Skip to main content
Top
Published in: BMC Neurology 1/2013

Open Access 01-12-2013 | Research article

Chronic cerebrospinal venous insufficiency in multiple sclerosis: a highly prevalent age-dependent phenomenon

Authors: Roberta Lanzillo, Marcello Mancini, Raffaele Liuzzi, Orlando Di Donato, Elena Salvatore, Valentina Maglio, Giovanni Vacca, Luca Amato, Gennaro D’Anna, Arturo Brunetti, Vincenzo Brescia Morra

Published in: BMC Neurology | Issue 1/2013

Login to get access

Abstract

Background

This study aimed to investigate the prevalence and clinical relevance of chronic cerebrospinal venous insufficiency (CCSVI) in multiple sclerosis (MS) patients and healthy controls using extra- and intracranial colour Doppler sonography.

Methods

We examined 146 MS patients, presenting with a clinically isolated syndrome, relapsing-remitting, secondary progressive, or primary progressive MS, and 38 healthy controls. Sonographic examination was performed according to Zamboni’s protocol and was performed by three independent sonographers. The results of sonographic examination were compared with clinical and demographic characteristics of the patients.

Results

CCSVI, defined as the presence of at least two positive Zamboni’s criteria, was found in 76% of MS patients and 16% of control subjects. B-mode anomalies of internal jugular veins, such as stenosis, malformed valves, annuli, and septa were the most common lesions detected in MS patients (80.8%) and controls (47.4%). We observed a positive correlation between sonographic diagnosis of CCSVI and the patients’ age (p = 0.003). However, such a correlation was not found in controls (p = 0.635). Notably, no significant correlations were found between sonographic signs of CCSVI and clinical characteristics of MS, except for absent flow in the jugular veins, which was found more often in primary (p<0.005) and secondary (p<0.05) progressive patients compared with non-progressive patients. Absent flow in jugular veins was significantly correlated with patients’ age (p < 0.0001).

