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Published in: BMC Medicine 1/2013

Open Access 01-12-2013 | Research article

Chronic cerebrospinal venous insufficiency is not associated with cognitive impairment in multiple sclerosis

Authors: Ralph HB Benedict, Bianca Weinstock-Guttmam, Karen Marr, Vesela Valnarov, Cheryl Kennedy, Ellen Carl, Christina Brooks, David Hojnacki, Robert Zivadinov

Published in: BMC Medicine | Issue 1/2013

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Abstract

Background

Chronic cerebrospinal venous insufficiency (CCSVI) has been reported in multiple sclerosis (MS) yet its significance in relation to cognitive function is undetermined.
This study measured the association between the presence and severity of CCSVI and cognitive impairment in patients with MS.

Methods

CCSVI was assessed using extra-cranial and trans-cranial Doppler sonography in 109 MS patients (79 with relapsing-remitting, 23 with secondary-progressive and 7 with primary-progressive disease subtype). A subject was considered CCSVI-positive if ≥2 venous hemodynamic criteria were fulfilled. The Minimal Assessment of Cognitive Function in MS (MACFIMS) battery was administered assessing the full spectrum of cognitive domains known to be affected by MS. Depression was quantified using the Beck Depression Inventory Fast Screen (BDIFS). Partial correlations, analysis of variance (or covariance) and linear regression were used to examine the hypothesis that CCSVI status is related to cognition or depression after controlling for education and gender.

Results

There were 64 (58.7%) patients who were considered CCSVI-positive. The regression models predicting venous hemodynamic insufficiency severity score were not statistically significant for any of the MACFIMS predictor variables. The analysis of variance tests showed a significant effect of CCSVI-positive diagnosis on cognitive ability in only one of the 10 MACFIMS outcomes, and that one was in the opposite direction of the tested hypothesis. There was no correspondence between CCSVI diagnosis and depression, as measured by the BDIFS.

Conclusions

We find no evidence of an association between the presence and severity of CCSVI with cognitive impairment and depression in patients with MS.
Appendix
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Literature
1.
go back to reference Hauser SL, Oksenberg JR, Hauser SL, Oksenberg JR: The neurobiology of multiple sclerosis: genes, inflammation, and neurodegeneration. Neuron. 2006, 52: 61-76. 10.1016/j.neuron.2006.09.011.CrossRefPubMed Hauser SL, Oksenberg JR, Hauser SL, Oksenberg JR: The neurobiology of multiple sclerosis: genes, inflammation, and neurodegeneration. Neuron. 2006, 52: 61-76. 10.1016/j.neuron.2006.09.011.CrossRefPubMed
2.
go back to reference Trapp BD, Nave KA: Multiple sclerosis: an immune or neurodegenerative disorder?. Annu Rev Neurosci. 2008, 31: 247-269. 10.1146/annurev.neuro.30.051606.094313.CrossRefPubMed Trapp BD, Nave KA: Multiple sclerosis: an immune or neurodegenerative disorder?. Annu Rev Neurosci. 2008, 31: 247-269. 10.1146/annurev.neuro.30.051606.094313.CrossRefPubMed
3.
go back to reference Rao SM, Leo GJ, Bernardin L, Unverzagt F: Cognitive dysfunction in multiple sclerosis. I. Frequency, patterns, and prediction. Neurology. 1991, 41: 685-691. 10.1212/WNL.41.5.685.CrossRefPubMed Rao SM, Leo GJ, Bernardin L, Unverzagt F: Cognitive dysfunction in multiple sclerosis. I. Frequency, patterns, and prediction. Neurology. 1991, 41: 685-691. 10.1212/WNL.41.5.685.CrossRefPubMed
4.
go back to reference Benedict RHB, Cookfair D, Gavett R, Gunther M, Munschauer F, Garg N, Weinstock-Guttman B: Validity of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS). J Int Neuropsychol Soc. 2006, 12: 549-558.CrossRefPubMed Benedict RHB, Cookfair D, Gavett R, Gunther M, Munschauer F, Garg N, Weinstock-Guttman B: Validity of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS). J Int Neuropsychol Soc. 2006, 12: 549-558.CrossRefPubMed
5.
