Research progresses in  cerebral venous sinus thrombosis animal models

doi:10.3969/j.issn.1006-7795.2023.05.002

Abstract

Abstract: Cerebral venous sinus thrombosis (CVST) is a special subtype for 0.5%-1% of all strokes，and it tends to occur in young adults and women. It is a difficult disease in neurology because of its complex pathology. The clinical diagnosis is difficult, with high rate of missed diagnosis and misdiagnosis, and severe mortality rate up to 30%. Beyond thrombosis, different CVST-related parenchymal injuries may occur and include edema, ischemic strokes, and intra-cerebral hemorrhage. There are many uncontrollable factors involved during CVST development. In order to further explore the pathological evolution and molecular pathological characteristics of CVST, it is necessary to establish a suitable animal model of CVST to study the molecular pathological mechanisms of CVST thrombosis, brain tissue damage and related prevention and treatment programs. Importantly， animal models are useful to study new therapeutic approaches. In this review, we provide a mainly overview of CVST experimental animal models, focusing on their strengths, limits, and applications for relevant studies.

Key words: cerebrovascular disease, stroke, cerebral venous sinus thrombosis, animal models, venous stroke

CLC Number:

R543

Ma Wei, Zhou Yifan, Jiang Huimin, Wei Huimin, Zhou Chen, Ji Xunming. Research progresses in cerebral venous sinus thrombosis animal models[J]. Journal of Capital Medical University, 2023, 44(5): 704-714.

0
/ / Recommend

Add to citation manager EndNote|Reference Manager|ProCite|BibTeX|RefWorks

URL: https://journal03.magtech.org.cn/Jweb_sdykdxxb/EN/10.3969/j.issn.1006-7795.2023.05.002