Conclusions

Sonographically defined CCSVI is common in MS patients. However, CCSVI appears to be primarily associated with the patient’s age, and poorly correlated with the clinical course of the disease.
Appendix
Available only for authorised users
Literature
1.
go back to reference Frohman EM, Racke MK, Raine CS: Multiple sclerosis–the plaque and its pathogenesis. N Engl J Med. 2006, 354 (9): 942-955. 10.1056/NEJMra052130.CrossRefPubMed Frohman EM, Racke MK, Raine CS: Multiple sclerosis–the plaque and its pathogenesis. N Engl J Med. 2006, 354 (9): 942-955. 10.1056/NEJMra052130.CrossRefPubMed
2.
go back to reference Lassmann H: Hypoxia-like tissue injury as a component of multiple sclerosis lesions. J Neurol Sci. 2003, 206 (2): 187-191. 10.1016/S0022-510X(02)00421-5.CrossRefPubMed Lassmann H: Hypoxia-like tissue injury as a component of multiple sclerosis lesions. J Neurol Sci. 2003, 206 (2): 187-191. 10.1016/S0022-510X(02)00421-5.CrossRefPubMed
3.
go back to reference Law M, Saindane AM, Ge Y, et al: Microvascular abnormality in relapsing-remitting multiple sclerosis: perfusion MR imaging findings in normal-appearing white matter. Radiology. 2004, 231 (3): 645-652. 10.1148/radiol.2313030996.CrossRefPubMed Law M, Saindane AM, Ge Y, et al: Microvascular abnormality in relapsing-remitting multiple sclerosis: perfusion MR imaging findings in normal-appearing white matter. Radiology. 2004, 231 (3): 645-652. 10.1148/radiol.2313030996.CrossRefPubMed
4.
go back to reference Zamboni P, Galeotti R, Menegatti E, et al: Chronic cerebrospinal venous insufficiency in patients with multiple sclerosis. J Neurol Neurosurg Psychiatry. 2009, 80 (4): 392-399.CrossRefPubMed Zamboni P, Galeotti R, Menegatti E, et al: Chronic cerebrospinal venous insufficiency in patients with multiple sclerosis. J Neurol Neurosurg Psychiatry. 2009, 80 (4): 392-399.CrossRefPubMed
5.
go back to reference Lugli M, Morelli M, Guerzoni S, et al: The hypothesis of patho-physiological correlation between chronic cerebrospinal venous insufficiency and multiple sclerosis: rationale of treatment. Phlebology. 2012, 27 (Suppl 1): 178-186.CrossRefPubMed Lugli M, Morelli M, Guerzoni S, et al: The hypothesis of patho-physiological correlation between chronic cerebrospinal venous insufficiency and multiple sclerosis: rationale of treatment. Phlebology. 2012, 27 (Suppl 1): 178-186.CrossRefPubMed
6.
go back to reference Simka M, Latacz P, Ludyga T, et al: Prevalence of extracranial venous abnormalities: results from a sample of 586 multiple sclerosis patients. Funct Neurol. 2011, 26 (4): 197-203.PubMed Simka M, Latacz P, Ludyga T, et al: Prevalence of extracranial venous abnormalities: results from a sample of 586 multiple sclerosis patients. Funct Neurol. 2011, 26 (4): 197-203.PubMed
7.
go back to reference Simka M, Ludyga T, Latacz P, et al: Diagnostic accuracy of current sonographic criteria for the detection of outflow abnormalities in the internal jugular veins. Phlebology. 2012, 10.1258/phleb.2012.011125. Simka M, Ludyga T, Latacz P, et al: Diagnostic accuracy of current sonographic criteria for the detection of outflow abnormalities in the internal jugular veins. Phlebology. 2012, 10.1258/phleb.2012.011125.
8.
go back to reference Yamout B, Herlopian A, Issa Z, et al: Extracranial venous stenosis is an unlikely cause of multiple sclerosis. Mult Scler. 2010, 16 (11): 1341-1348. 10.1177/1352458510385268.CrossRefPubMed Yamout B, Herlopian A, Issa Z, et al: Extracranial venous stenosis is an unlikely cause of multiple sclerosis. Mult Scler. 2010, 16 (11): 1341-1348. 10.1177/1352458510385268.CrossRefPubMed