go back to reference Patti F, Amato M, Trojano M, Bastianello S, Tola M, Goretti B, Caniatti L, Di Monte E, Ferrazza P, Brescia Morra V, Lo Fermo S, Picconi O, Luccichenti G, COGIMUS Study Group: Cognitive impairment and its relation with disease measures in mildly disabled patients with relapsing-remitting multiple sclerosis: baseline results from the Cognitive Impairment in Multiple Sclerosis (COGIMUS) study. Mult Scler. 2009, 15: 779-788. 10.1177/1352458509105544.CrossRefPubMed Patti F, Amato M, Trojano M, Bastianello S, Tola M, Goretti B, Caniatti L, Di Monte E, Ferrazza P, Brescia Morra V, Lo Fermo S, Picconi O, Luccichenti G, COGIMUS Study Group: Cognitive impairment and its relation with disease measures in mildly disabled patients with relapsing-remitting multiple sclerosis: baseline results from the Cognitive Impairment in Multiple Sclerosis (COGIMUS) study. Mult Scler. 2009, 15: 779-788. 10.1177/1352458509105544.CrossRefPubMed
6.
go back to reference Glanz BI, Holland CM, Gauthier SA, Amunwa EL, Liptak Z, Houtchens MK, Sperling RA, Khoury SJ, Guttmann CR, Weiner HL: Cognitive dysfunction in patients with clinically isolated syndromes or newly diagnosed multiple sclerosis. Mult Scler. 2007, 13: 1004-1010. 10.1177/1352458507077943.CrossRefPubMed Glanz BI, Holland CM, Gauthier SA, Amunwa EL, Liptak Z, Houtchens MK, Sperling RA, Khoury SJ, Guttmann CR, Weiner HL: Cognitive dysfunction in patients with clinically isolated syndromes or newly diagnosed multiple sclerosis. Mult Scler. 2007, 13: 1004-1010. 10.1177/1352458507077943.CrossRefPubMed
7.
go back to reference Houtchens MK, Benedict RHB, Killiany R, Sharma J, Jaisani Z, Singh B, Weinstock-Guttman B, Guttmann CRG, Bakshi R: Thalamic atrophy and cognition in multiple sclerosis. Neurology. 2007, 69: 113-123.CrossRef Houtchens MK, Benedict RHB, Killiany R, Sharma J, Jaisani Z, Singh B, Weinstock-Guttman B, Guttmann CRG, Bakshi R: Thalamic atrophy and cognition in multiple sclerosis. Neurology. 2007, 69: 113-123.CrossRef
8.
go back to reference Roosendaal SD, Bendfeldt K, Vrenken H, Polman CH, Borgwardt S, Radue EW, Kappos L, Pelletier D, Hauser SL, Matthews PM, Barkhof F, Geurts JJ: Grey matter volume in a large cohort of MS patients: relation to MRI parameters and disability. Mult Scler. 2011, 17: 1098-1106. 10.1177/1352458511404916.CrossRefPubMed Roosendaal SD, Bendfeldt K, Vrenken H, Polman CH, Borgwardt S, Radue EW, Kappos L, Pelletier D, Hauser SL, Matthews PM, Barkhof F, Geurts JJ: Grey matter volume in a large cohort of MS patients: relation to MRI parameters and disability. Mult Scler. 2011, 17: 1098-1106. 10.1177/1352458511404916.CrossRefPubMed
9.
go back to reference Fisher E, Lee JC, Nakamura K, Rudick RA: Gray matter atrophy in multiple sclerosis: a longitudinal study. Ann Neurol. 2008, 64: 255-265. 10.1002/ana.21436.CrossRefPubMed Fisher E, Lee JC, Nakamura K, Rudick RA: Gray matter atrophy in multiple sclerosis: a longitudinal study. Ann Neurol. 2008, 64: 255-265. 10.1002/ana.21436.CrossRefPubMed
10.
go back to reference Zamboni P, Galeotti R, Menegatti E, Malagoni AM, Tacconi G, Dall’Ara S, Bartolomei I, Salvi F: Chronic cerebrospinal venous insufficiency in patients with multiple sclerosis. J Neurol Neurosurg Psychiatry. 2009, 80: 392-399.CrossRefPubMed Zamboni P, Galeotti R, Menegatti E, Malagoni AM, Tacconi G, Dall’Ara S, Bartolomei I, Salvi F: Chronic cerebrospinal venous insufficiency in patients with multiple sclerosis. J Neurol Neurosurg Psychiatry. 2009, 80: 392-399.CrossRefPubMed
11.
