Veins and Lymphatics 2019; volume 8:7839

Venous and glymphatic house of Sal Sclafani, M.D. (one of the past drainage of the brain: Presidents of the Society). At that meeting it Correspondence: Ewart Mark Haacke, Wayne was decided to go ahead and form a 501(c)3 State University, School of Medicine, Brief history of the Non-Profit Society which was then centered Department of Radiology, 4201 St. Antoine, International Society for in Detroit, Michigan for the first 3 years. Detroit 48201, MI, USA. Neurovascular Disease Subsequently the office moved to Buffalo Tel.: +1.313.745.1395 - Fax: +1.313.745.9182. for the next 3 years with Robert Zivadinov, E-mail: [email protected] M.D., Ph.D. (also one of the past Presidents 1-4 5 Key words: Chronic cerebrospinal venous Ewart Mark Haacke, Meiyun Wang, of the Society) and then to Shreveport for Xiaoyue Ma,5 David Utriainen2,3 insufficiency; glymphatic system; neurovas- two years with Steve Alexander (also one of cular disease; cerebrospinal fluid; cerebral 1 Wayne State University, Detroit, MI, the past Presidents of the Society) and then drainage. USA; 2The Magnetic Resonance Imaging back to Detroit in 2017 with Mark Haacke Institute for Biomedical Research, Ph.D. (the current past president). Contributions:e author contributed to writing Detroit, MI, USA; 3Magnetic Resonance the paper. Innovations, Inc., Detroit, MI, USA; Received for publication: 19 September 2018. 4Spintech, Inc., Detroit, MI, USA; Accepted for publication: 24 September 2018 5Henan Provincial Peoples’ Hospital, Highlights of the past eight meetings Zhenzhou, Henan Province, China Bologna, 2011; President and This work is licensed under a Creative Annual Meeting Chair Paolo Commons Attribution 4.0 License (by-nc 4.0). Zamboni ©Copyright E.M. Haacke et al., 2019 The ability to understand the vascular Licensee PAGEPress, Italy Abstract system has the potential to lead to new treat- Veins and Lymphatics 2019; 8:7839 ments. Dr. Berislav Zlokovic had the insight doi:10.4081/vl.2019.7839 The International Society of to focus on the fundamental aspects of vas- Neurovascular Diseases is an International, only cular pathology including: the role of: Interdisciplinary Scientific Organization to neural injury and neurorestorative thera- reduced perfusion, hypoxia, tissue damage (ISNVD: www.isnvd.org) devoted to the pies. His work focused on using drugs such and endothelial damage.6-8 He suggested that study of intracranial and extracranial vascu- as Niaspin (niacin or vitamin B3) and silde- occurs secondary to vas- lature. Different from other scientific soci- nafil (Viagra) to help generate the formation cular damage and that novel pharmaceuticalsuse eties, ISNVD is interested also in the inves- of new micro-vessels to regenerate brain might be designed to target inflammation tigation of the cerebral drainage, including tissue.20-22 and endothelial pathology. Today trials are the venous and glymphatic systems. A highlight of this workshop was the underway using activated protein C, which is Moreover, ISNVD promotes studies on: focus on providing a Consensus on Imaging a blood protease with its anti-coagulant func- stroke, carotid surgery, neurovascular & Treatment Protocols. Ultrasound, tions turned off so that it is a multiple cell aspects of neurodegeneration, models of Magnetic Resonance Imaing (MRI) and signaling neuroprotective agent, 3K3A- circulation, vasoactive peptides, and basic 9 balloon angioplasty groups met separately APC, reducing the risk of hemorrhage. This science. This review summarizes the contri- is being studied in stroke today and Zlokovic to discuss the state-of-the-art technology in bution of the society to the fields above, as is an active participant in this work. each area with an eye toward creating a well as the history of the annual meetings This was followed by Dr. Costantino white paper. The outcome of this effort was and the major impact papers promoted by Iadecola who discussed the role of iron as a a paper published in 2014 in JVIR, 2014, ISNVD. 