9.
go back to reference Hojnacki D, Zamboni P, Lopez-Soriano A, et al: Use of neck magnetic resonance venography, Doppler sonography and selective venography for diagnosis of chronic cerebrospinal venous insufficiency: a pilot study in multiple sclerosis patients and healthy controls. Int Angiol. 2010, 29 (2): 127-139.PubMed Hojnacki D, Zamboni P, Lopez-Soriano A, et al: Use of neck magnetic resonance venography, Doppler sonography and selective venography for diagnosis of chronic cerebrospinal venous insufficiency: a pilot study in multiple sclerosis patients and healthy controls. Int Angiol. 2010, 29 (2): 127-139.PubMed
10.
go back to reference Zamboni P, Galeotti R, Menegatti E, et al: A prospective open-label study of endovascular treatment of chronic cerebrospinal venous insufficiency. J Vasc Surg. 2009, 50 (6): 1348-1358. 10.1016/j.jvs.2009.07.096. e1341-1343CrossRefPubMed Zamboni P, Galeotti R, Menegatti E, et al: A prospective open-label study of endovascular treatment of chronic cerebrospinal venous insufficiency. J Vasc Surg. 2009, 50 (6): 1348-1358. 10.1016/j.jvs.2009.07.096. e1341-1343CrossRefPubMed
11.
go back to reference Baracchini C, Perini P, Calabrese M, et al: No evidence of chronic cerebrospinal venous insufficiency at multiple sclerosis onset. Ann Neurol. 2011, 69 (1): 90-99. 10.1002/ana.22228.CrossRefPubMed Baracchini C, Perini P, Calabrese M, et al: No evidence of chronic cerebrospinal venous insufficiency at multiple sclerosis onset. Ann Neurol. 2011, 69 (1): 90-99. 10.1002/ana.22228.CrossRefPubMed
12.
go back to reference Zamboni P, Menegatti E, Galeotti R, et al: The value of cerebral Doppler venous haemodynamics in the assessment of multiple sclerosis. J Neurol Sci. 2009, 282 (1–2): 21-27.CrossRefPubMed Zamboni P, Menegatti E, Galeotti R, et al: The value of cerebral Doppler venous haemodynamics in the assessment of multiple sclerosis. J Neurol Sci. 2009, 282 (1–2): 21-27.CrossRefPubMed
13.
go back to reference Tsivgoulis G, Mantatzis M, Bogiatzi C, et al: Extracranial venous hemodynamics in multiple sclerosis: a case–control study. Neurology. 2011, 77 (13): 1241-1245. 10.1212/WNL.0b013e318230a149.CrossRefPubMed Tsivgoulis G, Mantatzis M, Bogiatzi C, et al: Extracranial venous hemodynamics in multiple sclerosis: a case–control study. Neurology. 2011, 77 (13): 1241-1245. 10.1212/WNL.0b013e318230a149.CrossRefPubMed
14.
go back to reference Zivadinov R, Marr K, Cutter G, et al: Prevalence, sensitivity, and specificity of chronic cerebrospinal venous insufficiency in MS. Neurology. 2011, 77 (2): 138-144. 10.1212/WNL.0b013e318212a901.CrossRefPubMed Zivadinov R, Marr K, Cutter G, et al: Prevalence, sensitivity, and specificity of chronic cerebrospinal venous insufficiency in MS. Neurology. 2011, 77 (2): 138-144. 10.1212/WNL.0b013e318212a901.CrossRefPubMed
15.
go back to reference Garaci FG, Marziali S, Meschini A, et al: Brain hemodynamic changes associated with chronic cerebrospinal venous insufficiency are not specific to multiple sclerosis and do not increase its severity. Radiology. 2012, 265 (1): 233-239. 10.1148/radiol.12112245.CrossRefPubMed Garaci FG, Marziali S, Meschini A, et al: Brain hemodynamic changes associated with chronic cerebrospinal venous insufficiency are not specific to multiple sclerosis and do not increase its severity. Radiology. 2012, 265 (1): 233-239. 10.1148/radiol.12112245.CrossRefPubMed
16.