https://journal03.magtech.org.cn/Jweb_sdykdxxb/EN/Y2023/V44/I5/704

References

［1］Fan Y H, Yu J, Chen H B, et al. Chinese stroke association guidelines for clinical management of cerebrovascular disorders: executive summary and 2019 update of clinical management of cerebral venous sinus thrombosis［J］. Stroke Vasc Neurol, 2020, 5(2): 152－158.
［2］Zhou L W, Yu A Y X, Ngo L, et al. Incidence of cerebral venous thrombosis: a population-based study, systematic review, and meta-analysis［J］. Stroke, 2023, 54(1): 169－177.
［3］Bousser M G, Ferro J M. Cerebral venous thrombosis: an update［J］. Lancet Neurol, 2007, 6(2): 162－170.
［4］Saposnik G, Barinagarrementeria F, Brown R D Jr, et al. Diagnosis and management of cerebral venous thrombosis: a statement for healthcare professionals from the American Heart Association/American Stroke Association［J］. Stroke, 2011, 42(4): 1158－1192.
［5］Stam J. Thrombosis of the cerebral veins and sinuses［J］. N Engl J Med, 2005, 352(17): 1791－1798.
［6］Kalita J, Chandra S, Kumar B, et al. Cerebral venous sinus thrombosis from a tertiary care teaching hospital in India［J］. Neurologist, 2016, 21(3): 35－38.
［7］Sidhom Y, Mansour M, Messelmani M, et al. Cerebral venous thrombosis: clinical features, risk factors, and long-term outcome in a Tunisian cohort［J］. J Stroke Cerebrovasc Dis, 2014, 23(6): 1291－1295.
［8］Wasay M, Bakshi R, Bobustuc G, et al. Cerebral venous thrombosis: analysis of a multicenter cohort from the United States［J］. J Stroke Cerebrovasc Dis, 2008, 17(2): 49－54.
［9］Ferro J M, Lopes M G, Rosas M J, et al. Delay in hospital admission of patients with cerebral vein and dural sinus thrombosis［J］. Cerebrovasc Dis, 2005, 19(3): 152－156.
［10］Ferro J M, Canhão P, Stam J, et al. Delay in the diagnosis of cerebral vein and dural sinus thrombosis: influence on outcome［J］. Stroke, 2009, 40(9): 3133－3138.
［11］Luo Y X, Tian X, Wang X F. Diagnosis and treatment of cerebral venous thrombosis: a review［J］. Front Aging Neurosci, 2018, 10: 2.
［12］Guo X B, Sun J C, Lu X K, et al. Intrasinus thrombolysis for cerebral venous sinus thrombosis: single-center experience［J］. Front Neurol, 2019, 10: 1185.
［13］Housley S B, Vakharia K, Waqas M, et al. Mechanical venous thrombectomy and prolonged infusion of tissue plasminogen activator for cerebral venous sinus thrombosis: video case report［J］. Surg Neurol Int, 2020, 11: 193.
［14］Afifi K, Bellanger G, Buyck P J, et al. Features of intracranial hemorrhage in cerebral venous thrombosis［J］. J Neurol, 2020, 267(11): 3292－3298.
［15］Simaan N, Molad J, Peretz S, et al. Characteristics of cerebral sinus venous thrombosis patients presenting with intracerebral hemorrhage［J］. J Clin Med, 2022, 11(4): 1040.
［16］Gupta N, Sahu A, Prabhakar A, et al. Activation of NLRP3 inflammasome complex potentiates venous thrombosis in response to hypoxia［J］. Proc Natl Acad Sci U S A, 2017, 114(18): 4763－4768.
［17］Ding J Y, Song B Y, Xie X R, et al. Inflammation in cerebral venous thrombosis［J］. Front Immunol, 2022, 13: 833490.
［18］Hu S Y, Lee H, Zhao H P, et al. Inflammation and severe cerebral venous thrombosis［J］. Front Neurol, 2022, 13: 873802.
［19］Rashad S, Niizuma K, Sato-Maeda M, et al. Early BBB breakdown and subacute inflammasome activation and pyroptosis as a result of cerebral venous thrombosis［J］. Brain Res, 2018, 1699: 54－68.
［20］Wolberg A S, Aleman M M, Leiderman K, et al. Procoagulant activity in hemostasis and thrombosis: Virchows triad revisited［J］. Anesth Analg, 2012, 114(2): 275－285.
［21］Jiang W Y, Jin C C, Xu W M, et al. Establishment of a rat model of superior sagittal-sinus occlusion via a thread-embolism method［J］. J Vis Exp, 2021(173): e62118.
［22］Wang W, Mu S W, Xu W M, et al. Establishment of a rat model of superior sagittal-sinus occlusion and recanalization via a thread-embolism method［J］. Neuroscience, 2019, 416: 41－49.
［23］Yang H, Meng Z W, Zhang C Z, et al. Establishing a new rat model of central venous sinus thrombosis and analyzing its pathophysiological and apoptotic changes［J］. J Neurosci Methods, 2012, 203(1): 130－135.
［24］Mu S W, Lin Y H, Xu Y J, et al. A novel rat model for cerebral venous sinus thrombosis: verification of similarity to human disease via clinical analysis and experimental validation［J］. J Transl Med, 2022, 20(1): 174.