go back to reference Khan O, Filippi M, Freedman MS, Barkhof F, Dore-Duffy P, Lassmann H, Trapp B, Bar-Or A, Zak I, Siegel MJ, Lisak R: Chronic cerebrospinal venous insufficiency and multiple sclerosis. Ann Neurol. 2010, 67: 286-290. 10.1002/ana.22001.CrossRefPubMed Khan O, Filippi M, Freedman MS, Barkhof F, Dore-Duffy P, Lassmann H, Trapp B, Bar-Or A, Zak I, Siegel MJ, Lisak R: Chronic cerebrospinal venous insufficiency and multiple sclerosis. Ann Neurol. 2010, 67: 286-290. 10.1002/ana.22001.CrossRefPubMed
12.
go back to reference Zivadinov R, Ramanathan M, Dolic K, Marr K, Karmon Y, Siddiqui AH, Benedict RH, Weinstock-Guttman B: Chronic cerebrospinal venous insufficiency in multiple sclerosis: diagnostic, pathogenetic, clinical and treatment perspectives. Expert Rev Neurother. 2011, 11: 1277-1294. 10.1586/ern.11.117.CrossRefPubMed Zivadinov R, Ramanathan M, Dolic K, Marr K, Karmon Y, Siddiqui AH, Benedict RH, Weinstock-Guttman B: Chronic cerebrospinal venous insufficiency in multiple sclerosis: diagnostic, pathogenetic, clinical and treatment perspectives. Expert Rev Neurother. 2011, 11: 1277-1294. 10.1586/ern.11.117.CrossRefPubMed
13.
go back to reference Rudick RA: Multiple sclerosis: is multiple sclerosis caused by venous insufficiency?. Nat Rev Neurol. 2010, 6: 472-474. 10.1038/nrneurol.2010.117.CrossRefPubMed Rudick RA: Multiple sclerosis: is multiple sclerosis caused by venous insufficiency?. Nat Rev Neurol. 2010, 6: 472-474. 10.1038/nrneurol.2010.117.CrossRefPubMed
14.
go back to reference Zamboni P, Menegatti E, Galeotti R, Malagoni AM, Tacconi G, Dall’Ara S, Bartolomei I, Salvi F: The value of cerebral Doppler venous haemodynamics in the assessment of multiple sclerosis. J Neurol Sci. 2009, 282: 21-27. 10.1016/j.jns.2008.11.027.CrossRefPubMed Zamboni P, Menegatti E, Galeotti R, Malagoni AM, Tacconi G, Dall’Ara S, Bartolomei I, Salvi F: The value of cerebral Doppler venous haemodynamics in the assessment of multiple sclerosis. J Neurol Sci. 2009, 282: 21-27. 10.1016/j.jns.2008.11.027.CrossRefPubMed
15.
go back to reference Zivadinov R: Funding CCSVI research is/was a waste of valuable time, money and intellectual energy. No. Mult Scler. 2013, 19: 858-860. 10.1177/1352458513480252.CrossRefPubMed Zivadinov R: Funding CCSVI research is/was a waste of valuable time, money and intellectual energy. No. Mult Scler. 2013, 19: 858-860. 10.1177/1352458513480252.CrossRefPubMed
16.
go back to reference Baracchini C, Perini P, Causin F, Calabrese M, Rinaldi F, Gallo P: Progressive multiple sclerosis is not associated with chronic cerebrospinal venous insufficiency. Neurology. 2011, 77: 844-850. 10.1212/WNL.0b013e31822c6208.CrossRefPubMed Baracchini C, Perini P, Causin F, Calabrese M, Rinaldi F, Gallo P: Progressive multiple sclerosis is not associated with chronic cerebrospinal venous insufficiency. Neurology. 2011, 77: 844-850. 10.1212/WNL.0b013e31822c6208.CrossRefPubMed
17.
go back to reference Batista S, Teter B, Sequeira K, Josyula S, Hoogs M, Ramanathan M, Benedict RH, Weinstock-Guttman B: Cognitive impairment is associated with reduced bone mass in multiple sclerosis. Mult Scler. 2012, 18: 1459-1465. 10.1177/1352458512440206.CrossRefPubMed Batista S, Teter B, Sequeira K, Josyula S, Hoogs M, Ramanathan M, Benedict RH, Weinstock-Guttman B: Cognitive impairment is associated with reduced bone mass in multiple sclerosis. Mult Scler. 2012, 18: 1459-1465. 10.1177/1352458512440206.CrossRefPubMed
18.