go back to reference Zamboni P, Menegatti E, Weinstock-Guttman B, et al: Hypoperfusion of brain parenchyma is associated with the severity of chronic cerebrospinal venous insufficiency in patients with multiple sclerosis: a cross-sectional preliminary report. BMC Med. 2011, 9: 22-10.1186/1741-7015-9-22.CrossRefPubMedPubMedCentral Zamboni P, Menegatti E, Weinstock-Guttman B, et al: Hypoperfusion of brain parenchyma is associated with the severity of chronic cerebrospinal venous insufficiency in patients with multiple sclerosis: a cross-sectional preliminary report. BMC Med. 2011, 9: 22-10.1186/1741-7015-9-22.CrossRefPubMedPubMedCentral
17.
go back to reference Baracchini C, Perini P, Causin F, et al: Progressive multiple sclerosis is not associated with chronic cerebrospinal venous insufficiency. Neurology. 2011, 77 (9): 844-850. 10.1212/WNL.0b013e31822c6208.CrossRefPubMed Baracchini C, Perini P, Causin F, et al: Progressive multiple sclerosis is not associated with chronic cerebrospinal venous insufficiency. Neurology. 2011, 77 (9): 844-850. 10.1212/WNL.0b013e31822c6208.CrossRefPubMed
18.
go back to reference Bastianello S, Romani A, Viselner G, et al: Chronic cerebrospinal venous insufficiency in multiple sclerosis: clinical correlates from a multicentre study. BMC Neurol. 2011, 11: 132-10.1186/1471-2377-11-132.CrossRefPubMedPubMedCentral Bastianello S, Romani A, Viselner G, et al: Chronic cerebrospinal venous insufficiency in multiple sclerosis: clinical correlates from a multicentre study. BMC Neurol. 2011, 11: 132-10.1186/1471-2377-11-132.CrossRefPubMedPubMedCentral
19.
go back to reference Centonze D, Floris R, Stefanini M, et al: Proposed chronic cerebrospinal venous insufficiency criteria do not predict multiple sclerosis risk or severity. Ann Neurol. 2011, 70 (1): 51-58.CrossRefPubMed Centonze D, Floris R, Stefanini M, et al: Proposed chronic cerebrospinal venous insufficiency criteria do not predict multiple sclerosis risk or severity. Ann Neurol. 2011, 70 (1): 51-58.CrossRefPubMed
20.
go back to reference McDonald WI, Compston A, Edan G, et al: Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol. 2001, 50 (1): 121-127. 10.1002/ana.1032.CrossRefPubMed McDonald WI, Compston A, Edan G, et al: Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol. 2001, 50 (1): 121-127. 10.1002/ana.1032.CrossRefPubMed
21.
go back to reference Lublin FD, Reingold SC: Defining the clinical course of multiple sclerosis: results of an international survey. National Multiple Sclerosis Society (USA) Advisory Committee on Clinical Trials of New Agents in Multiple Sclerosis. Neurology. 1996, 46 (4): 907-911. 10.1212/WNL.46.4.907.CrossRefPubMed Lublin FD, Reingold SC: Defining the clinical course of multiple sclerosis: results of an international survey. National Multiple Sclerosis Society (USA) Advisory Committee on Clinical Trials of New Agents in Multiple Sclerosis. Neurology. 1996, 46 (4): 907-911. 10.1212/WNL.46.4.907.CrossRefPubMed
22.
go back to reference Kurtzke JF: Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology. 1983, 33 (11): 1444-1452. 10.1212/WNL.33.11.1444.CrossRefPubMed Kurtzke JF: Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology. 1983, 33 (11): 1444-1452. 10.1212/WNL.33.11.1444.CrossRefPubMed
23.
go back to reference Roxburgh RH, Seaman SR, Masterman T, et al: Multiple Sclerosis Severity Score: using disability and disease duration to rate disease severity. Neurology. 2005, 64 (7): 1144-1151. 10.1212/01.WNL.0000156155.19270.F8.CrossRefPubMed Roxburgh RH, Seaman SR, Masterman T, et al: Multiple Sclerosis Severity Score: using disability and disease duration to rate disease severity. Neurology. 2005, 64 (7): 1144-1151. 10.1212/01.WNL.0000156155.19270.F8.CrossRefPubMed