［25］Bourrienne M C, Loyau S, Benichi S, et al. A novel mouse model for cerebral venous sinus thrombosis［J］. Transl Stroke Res, 2021, 12(6): 1055－1066.
［26］Miyamoto K, Heimann A, Kempski O. Microcirculatory alterations in a Mongolian gerbil sinus-vein thrombosis model［J］. J Clin Neurosci, 2001, 8(4): 97－105.
［27］Ueda K, Nakase H, Miyamoto K, et al. Impact of anatomical difference of the cerebral venous system on microcirculation in a gerbil superior sagittal sinus occlusion model［J］. Acta Neurochir (Wien), 2000, 142(1): 75－82.
［28］Ding R, Li H Y, Liu Y Q, et al. Activating cGAS-STING axis contributes to neuroinflammation in CVST mouse model and induces inflammasome activation and microglia pyroptosis［J］. J Neuroinflammation, 2022, 19(1): 137.
［29］Kim D E, Schellingerhout D, Jaffer F A, et al. Near-infrared fluorescent imaging of cerebral thrombi and blood-brain barrier disruption in a mouse model of cerebral venous sinus thrombosis［J］. J Cereb Blood Flow Metab, 2005, 25(2): 226－233.
［30］Nagai M, Terao S, Yilmaz G, et al. Roles of inflammation and the activated protein C pathway in the brain edema associated with cerebral venous sinus thrombosis［J］. Stroke, 2010, 41(1): 147－152.
［31］Röttger C, Madlener K, Heil M, et al. Is heparin treatment the optimal management for cerebral venous thrombosis? Effect of abciximab, recombinant tissue plasminogen activator, and enoxaparin in experimentally induced superior sagittal sinus thrombosis［J］. Stroke, 2005, 36(4): 841－846.
［32］Srivastava A K, Gupta R K, Haris M, et al. Cerebral venous sinus thrombosis: developing an experimental model［J］. J Neurosci Methods, 2007, 161(2): 220－222.
［33］Srivastava A K, Kalita J, Dohare P, et al. Studies of free radical generation by neurons in a rat model of cerebral venous sinus thrombosis［J］. Neurosci Lett, 2009, 450(2): 127－131.
［34］Srivastava A K, Kalita J, Haris M, et al. Radiological and histological changes following cerebral venous sinus thrombosis in a rat model［J］. Neurosci Res, 2009, 65(4): 343－346.
［35］Tiwari H S, Misra U K, Kalita J, et al. Oxidative stress and glutamate excitotoxicity contribute to apoptosis in cerebral venous sinus thrombosis［J］. Neurochem Int, 2016, 100: 91－96.
［36］Heimann A, Takeshima T, Alessandri B, et al. Effects of hypertonic/hyperoncotic treatment after rat cortical vein occlusion［J］. Crit Care Med, 2003, 31(10): 2495－2501.
［37］Kimura R, Nakase H, Sakaki T, et al. Vasogenic edema and VEGF expression in a rat two-vein occlusion model［J］. Acta Neurochir Suppl, 2003, 86: 213－217.
［38］Nakase H, Heimann A, Kempski O. Local cerebral blood flow in a rat cortical vein occlusion model［J］. J Cereb Blood Flow Metab, 1996, 16(4): 720－728.
［39］Nakase H, Kakizaki T, Miyamoto K, et al. Use of local cerebral blood flow monitoring to predict brain damage after disturbance to the venous circulation: cortical vein occlusion model by photochemical dye［J］. Neurosurgery, 1995, 37(2): 280－286.
［40］Nakase H, Nagata K, Ohtsuka H, et al. An experimental model of intraoperative venous injury in the rat［J］. Skull Base Surg, 1997, 7(3): 123－128.
［41］Nishioka T, Nakase H, Nakamura M, et al. Sequential and spatial profiles of apoptosis in ischemic penumbra after two-vein occlusion in rats［J］. J Neurosurg, 2006, 104(6): 938－944.
［42］Otsuka H, Ueda K, Heimann A, et al. Effects of cortical spreading depression on cortical blood flow, impedance, DC potential, and infarct size in a rat venous infarct model［J］. Exp Neurol, 2000, 162(1): 201－214.
［43］Schaller C, Nakase H, Kotani A, et al. Impairment of autoregulation following cortical venous occlusion in the rat［J］. Neurol Res, 2002, 24(2): 210－214.
［44］Wang J Z, Ji X M, Ling F, et al. A new model of reversible superior sagittal sinus thrombosis in rats［J］. Brain Res, 2007, 1181: 118－124.
［45］Wang J Z, Ji X M, Ling F, et al. Comparison of anticoagulation and thrombolysis treatments in a rat model of superior sagittal sinus thrombosis［J］. Int J Neurosci, 2014, 124(7): 532－541.
［46］Beck D J K, Russell D S. Experiments on thrombosis of the superior longitudinal sinus［J］. J Neurosurg, 1946, 3: 337－347.
［47］Schaller B, Graf R, Wienhard K, et al. A new animal model of cerebral venous infarction: ligation of the posterior part of the superior sagittal sinus in the cat［J］. Swiss Med Wkly, 2003, 133(29/30): 412－418.
［48］Fries G, Wallenfang T, Hennen J, et al. Occlusion of the pig superior sagittal sinus, bridging and cortical veins: multistep evolution of sinus-vein thrombosis［J］. J Neurosurg, 1992, 77(1): 127－133.