go back to reference Doepp F, Paul F, Valdueza JM, Schmierer K, Schreiber SJ: No cerebrocervical venous congestion in patients with multiple sclerosis. Ann Neurol. 2010, 68: 173-183.CrossRefPubMed Doepp F, Paul F, Valdueza JM, Schmierer K, Schreiber SJ: No cerebrocervical venous congestion in patients with multiple sclerosis. Ann Neurol. 2010, 68: 173-183.CrossRefPubMed
19.
go back to reference Baracchini C, Perini P, Calabrese M, Causin F, Rinaldi F, Gallo P: No evidence of chronic cerebrospinal venous insufficiency at multiple sclerosis onset. Ann Neurol. 2011, 69: 90-99. 10.1002/ana.22228.CrossRefPubMed Baracchini C, Perini P, Calabrese M, Causin F, Rinaldi F, Gallo P: No evidence of chronic cerebrospinal venous insufficiency at multiple sclerosis onset. Ann Neurol. 2011, 69: 90-99. 10.1002/ana.22228.CrossRefPubMed
20.
go back to reference Centonze D, Floris R, Stefanini M, Rossi S, Fabiano S, Castelli M, Marziali S, Spinelli A, Motta C, Garaci FG, Bernardi G, Simonetti G: Proposed chronic cerebrospinal venous insufficiency criteria do not predict multiple sclerosis risk or severity. Ann Neurol. 2011, 70: 51-58.CrossRefPubMed Centonze D, Floris R, Stefanini M, Rossi S, Fabiano S, Castelli M, Marziali S, Spinelli A, Motta C, Garaci FG, Bernardi G, Simonetti G: Proposed chronic cerebrospinal venous insufficiency criteria do not predict multiple sclerosis risk or severity. Ann Neurol. 2011, 70: 51-58.CrossRefPubMed
21.
go back to reference Tsivgoulis G, Mantatzis M, Bogiatzi C, Vadikolias K, Voumvourakis K, Prassopoulos P, Piperidou C, Heliopoulos I: Extracranial venous hemodynamics in multiple sclerosis: a case–control study. Neurology. 2011, 77: 1241-1245. 10.1212/WNL.0b013e318230a149.CrossRefPubMed Tsivgoulis G, Mantatzis M, Bogiatzi C, Vadikolias K, Voumvourakis K, Prassopoulos P, Piperidou C, Heliopoulos I: Extracranial venous hemodynamics in multiple sclerosis: a case–control study. Neurology. 2011, 77: 1241-1245. 10.1212/WNL.0b013e318230a149.CrossRefPubMed
22.
go back to reference Mayer CA, Pfeilschifter W, Lorenz MW, Nedelmann M, Bechmann I, Steinmetz H, Ziemann U: The perfect crime? CCSVI not leaving a trace in MS. J Neurol Neurosurg Psychiatry. 2011, 82: 436-440. 10.1136/jnnp.2010.231613.CrossRefPubMedPubMedCentral Mayer CA, Pfeilschifter W, Lorenz MW, Nedelmann M, Bechmann I, Steinmetz H, Ziemann U: The perfect crime? CCSVI not leaving a trace in MS. J Neurol Neurosurg Psychiatry. 2011, 82: 436-440. 10.1136/jnnp.2010.231613.CrossRefPubMedPubMedCentral
23.
go back to reference Zivadinov R, Marr K, Cutter G, Ramanathan M, Benedict RH, Kennedy C, Elfadil M, Yeh AE, Reuther J, Brooks C, Hunt K, Andrews M, Carl E, Dwyer MG, Hojnacki D, Weinstock-Guttman B: Prevalence, sensitivity, and specificity of chronic cerebrospinal venous insufficiency in MS. Neurology. 2011, 77: 138-144. 10.1212/WNL.0b013e318212a901.CrossRefPubMed Zivadinov R, Marr K, Cutter G, Ramanathan M, Benedict RH, Kennedy C, Elfadil M, Yeh AE, Reuther J, Brooks C, Hunt K, Andrews M, Carl E, Dwyer MG, Hojnacki D, Weinstock-Guttman B: Prevalence, sensitivity, and specificity of chronic cerebrospinal venous insufficiency in MS. Neurology. 2011, 77: 138-144. 10.1212/WNL.0b013e318212a901.CrossRefPubMed
24.