24.
go back to reference Dolic K, Marr K, Valnarov V, et al: Intra- and extraluminal structural and functional venous anomalies in multiple sclerosis, as evidenced by 2 noninvasive imaging techniques. AJNR Am J Neuroradiol. 2012, 33 (1): 16-23. 10.3174/ajnr.A2877.CrossRefPubMed Dolic K, Marr K, Valnarov V, et al: Intra- and extraluminal structural and functional venous anomalies in multiple sclerosis, as evidenced by 2 noninvasive imaging techniques. AJNR Am J Neuroradiol. 2012, 33 (1): 16-23. 10.3174/ajnr.A2877.CrossRefPubMed
25.
go back to reference Mancini M, Morra VB, Di Donato O, et al: Multiple sclerosis: cerebral circulation time. Radiology. 2012, 262 (3): 947-955. 10.1148/radiol.11111239.CrossRefPubMed Mancini M, Morra VB, Di Donato O, et al: Multiple sclerosis: cerebral circulation time. Radiology. 2012, 262 (3): 947-955. 10.1148/radiol.11111239.CrossRefPubMed
26.
go back to reference Coen M, Menegatti E, Salvi F, et al: Altered collagen expression in jugular veins in multiple sclerosis. Cardiovasc Pathol. 2013, 22 (1): 33-38. 10.1016/j.carpath.2012.05.005.CrossRefPubMed Coen M, Menegatti E, Salvi F, et al: Altered collagen expression in jugular veins in multiple sclerosis. Cardiovasc Pathol. 2013, 22 (1): 33-38. 10.1016/j.carpath.2012.05.005.CrossRefPubMed
27.
go back to reference Lee AB, Laredo J, Neville R: Embryological background of truncular venous malformation in the extracranial venous pathways as the cause of chronic cerebro spinal venous insufficiency. Int Angiol. 2010, 29 (2): 95-108.PubMed Lee AB, Laredo J, Neville R: Embryological background of truncular venous malformation in the extracranial venous pathways as the cause of chronic cerebro spinal venous insufficiency. Int Angiol. 2010, 29 (2): 95-108.PubMed
28.
go back to reference Chung CP, Wang PN, Wu YH, et al: More severe white matter changes in the elderly with jugular venous reflux. Ann Neurol. 2011, 69 (3): 553-559. 10.1002/ana.22276.CrossRefPubMed Chung CP, Wang PN, Wu YH, et al: More severe white matter changes in the elderly with jugular venous reflux. Ann Neurol. 2011, 69 (3): 553-559. 10.1002/ana.22276.CrossRefPubMed
29.
go back to reference Muhammad JK, Pugh ND, Boden L, et al: The effect of head rotation on the diameter of the internal jugular vein: implications for free tissue transfer. J Craniomaxillofac Surg. 2001, 29 (4): 214-218. 10.1054/jcms.2001.0225.CrossRefPubMed Muhammad JK, Pugh ND, Boden L, et al: The effect of head rotation on the diameter of the internal jugular vein: implications for free tissue transfer. J Craniomaxillofac Surg. 2001, 29 (4): 214-218. 10.1054/jcms.2001.0225.CrossRefPubMed
30.
go back to reference Buckey JC, Lane LD, Plath G, et al: Effects of head-down tilt for 10 days on the compliance of the leg. Acta Physiol Scand Suppl. 1992, 604: 53-59.PubMed Buckey JC, Lane LD, Plath G, et al: Effects of head-down tilt for 10 days on the compliance of the leg. Acta Physiol Scand Suppl. 1992, 604: 53-59.PubMed
31.
go back to reference Buckey JC, Peshock RM, Blomqvist CG: Deep venous contribution to hydrostatic blood volume change in the human leg. Am J Cardiol. 1988, 62 (7): 449-453. 10.1016/0002-9149(88)90976-9.CrossRefPubMed Buckey JC, Peshock RM, Blomqvist CG: Deep venous contribution to hydrostatic blood volume change in the human leg. Am J Cardiol. 1988, 62 (7): 449-453. 10.1016/0002-9149(88)90976-9.CrossRefPubMed
