Sex-specific extent and severity of white matter damage in multiple sclerosis: Implications for cognitive decline

Human Brain Mapping

Volumn 35, Issue 5, 2014, Pages 2348-2358

  Schoonheim, Menno M ^a   Vigeveno, René M ^a   Lopes, Fernanda C Rueda ^a,b   Pouwels, Petra J W ^a   Polman, Chris H ^a   Barkhof, Frederik ^a   Geurts, Jeroen J G ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Cognition; DTI; Gender; MRI; Multiple sclerosis; Sex; TBSS; Thalamus

Indexed keywords

ADULT; ARTICLE; CLINICAL ARTICLE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; DISABILITY; DISEASE DURATION; DISEASE SEVERITY; FEMALE; FRACTIONAL ANISOTROPY; HUMAN; MAJOR CLINICAL STUDY; MALE; MULTIPLE SCLEROSIS; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; SEX DIFFERENCE; WHITE MATTER LESION; CASE CONTROL STUDY; COGNITION DISORDERS; COMPLICATION; DIFFUSION WEIGHTED IMAGING; IMAGE PROCESSING; LEUKOENCEPHALOPATHIES; MIDDLE AGED; SEXUAL DEVELOPMENT; STATISTICAL MODEL;

ADULT; CASE-CONTROL STUDIES; COGNITION DISORDERS; DIFFUSION MAGNETIC RESONANCE IMAGING; DISABILITY EVALUATION; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LEUKOENCEPHALOPATHIES; LINEAR MODELS; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; NEUROPSYCHOLOGICAL TESTS; SEX CHARACTERISTICS;

EID: 84898042945     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22332     Document Type: Article

References (48)