23 potential inflammatory agent, the role of 25, 1785. oxidative stress and endothelial damage.10-12 The Gold Medal was given to Franz He further suggested there might be a rela- Schelling for his pioneering contributions to tionship with poor vascular conditions and understanding the role of the venous vascu- Introduction that these could lead to the production of lature in MS. Dr. Schelling then gave an Non-commercial13,14 overview of some of the history and where The foundation of the ISNVD had its beta amyloid plaque. Today, along with he thought we still needed to forge ahead to history in the first meeting held on chronic the glymphatic system to be discussed later, clearly addresses the role of abnormal venous hypertension by Dr. Paolo Zamboni this is now a very promising direction of venous vasculature in MS. in Bologna, Italy in 2009. His pioneering research. work on iron and vascular effects in multi- Dr. Robert Zivadinov followed with ple sclerosis (MS) opened the door to a examples from imaging demonstrating Krakow, Poland, 2013; President more intensive international effort to study reversible cerebrospinal fluid stagnation and Annual Meeting Chair Marian the vascular sources of neurodegenerative and increased iron content in MS patients, Simka disease.1,2 The story really began with his and also suggesting that these increases At this meeting the venue of presenta- may correlate with the severity of the dis- tions continued to expand and covered a seminal paper on iron: The big idea: iron- 15-19 dependent inflammation in venous disease ease (Figure 1). number of new concepts including the work and proposed parallels in multiple sclero- of Jaap Valk from Amsterdam.24 He present- sis.3 After the Bologna meeting, it became Orlando, Florida, USA 2012; ed the results of a prospective study on clear that there was not a major focus on President Robert Zivadinov, Annual patients with chronic intractable headache venous effects in neurodegenerative disease Meeting Chair Mark Haacke and other concurrent symptoms such as ver- and even the role of the arterial system was The keynote speech was given by tigo, dizziness, tinnitus and visual distur- under-represented.4,5 This spurred a group Michael Chopp, Ph.D., from Henry Ford bances. The patients were examined by the of leading scientists to meet in 2010 at the Hospital. He discussed vascular responses use of magnetic resonance venography.

[Veins and Lymphatics 2019; 8:7839] [page 3] Review

Often the patients were found to have year that continues to be an important topic cerebrospinal fluid systems as a whole, intracranial abnormalities such as persistent today. The session on Vascular Function, Prof. Jiani Hu spoke on The interaction occipital sinus with loop formation or Glymphatic System and New Drug between the vascular and glymphatic sys- thrombosis of the intracranial sinuses. He Development was led by the the next tems.43 Prof. Eleuterio F. Toro delivered a concluded that venous intracranial patholo- President, Dr. Steve Alexander.36-38 He talk titled Modeling flow in the head and gy is prevalent in patients presenting with spoke on Alterations in Hemodynamic Flow neck.44 He had reviewed the work of neurological symptoms and that MRI would Patterns and Endothelial Dysfunction in Warnert et al. and assessed Warnert’s play a key role in diagnosing these patients. Neurodegeneration. hypothesis by using a state-of-the-art global The Gold Medal was given to Mark mathematical model for human circula- San Francisco, California, USA Haacke for his pioneering efforts in devel- tion.45,46 He found that congenital anatomi- 2014; President and Annual Meeting oping MR vascular imaging methodologies cal variants (VHA and iCoW) do not exhibit Chair Mike Dake such as magnetic resonance angiography, alterations in cerebral blood flow. Dr. Jie Li, susceptibility weighted imaging, and representing the team of Satish Reflecting the expanding interest and MICRO imaging. He continues to push the Krishnamurthy, presented a talk on Delayed collaborations within the society, a special use of MRI to study the vascular system in macromolecular transport at the neurovas- focus on traumatic brain injury (TBI) was all neuro-degenerative diseases with a spe- cular unit in hydrocephalus. His studies the theme of the 2014 meeting. Dr. Diaz- cial focus on MS, Parkinson’s disease have shown that excess macromolecules in Arrastia discussed treatment of patients (PD), stroke, TBI and vascular dementia.39 the ventricles are sufficient to cause hydro- with TBI.25-28 He presented several different cephalus. He said these macromolecules are treatment options including: