Chronic cerebrospinal venous insufficiency and multiple sclerosis Review article
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Published:
Sep 30, 2013
Keywords:
chronic cerebrospinal venous insufficiency, CCSVI, multiple sclerosis
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Abstract
The chronic cerebrospinal venous insufficiency (CCSVI) arouses a lot of controversies concerning its role in pathogenesis of multiple sclerosis (SM). The knowledge about CCSVI has spread among patients with SM and the treatment method, named after its author Liberation, raised great hopes. The author presents the data from publications, which suggest the crucial cause-effect relationship between CCSVI and SM, as well as the remarks of many authors questioning the existence of such a relationship. Moreover, the author puts forward the stand of FDA and a national consultant in the field of neurology.
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References
1. Charcot J.: Histology of multiple sclerosis. Gaz. Hopit. Civils Milit. 1868; 41: 554-566.
2. Putnam T.: The pathogenesis of multiple sclerosis, a possible vascular factor. N. Engl. J. Med. 1933; 209: 786-790.
3. Putnam T., Adler A.: Vascular architecture of the lesions of multiple sclerosis. Arch. Neurol. Psychiatry 1937; 38: 1-15.
4. Fog T.: The topography of plaques in multiple sclerosis with special reference to cerebral plaques. Acta Neurol. Scand. Suppl. 1965; 15: 1-161.
5. 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.
6. 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.
7. Gisolf J., van Lieshout J.J., van Heusden K. et al.: Human cerebral venous outflow pathway depends on posture and central venous pressure. J. Physiol. 2004; 560: 317-27.
8. Dolic K., Weinstock-Guttman B., Marr K.: Risk factors for chronic cerebrospinal venous insufficiency (CCSVI) in a large cohort of volunteers. 2011; 6(11): e28062.
9. Zamboni P.: The big idea: iron-dependent inflammation in venous disease and proposed parallels in multiple sclerosis. J. R. Soc. Med. 2006; 99(11): 589-93.
10. Khan O., Filippi M., Freedman M.S. et al.: Chronic cerebrospinal venous insufficiency and multiple sclerosis. Ann. Neurol. 2010; 67(3): 286-90.
11. Kurtzke J.F.: A reassessment of the distribution of multiple sclerosis. Acta Neurol. Scand. 1975; 51(2): 137-157.
12. Rosati G.: The prevalence of multiple sclerosis in the world: an update. Neurol. Sci. 2001; 22(2): 117-139.
13. Worthington V., Killestein J., Eikelenboom M.J. et al.: Normal CSF ferritin levels in MS suggest against etiologic role of chronic venous insufficiency. Neurology 2010; 2; 75(18): 1617-22.
14. van Rensburg S.J., van Toorn R. et al.: The controversy of CCSVI and iron in multiple sclerosis: is ferritin the key? Neurology 2010; 75(18): 1581-2.
15. Hill A.B.: The environment and disease: association or causation? Proc. R. Soc. Med. 1965; 58: 295-300.
16. Bagert B., Marder E., Stüve O.: Chronic Cerebrospinal Venous Insufficiency and Multiple Sclerosis. Arch. Neurol. 2011; 68(11): 1379-1384.
17. Singh A.V., Zamboni P.: Anomalous venous blood flow and iron deposition in multiple sclerosis. J. Cereb. Blood Flow Metab. 2009; 29(12): 1867-1878.
18. Zivadinov R., Schirda C., Dwyer M.G. et al.: Chronic cerebrospinal venous insufficiency and iron deposition on susceptibility-weighted imaging in patients with multiple sclerosis: a pilot case-control study. Int. Angiol. 2010; 29(2): 158-175.
19. Haacke E.M., Garbern J., Miao Y. et al.: Iron stores and cerebral veins in MS studied by susceptibility weighted imaging. Int. Angiol. 2010; 29(2): 149-157.
20. Confavreux C., Hutchinson M., Hours M.M. et al.: Pregnancy in Multiple Sclerosis Group. Rate of pregnancy-related relapse in multiple sclerosis. N. Engl. J. Med. 1998; 339(5): 285-291.
21. Bernardi S., Grasso M.G., Bertollini R. et al.: The influence of pregnancy on relapses in multiple sclerosis: a cohort study. Acta Neurol. Scand. 1991; 84(5): 403-406.