go back to reference Weinstock-Guttman B, Ramanathan M, Marr K, Hojnack D, Benedict RH, Morgan C, Yeh EA, Carl E, Kennedy C, Reuther J, Brooks C, Hunt K, Elfadil M, Andrews M, Zivadinov R: Clinical correlates of chronic cerebrospinal venous insufficiency in multiple sclerosis. BMC Neurol. 2012, 12: 26-10.1186/1471-2377-12-26.CrossRefPubMedPubMedCentral Weinstock-Guttman B, Ramanathan M, Marr K, Hojnack D, Benedict RH, Morgan C, Yeh EA, Carl E, Kennedy C, Reuther J, Brooks C, Hunt K, Elfadil M, Andrews M, Zivadinov R: Clinical correlates of chronic cerebrospinal venous insufficiency in multiple sclerosis. BMC Neurol. 2012, 12: 26-10.1186/1471-2377-12-26.CrossRefPubMedPubMedCentral
25.
go back to reference Dolic K, Marr K, Valnarov V, Dwyer MG, Carl E, Hagemeier J, Kennedy C, Brooks C, Kilanowski C, Hunt K, Hojnacki D, Weinstock-Guttman B, Zivadinov R: Sensitivity and specificity for screening of chronic cerebrospinal venous insufficiency using a multimodal non-invasive imaging approach in patients with multiple sclerosis. Funct Neurol. 2011, 26: 205-214.PubMed Dolic K, Marr K, Valnarov V, Dwyer MG, Carl E, Hagemeier J, Kennedy C, Brooks C, Kilanowski C, Hunt K, Hojnacki D, Weinstock-Guttman B, Zivadinov R: Sensitivity and specificity for screening of chronic cerebrospinal venous insufficiency using a multimodal non-invasive imaging approach in patients with multiple sclerosis. Funct Neurol. 2011, 26: 205-214.PubMed
26.
go back to reference Bastianello S, Romani A, Viselner G, Tibaldi EC, Giugni E, Altieri M, Cecconi P, Mendozzi L, Farina M, Mariani D, Galassi A, Quattrini C, Mancini M, Bresciamorra V, Lagace A, McDonald S, Bono G, Bergamaschi R: 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, Tibaldi EC, Giugni E, Altieri M, Cecconi P, Mendozzi L, Farina M, Mariani D, Galassi A, Quattrini C, Mancini M, Bresciamorra V, Lagace A, McDonald S, Bono G, Bergamaschi R: 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
27.
go back to reference Zivadinov R, Cutter G, Marr K, Ramanathan M, Benedict RH, Bergsland N, Morgan C, Carl E, Hojnacki D, Yeh EA, Willis L, Cherneva M, Kennedy C, Dwyer MG, Weinstock-Guttman B: No association between conventional brain MR imaging and chronic cerebrospinal venous insufficiency in multiple sclerosis. AJNR Am J Neuroradiol. 2012, 33: 1913-1917. 10.3174/ajnr.A3112.CrossRefPubMed Zivadinov R, Cutter G, Marr K, Ramanathan M, Benedict RH, Bergsland N, Morgan C, Carl E, Hojnacki D, Yeh EA, Willis L, Cherneva M, Kennedy C, Dwyer MG, Weinstock-Guttman B: No association between conventional brain MR imaging and chronic cerebrospinal venous insufficiency in multiple sclerosis. AJNR Am J Neuroradiol. 2012, 33: 1913-1917. 10.3174/ajnr.A3112.CrossRefPubMed
28.
go back to reference Kurtzke JF: Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Ann Neurol. 1983, 13: 227-231. 10.1002/ana.410130302.CrossRef Kurtzke JF: Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Ann Neurol. 1983, 13: 227-231. 10.1002/ana.410130302.CrossRef
29.
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. [see comment]. Neurology. 1996, 46: 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. [see comment]. Neurology. 1996, 46: 907-911. 10.1212/WNL.46.4.907.CrossRefPubMed
30.
go back to reference Beck AT, Steer RA, Brown GK: BDI-Fast Screen for Medical Patients: Manual. 2000, San Antonio, TX: Psychological Corporation Beck AT, Steer RA, Brown GK: BDI-Fast Screen for Medical Patients: Manual. 2000, San Antonio, TX: Psychological Corporation
31.
go back to reference Benedict RHB, Fishman I, McClellan MM, Bakshi R, Weinstock-Guttman B: Validity of the beck depression inventory - fast screen in multiple sclerosis. Mult Scler. 2003, 9: 393-396. 10.1191/1352458503ms902oa.CrossRefPubMed Benedict RHB, Fishman I, McClellan MM, Bakshi R, Weinstock-Guttman B: Validity of the beck depression inventory - fast screen in multiple sclerosis. Mult Scler. 2003, 9: 393-396. 10.1191/1352458503ms902oa.CrossRefPubMed
32.