sildenafil, ery- transported in both normal and hydro- thropoietin, statins, G-CSF, VEGF, pioglita- Taormina, Sicily, Italy, 2017; cephalic states from the ventricles via the zone, exercise, enriched endothelia progen- President Steve Alexander, Annual perivascular pathways (glymphatic path- itor cells, from cord blood or bone marrow, Meeting Chair Pierfrancesco Veroux ways) and eliminated into the vascular sys- and low level laser light therapy. His find- Harking back to the foundations of the tem (serum). Imaging has shown that the ings in humans were similar to the keynote society, Byung-Boong Lee presented the iron dextran used in their experiments finds lecture in 2012 by Dr. Michael Chopp. keynote lecture: Defective Development of its wayonly into the venous system and is then Vena Cava: Embryological interpretation of 47 Hemodynamic Consequences.40,41 He also drained out of the brain. Naples, Italy, 2015; President Ziv The Gold Medal was given to Robert Haskal, Annual Meeting Chair presented Obstructive truncular venous malformations, which was an excellent Zivadinov for his pioneering efforts in Marcello Mancini overview of how venous malformationsuseapplying MRI methods to study MS. He Research into new therapeutic could contribute to blood flow disturbances continues to evaluate MS using a variety of approaches for human neuro-degenerative new methods in an attempt to understand in general with a focus on CNS participa- 48,49 disorders is part of the effort by Dr. Jacques tion. These truncular venous malformations the underlying etiology (Figure 2). De Keyser and his group from Brussels, The Zhengzhou meeting was the first 29-31 are known to occur in MS patients and Belgium. They demonstrated the recent evidence suggests they occur in time the ISNVD went to Asia. This year we reversibility of the reduction in cerebral Parkinson’s patients as well.42 were fortunate enough to have Dr. Meiyun blood flow observed in MS patients by Wang of Henan Provincial People’s th using antagonists of endothelin-1 (ET-1), a Zhengzhou, Henan Province, China, Hospital agree to host the 8 Annual vasoactive peptide which is also over- Meeting of the ISNVD in Zhengzhou, 2018; President Mark Haacke, th th 50 expressed in Alzheimer’s Disease (AD) and China from May 31 -June 2 , 2018. other disorders associated with chronic Annual Meeting Chair Meiyun During the three days of the meeting, more brain hypoperfusion.32 Wang than 40 well-known radiologists and neu- The role of vessel wall began taking on Bringing together efforts that recognize rologists gave presentations with more than importance at this meeting. The effects of the link between the arterial, venous and 300 attendees from around the world active- ET-1 and other markers of endothelial dys- function of the autoregulation of cerebral vessels and cerebral circulation timeNon-commercial in MS patients were quantitatively demonstrated by Serena Monti, M.S. from Siena, Italy using digital subtraction angiography.33 The Gold Medal was given to Paolo Zamboni for his pioneering contributions to understanding the role of the venous vascu- lature in chronic cerebral spinal venous insufficiency (CCSVI).34 Paolo continues to be a leader in this field not only constantly probing the effects of venous hypertension but also developing new means by which to monitor these vascular abnormalities.35

New York City, New York, USA 2016; President and Annual Meeting Figure 1. Five Presidents of the ISNVD, at that time Robert Zivadinov was the current Chair Sal Sclafani President, Paolo Zamboni the past President and Mike Dake the President Elect. A new area of interest sprang up this

[page 4] [Veins and Lymphatics 2019; 8:7839] Review ly participating. The speakers were able to techniques of cerebral ischemia by Dr. audience were excited about this new tech- give their presentations in both Chinese and Jianping Dai.52 He said new therapies of nology and its implications in the field of English as simultaneous interpretation was recanalization of cerebral ischemia may medical imaging. provided through special headsets. This improve patient outcome and that early Prof. E. Mark Haacke spoke about a ensured easy understanding of the speeches diagnosis by imaging is significant for rapid multi-contrast MRI method using and a fluent exchange of information choosing a suitable