32.
go back to reference Gottlob MMR: Pathologic venous valves. Venous Valves: Morphology, Function Radiology, Surgery. Edited by: Gottlob RM R. 1986, New York: Springer, 82-92.CrossRef Gottlob MMR: Pathologic venous valves. Venous Valves: Morphology, Function Radiology, Surgery. Edited by: Gottlob RM R. 1986, New York: Springer, 82-92.CrossRef
33.
go back to reference Chopard RP, Miranda Neto MH, Biazotto W, et al: Age-related changes in the human renal veins and their valves. Ital J Anat Embryol. 1994, 99 (2): 91-101.PubMed Chopard RP, Miranda Neto MH, Biazotto W, et al: Age-related changes in the human renal veins and their valves. Ital J Anat Embryol. 1994, 99 (2): 91-101.PubMed
34.
go back to reference Saphir O, Lev M: The venous valve in the aged. Am Heart J. 1952, 44 (6): 843-850. 10.1016/0002-8703(52)90130-0.CrossRefPubMed Saphir O, Lev M: The venous valve in the aged. Am Heart J. 1952, 44 (6): 843-850. 10.1016/0002-8703(52)90130-0.CrossRefPubMed
35.
go back to reference Schina MJ, Neumyer MM, Healy DA, et al: Influence of age on venous physiologic parameters. J Vasc Surg. 1993, 18 (5): 749-752.CrossRefPubMed Schina MJ, Neumyer MM, Healy DA, et al: Influence of age on venous physiologic parameters. J Vasc Surg. 1993, 18 (5): 749-752.CrossRefPubMed
36.
go back to reference van Langevelde K, Sramek A, Rosendaal FR: The effect of aging on venous valves. Arterioscler Thromb Vasc Biol. 2010, 30 (10): 2075-2080. 10.1161/ATVBAHA.110.209049.CrossRefPubMed van Langevelde K, Sramek A, Rosendaal FR: The effect of aging on venous valves. Arterioscler Thromb Vasc Biol. 2010, 30 (10): 2075-2080. 10.1161/ATVBAHA.110.209049.CrossRefPubMed
37.
go back to reference Lurie F, Kistner RL, Eklof B, et al: Mechanism of venous valve closure and role of the valve in circulation: a new concept. J Vasc Surg. 2003, 38 (5): 955-961. 10.1016/S0741-5214(03)00711-0.CrossRefPubMed Lurie F, Kistner RL, Eklof B, et al: Mechanism of venous valve closure and role of the valve in circulation: a new concept. J Vasc Surg. 2003, 38 (5): 955-961. 10.1016/S0741-5214(03)00711-0.CrossRefPubMed
38.
go back to reference Olsen H, Lanne T: Reduced venous compliance in lower limbs of aging humans and its importance for capacitance function. Am J Physiol. 1998, 275 (3 Pt 2): H878-886.PubMed Olsen H, Lanne T: Reduced venous compliance in lower limbs of aging humans and its importance for capacitance function. Am J Physiol. 1998, 275 (3 Pt 2): H878-886.PubMed
39.
go back to reference Young CN, Stillabower ME, DiSabatino A, et al: Venous smooth muscle tone and responsiveness in older adults. J Appl Physiol. 2006, 101 (5): 1362-1367. 10.1152/japplphysiol.00448.2006.CrossRefPubMed Young CN, Stillabower ME, DiSabatino A, et al: Venous smooth muscle tone and responsiveness in older adults. J Appl Physiol. 2006, 101 (5): 1362-1367. 10.1152/japplphysiol.00448.2006.CrossRefPubMed
40.
go back to reference De Keyser J, Steen C, Mostert JP, et al: Hypoperfusion of the cerebral white matter in multiple sclerosis: possible mechanisms and pathophysiological significance. J Cereb Blood Flow Metab. 2008, 28 (10): 1645-1651. 10.1038/jcbfm.2008.72.CrossRefPubMed De Keyser J, Steen C, Mostert JP, et al: Hypoperfusion of the cerebral white matter in multiple sclerosis: possible mechanisms and pathophysiological significance. J Cereb Blood Flow Metab. 2008, 28 (10): 1645-1651. 10.1038/jcbfm.2008.72.CrossRefPubMed
41.