go back to reference Benedict RHB, Fischer JS, Archibald CJ, Arnett PA, Beatty WW, Bobholz J, Chelune G, Fisk JD, Langdon DW, Caruso LS, Foley F, LaRocca NG, Vowels L, Weinstein A, DeLuca J, Rao SM, Munschauer F: Minimal neuropsychological assessment of MS patients: a consensus approach. Clin Neuropsychol. 2002, 16: 381-397. 10.1076/clin.16.3.381.13859.CrossRefPubMed Benedict RHB, Fischer JS, Archibald CJ, Arnett PA, Beatty WW, Bobholz J, Chelune G, Fisk JD, Langdon DW, Caruso LS, Foley F, LaRocca NG, Vowels L, Weinstein A, DeLuca J, Rao SM, Munschauer F: Minimal neuropsychological assessment of MS patients: a consensus approach. Clin Neuropsychol. 2002, 16: 381-397. 10.1076/clin.16.3.381.13859.CrossRefPubMed
33.
go back to reference Parmenter BA, Testa SM, Schretlen DJ, Weinstock-Guttman B, Benedict RHB: The utility of regression-based norms in interpreting the minimal assessment of cognitive function in multiple sclerosis (MACFIMS). J Int Neuropsychol Soc. 2010, 16: 6-16. 10.1017/S1355617709990750.CrossRefPubMed Parmenter BA, Testa SM, Schretlen DJ, Weinstock-Guttman B, Benedict RHB: The utility of regression-based norms in interpreting the minimal assessment of cognitive function in multiple sclerosis (MACFIMS). J Int Neuropsychol Soc. 2010, 16: 6-16. 10.1017/S1355617709990750.CrossRefPubMed
34.
go back to reference Benedict RHB: Effects of using same- versus alternate-form memory tests during short-interval repeated assessments in multiple sclerosis. J Int Neuropsychol Soc. 2005, 11: 727-736.CrossRefPubMed Benedict RHB: Effects of using same- versus alternate-form memory tests during short-interval repeated assessments in multiple sclerosis. J Int Neuropsychol Soc. 2005, 11: 727-736.CrossRefPubMed
35.
go back to reference Benedict R, Ramasamy D, Munschauer FE, Weinstock-Guttman B, Zivadinov R: Memory impairment in multiple sclerosis: correlation with deep gray matter and mesial temporal atrophy. Mult Scler. 2008, 14: S252.CrossRef Benedict R, Ramasamy D, Munschauer FE, Weinstock-Guttman B, Zivadinov R: Memory impairment in multiple sclerosis: correlation with deep gray matter and mesial temporal atrophy. Mult Scler. 2008, 14: S252.CrossRef
36.
go back to reference Tekok-Kilic A, Benedict RHB, Weinstock-Guttman B, Dwyer MG, Carone D, Srinivasaraghavan B, Yella V, Abdelrahman N, Munschauer F, Bakshi R, Zivadinov R: Independent contributions of cortical gray matter atrophy and ventricle enlargement for predicting neuropsychological impairment in multiple sclerosis. NeuroImage. 2007, 36: 1294-1300. 10.1016/j.neuroimage.2007.04.017.CrossRefPubMed Tekok-Kilic A, Benedict RHB, Weinstock-Guttman B, Dwyer MG, Carone D, Srinivasaraghavan B, Yella V, Abdelrahman N, Munschauer F, Bakshi R, Zivadinov R: Independent contributions of cortical gray matter atrophy and ventricle enlargement for predicting neuropsychological impairment in multiple sclerosis. NeuroImage. 2007, 36: 1294-1300. 10.1016/j.neuroimage.2007.04.017.CrossRefPubMed
37.
go back to reference Smith A: Symbol Digit Modalities Test: Manual. 1982, Los Angeles: Western Psychological Services Smith A: Symbol Digit Modalities Test: Manual. 1982, Los Angeles: Western Psychological Services
38.
go back to reference Gronwall D: Paced auditory serial addition task: A measure of recovery from concussion. Percept Mot Skills. 1977, 44: 367-373. 10.2466/pms.1977.44.2.367.CrossRefPubMed Gronwall D: Paced auditory serial addition task: A measure of recovery from concussion. Percept Mot Skills. 1977, 44: 367-373. 10.2466/pms.1977.44.2.367.CrossRefPubMed
39.