treatment. He noted that strategically acquired gradient echo throughout the meeting. The meeting was precision medicine requires the combina- (STAGE) imaging.54,55 He noted that formally hosted by Henan Provincial tion of P4 medicine, integrated imaging, STAGE provides a rapid standardized imag- People’s Hospital in Zhengzhou, Henan, artificial intelligence (AI) and molecular ing approach of the entire brain in less than China, which is one of the largest hospitals medicine but that despite advances in this 5 (7) minutes that can be used for all 3T 57-61 in China with a history of more than 114. era of precision medicine, challenges (1.5T) manufacturer’ systems. Please visit our website at www.isnvd.org remain. Dr. Meiyun Wang talked about chemi- for more information about the ISNVD or Prof. Lawrence L. Wald gave the sec- cal exchange saturation transfer (CEST) e-mail [email protected] ond keynote speech titled MRI unchained; imaging in stroke. She introduced two The opening ceremony welcomed removing hardware constraints to make CEST concepts: 1) amide proton transfer everyone with a video of the history and faster, portable and motion tolerant images. (APT) and length and 2) offset varied satu- culture of Henan Province, the Henan From the insight of biomedical imaging and ration (LOVARS). She and her team have Provincial People’s Hospital and the bioengineering, Prof. Wald gave an excel- pioneered the application of these methods ISNVD. Dr. Meiyun Wang gave a welcome lent talk on several advanced technologies, to demonstrate that they can be used to speech and introduced the other invited mainly about MR image reconstruction detect stroke and distinctly differentiate guests including: Dr. Longde Wang, an aca- (based on modeling the structure of interest hyperacute intracranial hemorrhage from demician of the Chinese Academy of rather than using Fourier Transform), the cerebral ischemia thus opening the door for 62,63 Engineering, Honorary President of the portable brain MRI, accelerated imaging a rapid single scan evaluation of stroke. 53 ISNVD 2018 Annual Meeting and President and removing motion artifacts. He said, Prof. Paolo Zamboni talked about Eagle of the Chinese Preventive Medicine “If you can measure a systematic error, you jugularonly syndrome. He said that the jugular Association from Stroke Prevention and can fix the systematic error”. Many in the variant of the Eagle syndrome is a distinct Control Project Committee, National Health Commission; Dr. Jianping Dai, a for- eign academician of the American Academy use of Medical Sciences, Past Vice-President of the Chinese Medical Association; Prof. Lawrence L. Wald, President-Elect of ISMRM; Prof. Bernd Hamm, the chairper- son of the European Society of Radiology (ESR) Board of Directors, President of the ESR and European Congress of Radiology (ECR) 2018. Prof. Xiaoliang Zhang, President of the Overseas Chinese Society for Magnetic Resonance in Medicine (OCSMRM); Dr. Wei Huang, Vice- Figure 2. Gold medal winners Franz Schelling (2012), Mark Haacke (2016), Robert President and Inspector of the Health and Zivadinov (2018) and Paolo Zamboni (2015). Family Planning Commission of Henan Province; Dr. Jianqin Gu, President of Henan Provincial People’s Hospital who spoke about the hospital’s development and endeavor in improving the diagnosticNon-commercial level of neurovascular diseases; Dr. Fengmin Shao, Secretary of the Party Committee of Henan Provincial People’s Hospital; Dr. Peichun Sun, the Vice President of Henan Provincial People’s Hospital and Prof. E. Mark Haacke, 2017/2018 President of the ISNVD (Figure 3).

Highlights of the 2018 meeting Dr. Longde Wang gave a lecture entitled Exploration on the prevention and control of stroke in China. He elaborated the major challenges, preliminary achievements and 51 Figure 3. Presidium and invited speakers. All the invited speakers and honorary guests future plans in stroke prevention in China. were present for this picture. This was followed by a speech on Imaging