22. Handel A.E., Williamson A.J., Disanto G. et al.: An updated meta-analysis of risk of multiple sclerosis following infectious mononucleosis. PLoS One 2010; 5(9): e12496.
23. Munger K.L., Zhang S.M., O’Reilly E. et al.: Vitamin D intake and incidence of multiple sclerosis. Neurology 2004; 62(1): 60-65.
24. Levin L.I., Munger K.L., Rubertone M.V. et al.: Multiple sclerosis and Epstein-Barr virus. JAMA 2003; 289(12): 1533-1536 [retracted in JAMA 2005; 293(20): 2466].
25. Qiu J.: Venous abnormalities and multiple sclerosis: another breakthrough claim? Lancet Neurol. 2010; 9(5): 464-465.
26. 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.
27. Zivadinov R., Marr K., Ramanathan M. et al.: Combined transcranial and extracranial venous Doppler evaluation (CTEVD study): description of the design and interim results of an epidemiological study of the prevalence of chronic cerebrospinal venous insufficiency in MS and related diseases. Poster presented at: Annual Meeting of the American Academy of Neurology; April 15, 2010; Toronto, ON.
28. Doepp F., Paul F., Valdueza J.M. et al.: No cerebrocervical venous congestion in patients with multiple sclerosis. Ann. Neurol. 2010; 68(2): 173-183.
29. Sundström P., Wĺhlin A., Ambarki K. et al.: Venous and cerebrospinal fluid flow in multiple sclerosis: a case-control study. Ann. Neurol. 2010; 68(2): 255-259.
30. Wattjes M.P., van Oosten B.W., de Graaf W.L. et al.: No association of abnormal cranial venous drainage with multiple sclerosis: a magnetic resonance venography and flow-quantification study. J. Neurol. Neurosurg. Psychiatry 2011; 82(4): 429-435.
31. 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.
32. Tan I.L., van Schijndel R.A., Pouwels P.J. et al.: MR venography of multiple sclerosis. AJNR Am. J. Neuroradiol. 2000; 21(6): 1039-42.
33. Grabner G., Dal-Bianco A., Schernthaner M. et al.: Analysis of multiple sclerosis lesions using a fusion of 3.0 T FLAIR and 7.0 T SWI phase: FLAIR SWI. J. Magn. Reson Imaging 2011; 33(3): 543-9.
34. Tallantyre E.C., Morgan P.S., Dixon J.E. et al.: 3 Tesla and 7 Tesla MRI of multiple sclerosis cortical lesions. J. Magn. Reson. Imaging 2010; 32(4): 971-7.
35. Hammond K.E., Metcalf M., Carvajal L. et al.: Quantitative in vivo magnetic resonance imaging of multiple sclerosis at 7 Tesla with sensitivity to iron. Ann. Neurol. 2008; 64(6): 707-13.
36. Haacke E.M., Mittal S., Wu Z. et al.: Susceptibility-weighted imaging: technical aspects and clinical applications, part 1. AJNR Am. J. Neuroradiol. 2009; 30(1): 19-30.
37. Ge Y., Zohrabian V.M., Osa E.O. et al.: Diminished visibility of cerebral venous vasculature in multiple sclerosis by susceptibility-weighted imaging at 3.0 Tesla. J. Magn. Reson Imaging. 2009 ; 29(5): 1190-4.
38. Zivadinov R., Poloni G., Schirda C. et al.: Presence and severity of chronic cerebrospinal venous insufficiency is related to lower brain parenchyma venous vasculature visibility on susceptibility-weighted imaging in patients with multiple sclerosis. Multiple Sclerosis 2010; 16 (supl. 10): O82, S24.
39. Adhya S., Johnson G., Herbert J. et al.: Pattern of hemodynamic impairment in multiple sclerosis: dynamic susceptibility contrast perfusion MR imaging at 3.0 T. Neuroimage 2006; 33(4): 1029-35.
40. Coen M., Menegatti E., Salvi F.: Altered collagen expression in jugular veins in multiple sclerosis. Cardiovasc. Pathol. 2013; 22(1): 33-38.
41. Chopard R.P., Miranda Neto M.H., Biazotto W. et al.: Age-related changes in the human renal veins and their valves. Ital. J. Anat. Embryol. 1994; 99(2): 91-101.
42. Lanzillo R., Mancini M., Liuzzi R. et al.: Chronic cerebrospinal venous insufficiency in multiple sclerosis: a highly prevalent age-dependent phenomenon BMC Neurology 2013; 13: 20.
