood flow and reduced white matter integrity in the first 2 weeks following revascularization surgery in adult moyamoya disease. J Neurosurg. 2017;127(2):260–9.

    Article  CAS  Google Scholar 

  38. Nanba T, Ogasawara K, Nishimoto H, Fujiwara S, Kuroda H, Sasaki M, et al. Postoperative cerebral white matter damage associated with cerebral hyperperfusion and cognitive impairment after carotid endarterectomy: a diffusion tensor magnetic resonance imaging study. Cerebrovasc Dis. 2012;34(5–6):358–67.

    Article  Google Scholar 

  39. Leblanc R, Tyler JL, Mohr G, Meyer E, Diksic M, Yamamoto L, et al. Hemodynamic and metabolic effects of cerebral revascularization. J Neurosurg. 1987;66(4):529–35.

    Article  CAS  Google Scholar 

  40. Hara S, Hori M, Ueda R, Hayashi S, Inaji M, Tanaka Y, et al. Unraveling specific brain microstructural damage in moyamoya disease using diffusion magnetic resonance imaging and positron emission tomography. J Stroke Cerebrovasc Dis. 2019;28(4):1113–25.

    Article  Google Scholar 

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Acknowledgments

This work was supported by Grant-in-Aid for Scientific Research “KAKENHI”, Japan Society for the Promotion of Science (Grant no. 26305031).

Funding

Grant-in-Aid for Scientific Research “KAKENHI”, Japan Society for the Promotion of Science (Grant no. 26305031) given to Tadashi Nariai.

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Authors and Affiliations

  1. Department of Neurosurgery, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo, 113-8519, Japan

    Shoko Hara, Takumi Kudo, Shihori Hayashi, Motoki Inaji, Yoji Tanaka, Taketoshi Maehara & Tadashi Nariai

  2. Department of Radiology, Juntendo University, 2-1-1 Hongo, Bunkyo-ku, Tokyo, Japan

    Shoko Hara

  3. Research Team for Neuroimaging, Tokyo Metropolitan Institute of Gerontology, 35-2 Sakaecho, Itabashi-ku, Tokyo, Japan

    Shihori Hayashi, Motoki Inaji, Kenji Ishii & Tadashi Nariai

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  1. Shoko Hara
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Correspondence to Shoko Hara.

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Hara, S., Kudo, T., Hayashi, S. et al. Improvement in cognitive decline after indirect bypass surgery in adult moyamoya disease: implication of 15O-gas positron emission tomography. Ann Nucl Med 34, 467–475 (2020). https://doi.org/10.1007/s12149-020-01473-8

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  • DOI: https://doi.org/10.1007/s12149-020-01473-8

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