[Veins and Lymphatics 2019; 8:7839] [page 5] Review clinical entity with respect to both classic rosis. J R Soc Med 2006;99:589-93. 2012;59:331-9. and carotid variants, and it seems to be a 4. Dake MD, Zivadinov R, Haacke EM. 17. Hagemeier J, Weinstock-Guttman B, factor which potentially increases the sus- Chronic cerebrospinal venous insuffi- Heininen-Brown M, et al. Gray matter ceptibility to subarachnoid hemorrhage ciency in : a historical SWI-filtered phase and atrophy are lin- (SAH).56 Prof. Bruno’s talk was called perspective. Funct Neurol 2011;26:181- ked to disability in MS. Front Biosci Venous lesions in patients with Meniere’s 95. (Elite Ed) 2013;5:525-32. Disease (MD): Results of a multicentric 5. Siskin GP, Haskal ZJ, Mclennan G, et 18. Hagemeier J, Zivadinov R, Dwyer MG, Italian study and guidelines for an interna- al. Development of a research agenda et al. Changes of deep gray matter tional project. His research found that the for evaluation of interventional thera- magnetic susceptibility over 2 years in prevalence of CCSVI in Meniere’s disease pies for chronic cerebrospinal venous multiple sclerosis and healthy control is high and PTA has a significant curative insufficiency: proceedings from a mul- brain. Neuroimage Clin 2018;18:1007- effect on MD.57 He believed that the venous tidisciplinary research consensus panel. 16. stasis of the head and neck veins may be J Vasc Interv Radiol 2011;22:587-93. 19. Zivadinov R, Tavazzi E, Bergsland N, considered a further etiopathogenetic mech- 6. Zlokovic BV. The blood-brain barrier in et al. Brain iron at quantitative MRI is anism which adds to many other already health and chronic neurodegenerative associated with disability in multiple known mechanisms that still define MD as disorders. Neuron 2008;57:178-201. sclerosis. Radiology 2018;180136. a multifactorial disease. 7. Sweeney MD, Sagare AP, Zlokovic BV. 20. Zhang R, Wang Y, Zhang L, et al. Prof. Paolo Zamboni also discussed the Blood-brain barrier breakdown in Sildenafil (Viagra) induces neurogene- Brave Dreams trial.58,59 He believed CCSVI Alzheimer disease and other neurodege- sis and promotes functional recovery contributed to a better understanding of the nerative disorders. Nat Rev Neurol after stroke in rats. Stroke 2002;33: function and role of the extracranial venous 2018;14:133-50. 2675-80. system. He then suggested, “Rather than 8. Brown R, Benveniste H, Black SE, et 21. Li L, Jiang Q, Zhang L, et al. rejecting this accumulated new knowledge, al. Understanding the role of the periva- Angiogenesis and improved cerebral we should use it more appropriately for scular space in cerebral small vessel blood flow in the ischemic boundary future endeavors”. Prof. Robert Zivadinov disease. Cardiovasc Res 2018;114: areaonly detected by MRI after administra- discussed the role of cardiovascular (CV) 1462-73. tion of sildenafil to rats with embolic comorbidities in the pathogenesis of neuro- 9. Griffin JH, Zlokovic BV, Mosnier LO. stroke. Brain Res 2007;1132:185-92. logical disorders.60 He pointed out that CV Activated protein C, protease activated 22. Zhang RL, Chopp M, Roberts C, et al. comorbidities are associated with higher receptor 1, and neuroprotection. Blooduse Sildenafil enhances neurogenesis and susceptibility to neurodegenerative disor- 2018;132:159-69. oligodendrogenesis in ischemic brain of ders and disease progression, there is a 10. Kunz A, Park L, Abe T, et al. middle-aged mouse. PLoS One 2012; stronger link between CSA of neck vessels Neurovascular protection by ischemic 7:e48141. and CV risk factors, and that the heart-brain tolerance: role of nitric oxide and reac- 23. Zivadinov R, Bastianello S, Dake MD, axis should be better investigated in dis- tive oxygen species. J Neurosci et al. Recommendations for multimodal eases such as MS, AD and PD. Prof. 2007;27:7083-93. noninvasive and invasive screening for Salvatore Sclafani discussed Carotid arteri- 11. Faraco G, Park L, Anrather J, Iadecola detection of extracranial venous abnor- al trauma and minimally invasive treat- C. Brain perivascular macrophages: malities indicative of chronic cerebro- ments. He believed that treating carotid characterization and functional roles in spinal venous insufficiency: a position injury surgically is challenging and health and disease. J Mol Med (Berl) statement of the International Society endovascular options are essential for sur- 2017;95:1143-52. for Neurovascular Disease. J Vasc vival.61 The 2019 meeting will be held in 12. Iadecola C. The neurovascular unit Interv Radiol 2014;25:1785-94. , Italy, bringing us back to our roots. coming of age: a journey through neu- 24. Valk J, Van