43. 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.
44. Aksungar F.B., Topkaya A.E., Yildiz Z. et al.: Coagulation status and biochemical and inflammatory markers in multiple sclerosis. J. Clin. Neurosci. 2008; 15(4): 393-397.
45. 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.
46. Zamboni P., Menegatti E., Weinstock-Guttman B. et al.: The severity of chronic cerebrospinal venous insufficiency in patients with multiple sclerosis is related to altered cerebrospinal fluid dynamics. Funct. Neurol. 2009; 24(3): 133-8.
47. Zivadinov R., Marr K., Cutter G. et al.: Prevalence, sensitivity, and specificity of chronic cerebrospinal venous insufficiency in MS. Neurology 2011; 77(2): 138-44.
48. Weinstock-Guttman B., Cutter G., Hojnacki D. et al.: Clinical correlates of chronic cerebrospinal venous insufficiency in multiple sclerosis. Mult. Scler. 2010; 16 (Suppl.10): P653, S224.
49. Zivadinov R., Cutter G., Marr K. et al.: MRI results of blinded chronic cerebrospinal venous insufficiency study in patients with multiple sclerosis, healthy controls and patients with other neurologic diseases. Multiple Sclerosis 2010; 16 (sup. 10): P318, S399.
50. Weinstock-Guttman B., Zivadinov R., Cutter R. et al.: Chronic Cerebrospinal Vascular Insufficiency Is Not Associated with HLA DRB1*1501 Status in Multiple Sclerosis Patients 2011. PLoS One 6(2), e16802.
51. Fox R.: Chronic Cerebrospinal Venous Insufficiency: have we found the cause of cure of MS? Neurology 2011; 77: 1-4.
52. Benedict R.H., Weinstock-Guttmam B., Marr K.: Chronic cerebrospinal venous insufficiency is not associated with cognitive impairment in multiple sclerosis. BMC Med. 2013; 11: 167.
53. FDA Safety Communication: Chronic Cerebrospinal Venous Insufficiency Treatment in Multiple Sclerosis Patients. Date Issued: May 10, 2012.
54. Comi G., Battaglia M.A., Bertolotto A. et al.: Italian multicentre observational study of the prevalence of CCSVI in multiple sclerosis (CoSMo study): rationale, design, and methodology. Neurol. Sci. 2013; 34(8): 1297-307.
55. Leone M.A., Raymkulova O., Naldi P. et al.: Chronic cerebrospinal venous insufficiency is not associated with multiple sclerosis and its severity: a blind-verified study. PLoS One 2013; 8(2): e56031.
56. Mayer C.A., Pfeilschifter W., Lorenz M.W. et al.: The perfect crime? CCSVI not leaving a trace in MS. J. Neurol. Neurosurg. Psychiatry 2011; 82(4): 436-40.
57. Barreto A.D., Brod S.A., Bui T.T. et al.: Chronic cerebrospinal venous insufficiency: Case-control neurosonography results. Ann. Neurol. 2013; 73(6): 721-8.
58. Blinkenberg M., Akeson P., Sillesen H. et al.: Chronic cerebrospinal venous insufficiency and venous stenoses in multiple sclerosis. Acta Neurol. Scand. 2012; 126(6): 421-7.
59. McAuliffe W., Kermode A.G. et al.: Mystery of Chronic Cerebrospinal Venous Insufficiency: Identical Venographic and Ultrasound Findings in Patients with MS and Controls. AJNR Am. J. Neuroradiol. 2013; 34(7): 1370-4.
60. Amato M.P., Saia V., Hakiki B.: No association between chronic cerebrospinal venous insufficiency and pediatric-onset multiple sclerosis. Mult. Scler. 2012; 18(12): 1791-6.
61. Ghezzi A., Annovazzi P., Cocco E.: Endovascular treatment of CCSVI in patients with multiple sclerosis: clinical outcome of 462 cases. Neurol. Sci. 2013 [online].
62. Ghezzi A., Annovazzi P., Amato M.P. et al.: Adverse events after endovascular treatment of chronic cerebro-spinal venous insufficiency (CCSVI) in patients with multiple sclerosis. Mult. Scler. 2013; 19(7): 961-3.