go back to reference Delis DC, Kramer JH, Kaplan E, Ober BA: Califorina Verbal Learning Test. 2000, San Antonio, TX: The Psychological Corporation, 2 Delis DC, Kramer JH, Kaplan E, Ober BA: Califorina Verbal Learning Test. 2000, San Antonio, TX: The Psychological Corporation, 2
40.
go back to reference Benedict RHB, Schretlen D, Groninger L, Dobraski M, Shpritz B: Revision of the Brief Visuospatial Memory Test: studies of normal performance, reliability, and validity. Psychol Assess. 1996, 8: 145-153.CrossRef Benedict RHB, Schretlen D, Groninger L, Dobraski M, Shpritz B: Revision of the Brief Visuospatial Memory Test: studies of normal performance, reliability, and validity. Psychol Assess. 1996, 8: 145-153.CrossRef
41.
go back to reference Benton AL, Hamsher KS: Multilingual Aphasia Examination. 1989, Iowa City: IA: AJA Associates Benton AL, Hamsher KS: Multilingual Aphasia Examination. 1989, Iowa City: IA: AJA Associates
42.
go back to reference Benton AL, Sivan AB, Hamsher K, Varney NR, Spreen O: Contributions to Neuropsychological Assessment. 1994, New York: Oxford University Press, 2 Benton AL, Sivan AB, Hamsher K, Varney NR, Spreen O: Contributions to Neuropsychological Assessment. 1994, New York: Oxford University Press, 2
43.
go back to reference Delis DC, Kaplan E, Kramer JH: Delis-Kaplan Executive Function System. 2001, San Antonio, TX: The Psychological Corporation Delis DC, Kaplan E, Kramer JH: Delis-Kaplan Executive Function System. 2001, San Antonio, TX: The Psychological Corporation
44.
go back to reference Zamboni P, Menegatti E, Weinstock-Guttman B, Schirda C, Cox JL, Malagoni AM, Hojanacki D, Kennedy C, Carl E, Dwyer MG, Bergsland N, Galeotti R, Hussein S, Bartolomei I, Salvi F, Zivadinov R: The severity of chronic cerebrospinal venous insufficiency in patients with multiple sclerosis is related to altered cerebrospinal fluid dynamics. Funct Neurol. 2009, 24: 133-138.PubMed Zamboni P, Menegatti E, Weinstock-Guttman B, Schirda C, Cox JL, Malagoni AM, Hojanacki D, Kennedy C, Carl E, Dwyer MG, Bergsland N, Galeotti R, Hussein S, Bartolomei I, Salvi F, Zivadinov R: The severity of chronic cerebrospinal venous insufficiency in patients with multiple sclerosis is related to altered cerebrospinal fluid dynamics. Funct Neurol. 2009, 24: 133-138.PubMed
45.
go back to reference Batista S, Zivadinov R, Hoogs M, Bergsland N, Heininen-Brown M, Dwyer MG, Weinstock-Guttman B, Benedict RH: Basal ganglia, thalamus and neocortical atrophy predicting slowed cognitive processing in multiple sclerosis. J Neurol. 2012, 259: 139-146. 10.1007/s00415-011-6147-1.CrossRefPubMed Batista S, Zivadinov R, Hoogs M, Bergsland N, Heininen-Brown M, Dwyer MG, Weinstock-Guttman B, Benedict RH: Basal ganglia, thalamus and neocortical atrophy predicting slowed cognitive processing in multiple sclerosis. J Neurol. 2012, 259: 139-146. 10.1007/s00415-011-6147-1.CrossRefPubMed
46.
go back to reference Eshaghi A, Riyahi-Alam S, Roostaei T, Haeri G, Aghsaei A, Aidi MR, Pouretemad HR, Zarei M, Farhang S, Saeedi R, Nazeri A, Ganjgahi H, Etesam F, Azimi AR, Benedict RH, Sahraian MA: Validity and reliability of a Persian translation of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS). Clin Neuropsychol. 2012, 26: 975-984. 10.1080/13854046.2012.694912.CrossRefPubMed Eshaghi A, Riyahi-Alam S, Roostaei T, Haeri G, Aghsaei A, Aidi MR, Pouretemad HR, Zarei M, Farhang S, Saeedi R, Nazeri A, Ganjgahi H, Etesam F, Azimi AR, Benedict RH, Sahraian MA: Validity and reliability of a Persian translation of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS). Clin Neuropsychol. 2012, 26: 975-984. 10.1080/13854046.2012.694912.CrossRefPubMed
47.