Vucht N, Pevenage P. MR The ISNVD is a non-profit organization rovascular coupling in health and disea- Venographic patterns in chronic intrac- registered in the United State of America. se. Neuron 2017;96:17-42. table headache. Neuroradiol J 2011; To become a member, please go to 13. Iadecola C. Vascular and metabolic fac- 24:13-9. www.isnvd.org. Non-commercialtors in Alzheimer’s disease and related 25. Hudak AM, Peng L, Marquez De La dementias: introduction. Cell Mol Plata C, et al. Cytotoxic and vasogenic Neurobiol 2016;36:151-4. cerebral oedema in traumatic brain inju- 14. Kahl A, Blanco I, Jackman K, et al. ry: assessment with FLAIR and DWI References Cerebral ischemia induces the aggrega- imaging. Brain Inj 2014;28:1602-9. tion of proteins linked to neurodegene- 26. Kenney K, Amyot F, Haber M, et al. 1. Zamboni P, Galeotti R, Menegatti E, et rative diseases. Sci Rep 2018;8:2701. Cerebral vascular injury in traumatic al. Chronic cerebrospinal venous insuf- 15. Zivadinov R, Magnano C, Galeotti R, et brain injury. Exp Neurol 2016;275:353- ficiency in patients with multiple scle- al. Changes of cine cerebrospinal fluid 66. rosis. J Neurol Neurosurg Psychiatry dynamics in patients with multiple scle- 27. Okonkwo DO, Shutter LA, Moore C, et 2009;80:392-9. rosis treated with percutaneous translu- al. Brain oxygen optimization in severe 2. Zamboni P, Sisini F, Menegatti E, et al. minal angioplasty: a case-control study. traumatic brain injury phase-II: a phase An ultrasound model to calculate the J Vasc Interv Radiol 2013;24:829-38. II randomized trial. Crit Care Med brain blood outflow through collateral 16. Zivadinov R, Heininen-Brown M, 2017;45:1907-14. vessels: a pilot study. BMC Neurology Schirda CV, et al. Abnormal subcortical 28. Haber M, Amyot F, Kenney K, et al. 2013;13:81. deep-gray matter susceptibility-wei- Vascular abnormalities within normal 3. Zamboni P. The big idea: iron-depen- ghted imaging filtered phase measure- appearing tissue in chronic traumatic dent inflammation in venous disease ments in patients with multiple sclero- brain injury. J Neurotrauma 2018 [Epub and proposed parallels in multiple scle- sis: a case-control study. Neuroimage ahead of print].

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29. Cambron M, Mostert J, Haentjens P, et 2015;34:97-49. study. Eur J Radiol 2018;100:156-65. al. Fluoxetine in progressive multiple 42. Liu M, Xu H, Wang Y, et al. Patterns of 53. Polimeni JR, Wald LL. Magnetic reso- sclerosis (FLUOX-PMS): study proto- chronic venous insufficiency in the nance imaging technology-bridging the col for a randomized controlled trial. dural sinuses and extracranial draining gap between noninvasive human ima- Trials 2014;15:37. veins and their relationship with white ging and optical microscopy. Curr Opin 30. D’haeseleer M, Hostenbach S, Peeters matter hyperintensities for patients with Neurobiol 2018;50:250-60. I, et al. Cerebral hypoperfusion: a new Parkinson's disease. J Vasc Surg 54. Chen Y, Liu S, Wang Y, et al. pathophysiologic concept in multiple 2015;61:1511-20. STrategically Acquired Gradient Echo sclerosis? J Cereb Blood Flow Metab 43. Bacyinski A, Xu M, Wang W, Hu J. The (STAGE) imaging, part I: Creating 2015;35:1406-10. paravascular pathway for brain waste enhanced T1 contrast and standardized 31. Vande Vyver M, Beelen R, De Keyser J, clearance: current understanding, signi- susceptibility weighted imaging and et al. Plasma citrulline levels are increa- ficance and controversy. Front quantitative susceptibility mapping. sed in patients with multiple sclerosis. J Neuroanat 2017;11:101. Magn Reson Imaging 2018;46:130-9. Neurol Sci 2018;387:174-8. 44. Contarino C, Toro EF. A one-dimensio- 55. Wang Y, Chen Y, Wu D, et al. 32. D’haeseleer M, Beelen R, Fierens Y, et nal mathematical model of collecting STrategically Acquired Gradient Echo al. Cerebral hypoperfusion in multiple lymphatics coupled with an electro- (STAGE) imaging, part II: Correcting sclerosis is reversible and mediated by fluid-mechanical contraction model and for RF inhomogeneities in estimating endothelin-1. Proc Natl Acad Sci U S A valve dynamics. Biomech Model T1 and proton density. Magn Reson 2013;110:5654-8. Mechanobiol 2018 [Epub ahead of Imaging 2018;46:140-50. 33. Monti L, Donati D, Menci E, et al. print]. 