［49］Röttger C, Bachmann G, Gerriets T, et al. A new model of reversible sinus sagittalis superior thrombosis in the rat: magnetic resonance imaging changes［J］. Neurosurgery, 2005, 57(3): 573－580.
［50］Cervós-Navarro J, Kannuki S, Matsumoto K. Neuropathological changes following occlusion of the superior sagittal sinus and cerebral veins in the cat［J］. Neuropathol Appl Neurobiol, 1994, 20(2): 122－129.
［51］Chen C, Wang Q, Gao Y, et al. Photothrombosis combined with thrombin injection establishes a rat model of cerebral venous sinus thrombosis［J］. Neuroscience, 2015, 306: 39－49.
［52］Frerichs K U, Deckert M, Kempski O, et al. Cerebral sinus and venous thrombosis in rats induces long-term deficits in brain function and morphology—evidence for a cytotoxic Genesis［J］. J Cereb Blood Flow Metab, 1994, 14(2): 289－300.
［53］Li G W, Zeng X W, Ji T L, et al. A new thrombosis model of the superior sagittal sinus involving cortical veins［J］. World Neurosurg, 2014, 82(1/2): 169－174.
［54］Nakase H, Heimann A, Kempski O. Alterations of regional cerebral blood flow and oxygen saturation in a rat sinus-vein thrombosis model［J］. Stroke, 1996, 27(4): 720－728.
［55］Röther J, Waggie K, van Bruggen N, et al. Experimental cerebral venous thrombosis: evaluation using magnetic resonance imaging［J］. J Cereb Blood Flow Metab, 1996, 16(6): 1353－1361.
［56］Ungersböck K, Heimann A, Kempski O. Cerebral blood flow alterations in a rat model of cerebral sinus thrombosis［J］. Stroke, 1993, 24(4): 563－569.
［57］Vosko M R, Röther J, Friedl B, et al. Microvascular damage following experimental sinus-vein thrombosis in rats［J］. Acta Neuropathol, 2003, 106(5): 501－505.
［58］Wei Y, Deng X, Sheng G, et al. A rabbit model of cerebral venous sinus thrombosis established by ferric chloride and thrombin injection［J］. Neurosci Lett, 2018, 662: 205－212.
［59］Xiao L P, Ji X M, Zhao H P, et al. A novel severe cerebral venous thrombosis rat model based on semi-ligation combined with ferric chloride and thrombin［J］. CNS Neurosci Ther, 2022, 28(12): 2129－2140.
［60］Ding R, Ou W Y, Chen C W, et al. Endoplasmic reticulum stress and oxidative stress contribute to neuronal pyroptosis caused by cerebral venous sinus thrombosis in rats: involvement of TXNIP/peroxynitrite-NLRP3 inflammasome activation［J］. Neurochem Int, 2020, 141: 104856.
［61］Stracke C P, Spuentrup E, Katoh M, et al. New experimental model of sinus and cortical vein thrombosis in pigs for MR imaging studies［J］. Neuroradiology, 2006, 48(10): 721－729.
［62］Wang R, Kozhaya L, Mercer F, et al. Expression of GARP selectively identifies activated human FOXP3+ regulatory T cells［J］. Proc Natl Acad Sci U S A, 2009, 106(32): 13439－13444.
［63］Kanaiwa H, Kuchiwaki H, Inao S, et al. Changes in the cerebrocortical capillary network following venous sinus occlusion in cats［J］. Surg Neurol, 1995, 44(2): 172－180.
［64］Heinz E R, Geeter D, Gabrielsen T O. Cortical vein thrombosis in the dog with a review of aseptic intracranial venous thrombosis in man［J］. Acta Radiol Diagn (Stockh), 1972, 13(1): 105－114.
［65］Sarwar M, Virapongse C, Carbo P. Experimental production of superior sagittal sinus thrombosis in the dog［J］. AJNR Am J Neuroradiol, 1985, 6(1): 19－22.
［66］Owens G, Stahlman G, Capps J, et al. Experimental occlusion of dural sinuses［J］. J Neurosurg, 1957, 14(6): 640－647.
［67］Sader N, de Lotbinière-Bassett M, Tso M K, et al. Management of venous sinus thrombosis［J］. Neurosurg Clin N Am, 2018, 29(4): 585－594.
［68］Silvis S M, de Sousa D A, Ferro J M, et al. Cerebral venous thrombosis［J］. Nat Rev Neurol, 2017, 13(9): 555－565.
［69］Silvis S M, Middeldorp S, Zuurbier S M, et al. Risk factors for cerebral venous thrombosis［J］. Semin Thromb Hemost, 2016, 42(6): 622－631.
［70］Aguiar de Sousa D, Lucas Neto L, Arauz A, et al. Early recanalization in patients with cerebral venous thrombosis treated with anticoagulation［J］. Stroke, 2020, 51(4): 1174－1181.
［71］Barboza M A, Chiquete E, Arauz A, et al. A practical score for prediction of outcome after cerebral venous thrombosis［J］. Front Neurol, 2018, 9: 882.

Research progresses in cerebral venous sinus thrombosis animal models

PDF

Knowledge

Abstract

Cite this article

share this article

References

Related Articles 1

Recommended Articles

Metrics

Comments