go back to reference Inglese M, Adhya S, Johnson G, et al: Perfusion magnetic resonance imaging correlates of neuropsychological impairment in multiple sclerosis. J Cereb Blood Flow Metab. 2008, 28 (1): 164-171. 10.1038/sj.jcbfm.9600504.CrossRefPubMed Inglese M, Adhya S, Johnson G, et al: Perfusion magnetic resonance imaging correlates of neuropsychological impairment in multiple sclerosis. J Cereb Blood Flow Metab. 2008, 28 (1): 164-171. 10.1038/sj.jcbfm.9600504.CrossRefPubMed
42.
go back to reference Varga AW, Johnson G, Babb JS, et al: White matter hemodynamic abnormalities precede sub-cortical gray matter changes in multiple sclerosis. J Neurol Sci. 2009, 282 (1–2): 28-33.CrossRefPubMedPubMedCentral Varga AW, Johnson G, Babb JS, et al: White matter hemodynamic abnormalities precede sub-cortical gray matter changes in multiple sclerosis. J Neurol Sci. 2009, 282 (1–2): 28-33.CrossRefPubMedPubMedCentral
43.
go back to reference Wuerfel J, Paul F, Zipp F: Cerebral blood perfusion changes in multiple sclerosis. J Neurol Sci. 2007, 259 (1–2): 16-20.CrossRefPubMed Wuerfel J, Paul F, Zipp F: Cerebral blood perfusion changes in multiple sclerosis. J Neurol Sci. 2007, 259 (1–2): 16-20.CrossRefPubMed
44.
go back to reference Zhuang YJ, Singh TM, Zarins CK, et al: Sequential increases and decreases in blood flow stimulates progressive intimal thickening. Eur J Vasc Endovasc Surg. 1998, 16 (4): 301-310. 10.1016/S1078-5884(98)80049-X.CrossRefPubMed Zhuang YJ, Singh TM, Zarins CK, et al: Sequential increases and decreases in blood flow stimulates progressive intimal thickening. Eur J Vasc Endovasc Surg. 1998, 16 (4): 301-310. 10.1016/S1078-5884(98)80049-X.CrossRefPubMed
45.
go back to reference Simka M, Ludyga T, Kazibudzki M, et al: Multiple sclerosis, an unlikely cause of chronic cerebrospinal venous insufficiency: retrospective analysis of catheter venography. J R Soc Med Sh Rep. 2012, 3 (8): 6- Simka M, Ludyga T, Kazibudzki M, et al: Multiple sclerosis, an unlikely cause of chronic cerebrospinal venous insufficiency: retrospective analysis of catheter venography. J R Soc Med Sh Rep. 2012, 3 (8): 6-
46.
go back to reference Aksungar FB, Topkaya AE, Yildiz Z, et al: Coagulation status and biochemical and inflammatory markers in multiple sclerosis. J Clin Neurosci. 2008, 15 (4): 393-397. 10.1016/j.jocn.2007.02.090.CrossRefPubMed Aksungar FB, Topkaya AE, Yildiz Z, et al: Coagulation status and biochemical and inflammatory markers in multiple sclerosis. J Clin Neurosci. 2008, 15 (4): 393-397. 10.1016/j.jocn.2007.02.090.CrossRefPubMed
47.
go back to reference Vandenberghe N, Debouverie M, Anxionnat R, et al: Cerebral venous thrombosis in four patients with multiple sclerosis. Eur J Neurol. 2003, 10 (1): 63-66. 10.1046/j.1468-1331.2003.00513.x.CrossRefPubMed Vandenberghe N, Debouverie M, Anxionnat R, et al: Cerebral venous thrombosis in four patients with multiple sclerosis. Eur J Neurol. 2003, 10 (1): 63-66. 10.1046/j.1468-1331.2003.00513.x.CrossRefPubMed
Metadata
Title
Chronic cerebrospinal venous insufficiency in multiple sclerosis: a highly prevalent age-dependent phenomenon
Authors
Roberta Lanzillo
Marcello Mancini
Raffaele Liuzzi
Orlando Di Donato
Elena Salvatore
Valentina Maglio
Giovanni Vacca
Luca Amato
Gennaro D’Anna
Arturo Brunetti
Vincenzo Brescia Morra
Publication date
01-12-2013
Publisher
BioMed Central
Published in
BMC Neurology / Issue 1/2013
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/1471-2377-13-20

Other articles of this Issue 1/2013

BMC Neurology 1/2013 Go to the issue