go back to reference Parmenter BA, Zivadinov R, Kerenyi L, Gavett R, Weinstock-Guttman B, Dwyer M, Garg N, Munschauer F, Benedict RHB: Validity of the Wisconsin card sorting and Delis-Kaplan executive function system (DKEFS) sorting tests in multiple sclerosis. J Clin Exp Neuropsychol. 2007, 29: 215-223. 10.1080/13803390600672163.CrossRefPubMed Parmenter BA, Zivadinov R, Kerenyi L, Gavett R, Weinstock-Guttman B, Dwyer M, Garg N, Munschauer F, Benedict RHB: Validity of the Wisconsin card sorting and Delis-Kaplan executive function system (DKEFS) sorting tests in multiple sclerosis. J Clin Exp Neuropsychol. 2007, 29: 215-223. 10.1080/13803390600672163.CrossRefPubMed
48.
go back to reference Zivadinov R, Galeotti R, Hojnacki D, Menegatti E, Dwyer MG, Schirda C, Malagoni AM, Marr K, Kennedy C, Bartolomei I, Magnano C, Salvi F, Weinstock-Guttman B, Zamboni P: Value of MR venography for detection of internal jugular vein anomalies in multiple sclerosis: a pilot longitudinal study. AJNR Am J Neuroradiol. 2011, 32: 938-946. 10.3174/ajnr.A2386.CrossRefPubMed Zivadinov R, Galeotti R, Hojnacki D, Menegatti E, Dwyer MG, Schirda C, Malagoni AM, Marr K, Kennedy C, Bartolomei I, Magnano C, Salvi F, Weinstock-Guttman B, Zamboni P: Value of MR venography for detection of internal jugular vein anomalies in multiple sclerosis: a pilot longitudinal study. AJNR Am J Neuroradiol. 2011, 32: 938-946. 10.3174/ajnr.A2386.CrossRefPubMed
49.
go back to reference Hojnacki D, Zamboni P, Lopez-Soriano A, Galleotti R, Menegatti E, Weinstock-Guttman B, Schirda C, Magnano C, Malagoni AM, Kennedy C, Bartolomei I, Salvi F, Zivadinov R: 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: 127-139.PubMed Hojnacki D, Zamboni P, Lopez-Soriano A, Galleotti R, Menegatti E, Weinstock-Guttman B, Schirda C, Magnano C, Malagoni AM, Kennedy C, Bartolomei I, Salvi F, Zivadinov R: 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: 127-139.PubMed
50.
go back to reference Benedict RH, Zivadinov R: Risk factors for and management of cognitive dysfunction in multiple sclerosis. Nat Rev Neurol. 2011, 7: 332-342. 10.1038/nrneurol.2011.61.CrossRefPubMed Benedict RH, Zivadinov R: Risk factors for and management of cognitive dysfunction in multiple sclerosis. Nat Rev Neurol. 2011, 7: 332-342. 10.1038/nrneurol.2011.61.CrossRefPubMed
51.
go back to reference Filippi M, Rocca MA, Benedict RH, DeLuca J, Geurts JJ, Rombouts SA, Ron M, Comi G: The contribution of MRI in assessing cognitive impairment in multiple sclerosis. Neurology. 2010, 75: 2121-2128. 10.1212/WNL.0b013e318200d768.CrossRefPubMedPubMedCentral Filippi M, Rocca MA, Benedict RH, DeLuca J, Geurts JJ, Rombouts SA, Ron M, Comi G: The contribution of MRI in assessing cognitive impairment in multiple sclerosis. Neurology. 2010, 75: 2121-2128. 10.1212/WNL.0b013e318200d768.CrossRefPubMedPubMedCentral
Metadata
Title
Chronic cerebrospinal venous insufficiency is not associated with cognitive impairment in multiple sclerosis
Authors
Ralph HB Benedict
Bianca Weinstock-Guttmam
Karen Marr
Vesela Valnarov
Cheryl Kennedy
Ellen Carl
Christina Brooks
David Hojnacki
Robert Zivadinov
Publication date
01-12-2013
Publisher
BioMed Central
Published in
BMC Medicine / Issue 1/2013
Electronic ISSN: 1741-7015
DOI
https://doi.org/10.1186/1741-7015-11-167

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