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Neurosurgery
Sep 01, 2024;95 (3): 596-604.

Impact of Cerebral Revascularization on Pial Collateral Flow in Patients With Unilateral Moyamoya Disease Using Quantitative Magnetic Resonance Angiography.

Brandon A Santhumayor, Timothy G White, Danielle Golub, Moses Rivera, Justin Turpin, David Golombeck, Brendan Ryu, Kevin Shah, Rafael Ortiz, Karen Black, Jeffrey M Katz, Amir R Dehdashti, David J Langer
Author Information
  1. Brandon A Santhumayor: Department of Neurosurgery, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Northwell Health, Hempstead , New York , USA. ORCID
  2. Timothy G White: Department of Neurosurgery, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Northwell Health, Hempstead , New York , USA. ORCID
  3. Danielle Golub: Department of Neurosurgery, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Northwell Health, Hempstead , New York , USA. ORCID
  4. Moses Rivera: Department of Neurosurgery, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Northwell Health, Hempstead , New York , USA.
  5. Justin Turpin: Department of Neurosurgery, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Northwell Health, Hempstead , New York , USA. ORCID
  6. David Golombeck: Department of Neurosurgery, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Northwell Health, Hempstead , New York , USA.
  7. Brendan Ryu: Department of Neurosurgery, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Northwell Health, Hempstead , New York , USA.
  8. Kevin Shah: Department of Neurosurgery, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Northwell Health, Hempstead , New York , USA.
  9. Rafael Ortiz: Department of Neurosurgery, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Northwell Health, Hempstead , New York , USA.
  10. Karen Black: Department of Radiology, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Northwell Health, Hempstead , New York , USA.
  11. Jeffrey M Katz: Department of Neurology, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Northwell Health, Hempstead , New York , USA.
  12. Amir R Dehdashti: Department of Neurosurgery, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Northwell Health, Hempstead , New York , USA. ORCID
  13. David J Langer: Department of Neurosurgery, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Northwell Health, Hempstead , New York , USA. ORCID
PMID: 38501815 DOI: 10.1227/neu.0000000000002905

Abstract

BACKGROUND AND OBJECTIVES: Moyamoya disease (MMD) is a chronic steno-occlusive disease of the intracranial circulation that depends on neoangiogenesis of collateral vessels to maintain cerebral perfusion and is primarily managed with cerebral revascularization surgery. A quantitative assessment of preoperative and postoperative collateral flow using quantitative magnetic resonance angiography with noninvasive optimal vessel analysis (NOVA) was used to illustrate the impact of revascularization on cerebral flow distribution.
METHODS: A retrospective review of patients with unilateral MMD who underwent direct, indirect, or combined direct/indirect cerebral revascularization surgery was conducted between 2011 and 2020. Using NOVA, flow was measured at the anterior cerebral artery (ACA), ACA distal to the anterior communicating artery (A2), middle cerebral artery (MCA), posterior cerebral artery (PCA), and PCA distal to the posterior communicating artery (P2). Pial flow (A2 + P2) and collateral flow (ipsilateral [A2 + P2])-(contralateral [A2 + P2]) were measured and compared before and after revascularization surgery. Total hemispheric flow (MCA + A2 + P2) with the addition of the bypass graft flow postoperatively was likewise measured.
RESULTS: Thirty-four patients with unilateral MMD underwent cerebral revascularization. Median collateral flow significantly decreased from 68 to 39.5 mL/min ( P = .007) after bypass. Hemispheres with maintained measurable bypass signal on postoperative NOVA demonstrated significant reduction in median collateral flow after bypass ( P = .002). Median total hemispheric flow significantly increased from 227 mL/min to 247 mL/min ( P = .007) after bypass. Only one patient suffered an ipsilateral ischemic stroke, and no patients suffered a hemorrhage during follow-up.
CONCLUSION: NOVA measurements demonstrate a reduction in pial collateral flow and an increase in total hemispheric flow after bypass for MMD, likely representing a decrease in leptomeningeal collateral stress on the distal ACA and PCA territories. Further studies with these measures in larger cohorts may elucidate a role for NOVA in predicting the risk of ischemic and hemorrhagic events in MMD.