63. Kostecki J., Zaniewski M., Ziaja K. et al.: An endovascular treatment of Chronic Cerebro-Spinal Venous Insufficiency in multiple sclerosis patients – 6 month follow-up results. Neuro. Endocrinol. Lett. 2011; 32(4): 557-62.
64. Zagaglia S., Balestrini S., Perticaroli E. et al.: Percutaneous transluminal angioplasty for chronic cerebrospinal venous insufficiency in multiple sclerosis: dichotomy between subjective and objective outcome scores [online].
2. Putnam T.: The pathogenesis of multiple sclerosis, a possible vascular factor. N. Engl. J. Med. 1933; 209: 786-790.
3. Putnam T., Adler A.: Vascular architecture of the lesions of multiple sclerosis. Arch. Neurol. Psychiatry 1937; 38: 1-15.
4. Fog T.: The topography of plaques in multiple sclerosis with special reference to cerebral plaques. Acta Neurol. Scand. Suppl. 1965; 15: 1-161.
5. 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.
6. 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.
7. Gisolf J., van Lieshout J.J., van Heusden K. et al.: Human cerebral venous outflow pathway depends on posture and central venous pressure. J. Physiol. 2004; 560: 317-27.
8. Dolic K., Weinstock-Guttman B., Marr K.: Risk factors for chronic cerebrospinal venous insufficiency (CCSVI) in a large cohort of volunteers. 2011; 6(11): e28062.
9. Zamboni P.: The big idea: iron-dependent inflammation in venous disease and proposed parallels in multiple sclerosis. J. R. Soc. Med. 2006; 99(11): 589-93.
10. Khan O., Filippi M., Freedman M.S. et al.: Chronic cerebrospinal venous insufficiency and multiple sclerosis. Ann. Neurol. 2010; 67(3): 286-90.
11. Kurtzke J.F.: A reassessment of the distribution of multiple sclerosis. Acta Neurol. Scand. 1975; 51(2): 137-157.
12. Rosati G.: The prevalence of multiple sclerosis in the world: an update. Neurol. Sci. 2001; 22(2): 117-139.
13. Worthington V., Killestein J., Eikelenboom M.J. et al.: Normal CSF ferritin levels in MS suggest against etiologic role of chronic venous insufficiency. Neurology 2010; 2; 75(18): 1617-22.
14. van Rensburg S.J., van Toorn R. et al.: The controversy of CCSVI and iron in multiple sclerosis: is ferritin the key? Neurology 2010; 75(18): 1581-2.
15. Hill A.B.: The environment and disease: association or causation? Proc. R. Soc. Med. 1965; 58: 295-300.
16. Bagert B., Marder E., Stüve O.: Chronic Cerebrospinal Venous Insufficiency and Multiple Sclerosis. Arch. Neurol. 2011; 68(11): 1379-1384.
17. Singh A.V., Zamboni P.: Anomalous venous blood flow and iron deposition in multiple sclerosis. J. Cereb. Blood Flow Metab. 2009; 29(12): 1867-1878.
18. Zivadinov R., Schirda C., Dwyer M.G. et al.: Chronic cerebrospinal venous insufficiency and iron deposition on susceptibility-weighted imaging in patients with multiple sclerosis: a pilot case-control study. Int. Angiol. 2010; 29(2): 158-175.
19. Haacke E.M., Garbern J., Miao Y. et al.: Iron stores and cerebral veins in MS studied by susceptibility weighted imaging. Int. Angiol. 2010; 29(2): 149-157.
20. Confavreux C., Hutchinson M., Hours M.M. et al.: Pregnancy in Multiple Sclerosis Group. Rate of pregnancy-related relapse in multiple sclerosis. N. Engl. J. Med. 1998; 339(5): 285-291.
21. Bernardi S., Grasso M.G., Bertollini R. et al.: The influence of pregnancy on relapses in multiple sclerosis: a cohort study. Acta Neurol. Scand. 1991; 84(5): 403-406.
22. Handel A.E., Williamson A.J., Disanto G. et al.: An updated meta-analysis of risk of multiple sclerosis following infectious mononucleosis. PLoS One 2010; 5(9): e12496.
23. Munger K.L., Zhang S.M., O’Reilly E. et al.: Vitamin D intake and incidence of multiple sclerosis. Neurology 2004; 62(1): 60-65.