56. Aydin E, Quliyev H, Cinar C, et al. Cerebral circulation time is prolonged 45. Warnert EA, Murphy K, Hall JE, Wise Eagle syndrome presenting with neuro- and not correlated with EDSS in multi- RG. Noninvasive assessment of arterial logical symptoms. Turk Neurosurg ple sclerosis patients: a study using compliance of human cerebral arteries 2018;28:219-25. digital subtracted angiography. PLoS with short inversion time arterial spin 57. Bruno A, Quarto G, Califano L, et al. One 2015;10:e0116681. labeling. J Cereb Blood Flow Metab onlyChronic cerebrospinal venous insuffi- 34. Zamboni P, Zivadinov R. Extracranial 2015;35:461-8. ciency in Ménière’s disease: diagnosis veins in multiple sclerosis: is there a 46. Warnert EA, Hart EC, Hall JE, et al. and treatment. Veins and Lymphatics role for vascular surgery? Eur J Vasc The major cerebral arteries proximal to 2014;3:3854. Endovasc Surg 2018;pii:S1078- the Circle of Willis contribute to cere- 58. Zamboni P, Tesio L, Galimberti S, et al. 5884(18)30387-3. brovascular resistance in humans.use J Efficacy and safety of extracranial vein 35. Zamboni P, Sisini F, Menegatti E, et al. Cereb Blood Flow Metab angioplasty in multiple sclerosis: a ran- Ultrasound monitoring of jugular 2016;36:1384-95. domized clinical trial. JAMA Neurol venous pulse during space missions: 47. Krishnamurthy S, Li J, Shen Y, et al. 2018;75:35-43. proof of concept. Ultrasound Med Biol Normal macromolecular clearance out 59. Juurlink BHJ, Bavera PM, Sclafani S, et 2018;44:726-33. of the ventricles is delayed in hydroce- al. Brave Dreams: an overestimated 36. Alexander JS, Zivadinov R, Maghzi phalus. Brain Res 2018;1678:337-55. AH, et al. Multiple sclerosis and cere- 48. Dwyer MG, Bergsland N, Ramasamy study, crippled by recruitment failure ad bral endothelial dysfunction: mecha- DP, et al. Atrophied brain lesion volu- misleading conclusions. Veins and nisms. Pathophysiology 2011;18:3-12. me: a new imaging biomarker in multi- Lymphatics 2018;7:7340. 37. Yun JW, Xiao A, Tsunoda I, et al. From ple sclerosis. J Neuroimaging 2018; 60. Zivadinov R, Ramasamy DP, Benedict trash to treasure: the untapped potential 28:490-5. RR, et al. Cerebral microbleeds in mul- of endothelial microparticles in neuro- 49. Lin F, Zivadinov R, Hagemeier J, et al. tiple sclerosis evaluated on susceptibili- vascular diseases. Pathophysiology Altered nuclei-specific thalamic fun- ty-weighted images and quantitative 2016;23:265-74. ctional connectivity patterns in multiple susceptibility maps: a case-control 38. Shrestha B, Prasai PK, Kaskas AM, et sclerosis and their associations with study. Radiology 2016;281:884-95. al. Differential arterial andNon-commercial venous fatigue and cognition. Mult Scler 2018 61. Ghanaat M, Goldenberg C, Walsh J, endothelial redox responses to oxidative [Epub ahead of print]. Sclafani SJ. Endovascular management stress. Microcirculation 2018;e12486. 50. Van Beek EJR, Kuhl C, Anzai Y, et al. of an intracardiac bullet. Injury 39. Liu S, Buch S, Chen Y, et al. Value of MRI in medicine: more than 2015;46:166-8. Susceptibility-weighted imaging: cur- just another test? J Magn Reson 62. Ma X, Bai Y, Lin Y, et al. Amide proton rent status and future directions. NMR Imaging 2018 [Epub ahead of print]. transfer magnetic resonance imaging in Biomed 2017;30. 51. Fu W, Cao S, Liu B, et al. Association detecting intracranial hemorrhage at 40. Lee BB. Venous malformation and hae- of general and central adiposity with different stages: a comparative study mangioma: differential diagnosis, dia- blood pressure among Chinese adults: with susceptibility weighted imaging. gnosis, natural history and consequen- results from the China National Stroke Sci Rep 2017;7:45696. ces. Phlebology 2013;28:176-87. Prevention Project. J Hypertens 2018 63. Wang M, Hong X, Chang CF, et al. 41. Lee BB, Baumgartner I, Berlien P, et al. [Epub ahead of print]. Simultaneous detection and separation Diagnosis and treatment of venous mal- 52. Zhang P, Wang J, Xu Q, et al. Altered of hyperacute intracerebral hemorrhage formations. Consensus Document of the functional connectivity in post-ische- and cerebral ischemia using amide pro- International Union of Phlebology mic stroke depression: a resting-state ton transfer MRI. Magn Reson Med (IUP): updated 2013. Int Angiol functional magnetic resonance imaging 2015;74:42-50.

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