References

Suzuki J, Takaku A. Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol. 1969;20(3):288-299.
Ohkura A, Negoto T, Aoki T, et al. Stenotic changes of the posterior cerebral artery are a major contributing factor for cerebral infarction in moyamoya disease. Surg Neurol Int. 2018;9:105.
Mertens R, Graupera M, Gerhardt H, et al. The genetic basis of moyamoya disease. Transl Stroke Res. 2022;13(1):25-45.
Ihara M, Yamamoto Y, Hattori Y, et al. Moyamoya disease: diagnosis and interventions. Lancet Neurol. 2022;21(8):747-758.
Jang DK, Lee KS, Rha HK, et al. Clinical and angiographic features and stroke types in adult moyamoya disease. AJNR Am J Neuroradiol. 2014;35(6):1124-1131.
Lee SU, Oh CW, Kwon OK, et al. Surgical treatment of adult moyamoya disease. Curr Treat Options Neurol. 2018;20(7):22.
Storey A, Michael Scott R, Robertson R, Smith E. Preoperative transdural collateral vessels in moyamoya as radiographic biomarkers of disease. J Neurosurg Pediatr. 2017;19(3):289-295.
Funaki T, Takahashi JC, Yoshida K, et al. Periventricular anastomosis in moyamoya disease: detecting fragile collateral vessels with MR angiography. J Neurosurg. 2016;124(6):1766-1772.
Sato Y, Kazumata K, Nakatani E, Houkin K, Kanatani Y. Characteristics of moyamoya disease based on national registry data in Japan. Stroke. 2019;50(8):1973-1980.
Nossek E, Langer DJ. How I do it: combined direct (STA-MCA) and indirect (EDAS) EC-IC bypass. Acta Neurochir (Wien). 2014;156(11):2079-2084.
Zhao M, Amin-Hanjani S, Ruland S, Curcio AP, Ostergren L, Charbel FT. Regional cerebral blood flow using quantitative MR angiography. AJNR Am J Neuroradiol. 2007;28(8):1470-1473.
Scott RM, Smith ER. Moyamoya disease and moyamoya syndrome. N Engl J Med. 2009;360(12):1226-1237.
Rankin J. Cerebral vascular accidents in patients over the age of 60: II. Prognosis. Scottish Med J. 1957;2(5):200-215.
Liu ZW, Han C, Wang H, et al. Clinical characteristics and leptomeningeal collateral status in pediatric and adult patients with ischemic moyamoya disease. CNS Neurosci Ther. 2020;26(1):14-20.
Vajkoczy P. Moyamoya disease: collateralization is everything. Cerebrovasc Dis. 2009;28(3):258.
Miyoshi K, Chida K, Kobayashi M, et al. Two-year clinical, cerebral hemodynamic, and cognitive outcomes of adult patients undergoing medication alone for symptomatically ischemic moyamoya disease without cerebral misery perfusion: a prospective cohort study. Neurosurgery. 2019;84(6):1233-1241.
Sato S, Kojima D, Shimada Y, et al. Preoperatively reduced cerebrovascular contractile reactivity to hypocapnia by hyperventilation is associated with cerebral hyperperfusion syndrome after arterial bypass surgery for adult patients with cerebral misery perfusion due to ischemic moyamoya disease. J Cereb Blood Flow Metab. 2018;38(6):1021-1031.
Ohta S, Meyer E, Thompson CJ, Gjedde A. Oxygen consumption of the living human brain measured after a single inhalation of positron emitting oxygen. J Cereb Blood Flow Metab. 1992;12(2):179-192.
Kuroda H, Ogasawara K, Suzuki T, et al. Accuracy of central benzodiazepine receptor binding potential/cerebral blood flow SPECT imaging for detecting misery perfusion in patients with unilateral major cerebral artery occlusive diseases: comparison with cerebrovascular reactivity to acetazolamide and cerebral blood flow SPECT imaging. Clin Nucl Med. 2012;37(3):235-240.
Khan N, Lober RM, Ostergren L, et al. Measuring cerebral blood flow in moyamoya angiopathy by quantitative magnetic resonance angiography noninvasive optimal vessel analysis. Neurosurgery. 2017;81(6):921-927.
White T, Gandhi S, Langer DJ, Katz JM, Dehdashti AR. Does advanced imaging aid in the preoperative evaluation of patients with moyamoya disease? Cureus. 2022;14(10):e29816.
Amin-Hanjani S, Shin JH, Zhao M, Du X, Charbel FT. Evaluation of extracranial–intracranial bypass using quantitative magnetic resonance angiography. J Neurosurg. 2007;106(2):291-298.
Amin-Hanjani S, Singh A, Rifai H, et al. Combined direct and indirect bypass for moyamoya: quantitative assessment of direct bypass flow over time. Neurosurgery. 2013;73(6):962-968; discussion 7-8.
Starke RM, Chwajol M, Lefton D, Sen C, Berenstein A, Langer DJ. Occipital artery-to-posterior inferior cerebellar artery bypass for treatment of bilateral vertebral artery occlusion: the role of quantitative magnetic resonance angiography noninvasive optimal vessel analysis: technical case report. Neurosurgery. 2009;64(4):e779-e781; discussion e81.
Kim T, Bang JS, Kwon OK, et al. Hemodynamic changes after unilateral revascularization for moyamoya disease: serial assessment by quantitative magnetic resonance angiography. Neurosurgery. 2017;81(1):111-119.
Rosi A, Riordan CP, Smith ER, Scott RM, Orbach DB. Clinical status and evolution in moyamoya: which angiographic findings correlate? Brain Commun. 2019;1(1):fcz029.
Amin-Hanjani S, Du X, Mlinarevich N, Meglio G, Zhao M, Charbel FT. The cut flow index: an intraoperative predictor of the success of extracranial-intracranial bypass for occlusive cerebrovascular disease. Neurosurgery. 2005;56(1 Suppl):75-85; discussion 75–85.

MeSH Term

Humans
Moyamoya Disease
Cerebral Revascularization
Female
Male
Collateral Circulation
Adult
Retrospective Studies
Magnetic Resonance Angiography
Middle Aged
Cerebrovascular Circulation
Young Adult
Adolescent
Child
Pia Mater
Journal Article

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