24. Levin L.I., Munger K.L., Rubertone M.V. et al.: Multiple sclerosis and Epstein-Barr virus. JAMA 2003; 289(12): 1533-1536 [retracted in JAMA 2005; 293(20): 2466].
25. Qiu J.: Venous abnormalities and multiple sclerosis: another breakthrough claim? Lancet Neurol. 2010; 9(5): 464-465.
26. 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.
27. Zivadinov R., Marr K., Ramanathan M. et al.: Combined transcranial and extracranial venous Doppler evaluation (CTEVD study): description of the design and interim results of an epidemiological study of the prevalence of chronic cerebrospinal venous insufficiency in MS and related diseases. Poster presented at: Annual Meeting of the American Academy of Neurology; April 15, 2010; Toronto, ON.
28. Doepp F., Paul F., Valdueza J.M. et al.: No cerebrocervical venous congestion in patients with multiple sclerosis. Ann. Neurol. 2010; 68(2): 173-183.
29. Sundström P., Wĺhlin A., Ambarki K. et al.: Venous and cerebrospinal fluid flow in multiple sclerosis: a case-control study. Ann. Neurol. 2010; 68(2): 255-259.
30. Wattjes M.P., van Oosten B.W., de Graaf W.L. et al.: No association of abnormal cranial venous drainage with multiple sclerosis: a magnetic resonance venography and flow-quantification study. J. Neurol. Neurosurg. Psychiatry 2011; 82(4): 429-435.
31. 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.
32. Tan I.L., van Schijndel R.A., Pouwels P.J. et al.: MR venography of multiple sclerosis. AJNR Am. J. Neuroradiol. 2000; 21(6): 1039-42.
33. Grabner G., Dal-Bianco A., Schernthaner M. et al.: Analysis of multiple sclerosis lesions using a fusion of 3.0 T FLAIR and 7.0 T SWI phase: FLAIR SWI. J. Magn. Reson Imaging 2011; 33(3): 543-9.
34. Tallantyre E.C., Morgan P.S., Dixon J.E. et al.: 3 Tesla and 7 Tesla MRI of multiple sclerosis cortical lesions. J. Magn. Reson. Imaging 2010; 32(4): 971-7.
35. Hammond K.E., Metcalf M., Carvajal L. et al.: Quantitative in vivo magnetic resonance imaging of multiple sclerosis at 7 Tesla with sensitivity to iron. Ann. Neurol. 2008; 64(6): 707-13.
36. Haacke E.M., Mittal S., Wu Z. et al.: Susceptibility-weighted imaging: technical aspects and clinical applications, part 1. AJNR Am. J. Neuroradiol. 2009; 30(1): 19-30.
37. Ge Y., Zohrabian V.M., Osa E.O. et al.: Diminished visibility of cerebral venous vasculature in multiple sclerosis by susceptibility-weighted imaging at 3.0 Tesla. J. Magn. Reson Imaging. 2009 ; 29(5): 1190-4.
38. Zivadinov R., Poloni G., Schirda C. et al.: Presence and severity of chronic cerebrospinal venous insufficiency is related to lower brain parenchyma venous vasculature visibility on susceptibility-weighted imaging in patients with multiple sclerosis. Multiple Sclerosis 2010; 16 (supl. 10): O82, S24.
39. Adhya S., Johnson G., Herbert J. et al.: Pattern of hemodynamic impairment in multiple sclerosis: dynamic susceptibility contrast perfusion MR imaging at 3.0 T. Neuroimage 2006; 33(4): 1029-35.
40. Coen M., Menegatti E., Salvi F.: Altered collagen expression in jugular veins in multiple sclerosis. Cardiovasc. Pathol. 2013; 22(1): 33-38.
41. Chopard R.P., Miranda Neto M.H., Biazotto W. et al.: Age-related changes in the human renal veins and their valves. Ital. J. Anat. Embryol. 1994; 99(2): 91-101.
42. Lanzillo R., Mancini M., Liuzzi R. et al.: Chronic cerebrospinal venous insufficiency in multiple sclerosis: a highly prevalent age-dependent phenomenon BMC Neurology 2013; 13: 20.
43. 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.
44. Aksungar F.B., Topkaya A.E., Yildiz Z. et al.: Coagulation status and biochemical and inflammatory markers in multiple sclerosis. J. Clin. Neurosci. 2008; 15(4): 393-397.
45. 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.
46. Zamboni P., Menegatti E., Weinstock-Guttman B. et al.: The severity of chronic cerebrospinal venous insufficiency in patients with multiple sclerosis is related to altered cerebrospinal fluid dynamics. Funct. Neurol. 2009; 24(3): 133-8.
47. Zivadinov R., Marr K., Cutter G. et al.: Prevalence, sensitivity, and specificity of chronic cerebrospinal venous insufficiency in MS. Neurology 2011; 77(2): 138-44.
48. Weinstock-Guttman B., Cutter G., Hojnacki D. et al.: Clinical correlates of chronic cerebrospinal venous insufficiency in multiple sclerosis. Mult. Scler. 2010; 16 (Suppl.10): P653, S224.
49. Zivadinov R., Cutter G., Marr K. et al.: MRI results of blinded chronic cerebrospinal venous insufficiency study in patients with multiple sclerosis, healthy controls and patients with other neurologic diseases. Multiple Sclerosis 2010; 16 (sup. 10): P318, S399.
50. Weinstock-Guttman B., Zivadinov R., Cutter R. et al.: Chronic Cerebrospinal Vascular Insufficiency Is Not Associated with HLA DRB1*1501 Status in Multiple Sclerosis Patients 2011. PLoS One 6(2), e16802.
51. Fox R.: Chronic Cerebrospinal Venous Insufficiency: have we found the cause of cure of MS? Neurology 2011; 77: 1-4.
52. Benedict R.H., Weinstock-Guttmam B., Marr K.: Chronic cerebrospinal venous insufficiency is not associated with cognitive impairment in multiple sclerosis. BMC Med. 2013; 11: 167.
53. FDA Safety Communication: Chronic Cerebrospinal Venous Insufficiency Treatment in Multiple Sclerosis Patients. Date Issued: May 10, 2012.
54. Comi G., Battaglia M.A., Bertolotto A. et al.: Italian multicentre observational study of the prevalence of CCSVI in multiple sclerosis (CoSMo study): rationale, design, and methodology. Neurol. Sci. 2013; 34(8): 1297-307.
55. Leone M.A., Raymkulova O., Naldi P. et al.: Chronic cerebrospinal venous insufficiency is not associated with multiple sclerosis and its severity: a blind-verified study. PLoS One 2013; 8(2): e56031.
56. Mayer C.A., Pfeilschifter W., Lorenz M.W. et al.: The perfect crime? CCSVI not leaving a trace in MS. J. Neurol. Neurosurg. Psychiatry 2011; 82(4): 436-40.
57. Barreto A.D., Brod S.A., Bui T.T. et al.: Chronic cerebrospinal venous insufficiency: Case-control neurosonography results. Ann. Neurol. 2013; 73(6): 721-8.
58. Blinkenberg M., Akeson P., Sillesen H. et al.: Chronic cerebrospinal venous insufficiency and venous stenoses in multiple sclerosis. Acta Neurol. Scand. 2012; 126(6): 421-7.
59. McAuliffe W., Kermode A.G. et al.: Mystery of Chronic Cerebrospinal Venous Insufficiency: Identical Venographic and Ultrasound Findings in Patients with MS and Controls. AJNR Am. J. Neuroradiol. 2013; 34(7): 1370-4.
60. Amato M.P., Saia V., Hakiki B.: No association between chronic cerebrospinal venous insufficiency and pediatric-onset multiple sclerosis. Mult. Scler. 2012; 18(12): 1791-6.
61. Ghezzi A., Annovazzi P., Cocco E.: Endovascular treatment of CCSVI in patients with multiple sclerosis: clinical outcome of 462 cases. Neurol. Sci. 2013 [online].
62. Ghezzi A., Annovazzi P., Amato M.P. et al.: Adverse events after endovascular treatment of chronic cerebro-spinal venous insufficiency (CCSVI) in patients with multiple sclerosis. Mult. Scler. 2013; 19(7): 961-3.
63. Kostecki J., Zaniewski M., Ziaja K. et al.: An endovascular treatment of Chronic Cerebro-Spinal Venous Insufficiency in multiple sclerosis patients – 6 month follow-up results. Neuro. Endocrinol. Lett. 2011; 32(4): 557-62.
64. Zagaglia S., Balestrini S., Perticaroli E. et al.: Percutaneous transluminal angioplasty for chronic cerebrospinal venous insufficiency in multiple sclerosis: dichotomy between subjective and objective outcome scores [online].