1. Amato MP, Zipoli V, Portaccio E (2006): Multiple sclerosis-related cognitive changes: A review of cross-sectional and longitudinal studies. J Neurol Sci 245:41-46.
2. Antulov R, Weinstock-Guttman B, Cox JL, Hussein S, Durfee J, Caiola C, Dwyer MG, Bergsland N, Abdelrahman N, Stosic M, Hojnacki D, Munschauer FE, Miletic D, Zivadinov R (2009): Gender-related differences in MS: A study of conventional and nonconventional MRI measures. Mult Scler 15:345-354.
3. Batista S, Zivadinov R, Hoogs M, Bergsland N, Heininen-Brown M, Dwyer MG, Weinstock-Guttman B, Benedict RH (2012): Basal ganglia, thalamus and neocortical atrophy predicting slowed cognitive processing in multiple sclerosis. J Neurol 259:139-146.
4. Benedict RH, Bruce J, Dwyer MG, Weinstock-Guttman B, Tjoa C, Tavazzi E, Munschauer FE, Zivadinov R (2007): Diffusion-weighted imaging predicts cognitive impairment in multiple sclerosis. Mult Scler 13:722-730.
5. Benedict RH, Weinstock-Guttman B, Fishman I, Sharma J, Tjoa CW, Bakshi R (2004): Prediction of neuropsychological impairment in multiple sclerosis: Comparison of conventional magnetic resonance imaging measures of atrophy and lesion burden. Arch Neurol 61:226-230.
6. Benedict RH, Zivadinov R (2011): Risk factors for and management of cognitive dysfunction in multiple sclerosis. Nat Rev Neurol 7:333-342.
7. Bodini B, Khaleeli Z, Cercignani M, Miller DH, Thompson AJ, Ciccarelli O (2009): Exploring the relationship between white matter and gray matter damage in early primary progressive multiple sclerosis: An in vivo study with TBSS and VBM. Hum Brain Mapp 30:2852-2861.
8. Cader S, Cifelli A, Abu-Omar Y, Palace J, Matthews PM (2006): Reduced brain functional reserve and altered functional connectivity in patients with multiple sclerosis. Brain 129:527-537.
9. Chiaravalloti ND, DeLuca J (2008): Cognitive impairment in multiple sclerosis. Lancet Neurol 7:1139-1151.
10. Cosgrove KP, Mazure CM, Staley JK (2007): Evolving knowledge of sex differences in brain structure, function, and chemistry. Biol Psychiatry 62:847-855.
11. Deloire MS, Ruet A, Hamel D, Bonnet M, Dousset V, Brochet B (2011): MRI predictors of cognitive outcome in early multiple sclerosis. Neurology 76:1161-1167.
12. Deloire MS, Salort E, Bonnet M, Arimone Y, Boudineau M, Amieva H, Barroso B, Ouallet JC, Pachai C, Galliaud E, Petry KG, Dousset V, Fabrigoule C, Brochet B (2005): Cognitive impairment as marker of diffuse brain abnormalities in early relapsing remitting multiple sclerosis. J Neurol Neurosurg Psychiatry 76:519-526.
13. Dineen RA, Vilisaar J, Hlinka J, Bradshaw CM, Morgan PS, Constantinescu CS, Auer DP (2009): Disconnection as a mechanism for cognitive dysfunction in multiple sclerosis. Brain 132:239-249.
14. Filippi M, Riccitelli G, Mattioli F, Capra R, Stampatori C, Pagani E, Valsasina P, Copetti M, Falini A, Comi G, Rocca MA (2012): Multiple sclerosis: Effects of cognitive rehabilitation on structural and functional MR imaging measures-An explorative study. Radiology 262:932-940.
15. Filippi M, Rocca MA, Benedict RH, DeLuca J, Geurts JJ, Rombouts SA, Ron M, Comi G (2010): The contribution of MRI in assessing cognitive impairment in multiple sclerosis. Neurology 75:2121-2128.
16. Fisher E, Lee JC, Nakamura K, Rudick RA (2008): Gray matter atrophy in multiple sclerosis: A longitudinal study. Ann Neurol 64:255-265.
17. Gong G, He Y, Evans AC (2011): Brain connectivity: Gender makes a difference. Neuroscientist 17:575-591.
18. Gong G, Rosa-Neto P, Carbonell F, Chen ZJ, He Y, Evans AC (2009): Age- and gender-related differences in the cortical anatomical network. J Neurosci 29:15684-15693.
19. Hawellek DJ, Hipp JF, Lewis CM, Corbetta M, Engel AK (2011): Increased functional connectivity indicates the severity of cognitive impairment in multiple sclerosis. Proc Natl Acad Sci U S A 108:19066-19071.
20. Houtchens MK, Benedict RH, Killiany R, Sharma J, Jaisani Z, Singh B, Weinstock-Guttman B, Guttmann CR, Bakshi R (2007): Thalamic atrophy and cognition in multiple sclerosis. Neurology 69:1213-1223.
21. Klawiter EC, Schmidt RE, Trinkaus K, Liang HF, Budde MD, Naismith RT, Song SK, Cross AH, Benzinger TL (2011): Radial diffusivity predicts demyelination in ex vivo multiple sclerosis spinal cords. Neuroimage 55:1454-1460.
22. Koch M, Kingwell E, Rieckmann P, Tremlett H (2010): The natural history of secondary progressive multiple sclerosis. J Neurol Neurosurg Psychiatry 81:1039-1043.
23. Kuhlmann T, Goldschmidt T, Antel J, Wegner C, Konig F, Metz I, Bruck W (2009): Gender differences in the histopathology of MS? J Neurol Sci 286:86-91.
24. Kumar R, Nguyen HD, Macey PM, Woo MA, Harper RM (2012): Regional brain axial and radial diffusivity changes during development. J Neurosci Res 90:346-355.
25. Kurtzke JF (1983): Rating neurologic impairment in multiple-sclerosis-An Expanded Disability Status Scale (Edss). Neurology 33:1444-1452.
26. Lublin FD, Reingold SC (1996): Defining the clinical course of multiple sclerosis: Results of an international survey. Neurology 46:907-911.
27. Menzler K, Belke M, Wehrmann E, Krakow K, Lengler U, Jansen A, Hamer HM, Oertel WH, Rosenow F, Knake S (2011): Men and women are different: Diffusion tensor imaging reveals sexual dimorphism in the microstructure of the thalamus, corpus callosum and cingulum. Neuroimage 54:2557-2562.
28. Moll NM, Rietsch AM, Thomas S, Ransohoff AJ, Lee JC, Fox R, Chang A, Ransohoff RM, Fisher E (2011): Multiple sclerosis normal-appearing white matter: Pathology-imaging correlations. Ann Neurol 70:764-773.
29. Pagani E, Bammer R, Horsfield MA, Rovaris M, Gass A, Ciccarelli O, Filippi M (2007): Diffusion MR imaging in multiple sclerosis: Technical aspects and challenges. AJNR Am J Neuroradiol 28:411-420.
30. Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, Fujihara K, Havrdova E, Hutchinson M, Kappos L, Lublin FD, Montalban X, O'Connor P, Sandberg-Wollheim M, Thompson AJ, Waubant E, Weinshenker B, Wolinsky JS (2011): Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol 69:292-302.
31. Pujol J, Vendrell P, Deus J, Junque C, Bello J, Marti-Vilalta JL, Capdevila A (2001): The effect of medial frontal and posterior parietal demyelinating lesions on stroop interference. Neuroimage 13:68-75.
32. Rao SM (1990): A Manual for the Brief Repeatable Battery of Neuropsychological Tests in Multiple Sclerosis. Milwaukee, WI: Medical College of Wisconsin.
33. Rocca MA, Valsasina P, Absinta M, Riccitelli G, Rodegher ME, Misci P, Rossi P, Falini A, Comi G, Filippi M (2010): Default-mode network dysfunction and cognitive impairment in progressive MS. Neurology 74:1252-1259.
34. Rocca MA, Valsasina P, Ceccarelli A, Absinta M, Ghezzi A, Riccitelli G, Pagani E, Falini A, Comi G, Scotti G, Filippi M (2009): Structural and functional MRI correlates of Stroop control in benign MS. Hum Brain Mapp 30:276-290.
35. Roosendaal SD, Geurts JJ, Vrenken H, Hulst HE, Cover KS, Castelijns JA, Pouwels PJ, Barkhof F (2009): Regional DTI differences in multiple sclerosis patients. Neuroimage 44:1397-1403.
36. Rovaris M, Gass A, Bammer R, Hickman SJ, Ciccarelli O, Miller DH, Filippi M (2005): Diffusion MRI in multiple sclerosis. Neurology 65:1526-1532.
37. Rovaris M, Iannucci G, Falautano M, Possa F, Martinelli V, Comi G, Filippi M (2002): Cognitive dysfunction in patients with mildly disabling relapsing-remitting multiple sclerosis: An exploratory study with diffusion tensor MR imaging. J Neurol Sci 195:103-109.
38. Savettieri G, Messina D, Andreoli V, Bonavita S, Caltagirone C, Cittadella R, Farina D, Fazio MC, Girlanda P, Le PF, Liguori M, Lugaresi A, Nocentini U, Reggio A, Salemi G, Tedeschi G, Trojano M, Valentino P, Quattrone A (2004): Gender-related effect of clinical and genetic variables on the cognitive impairment in multiple sclerosis. J Neurol 251:1208-1214.
39. Schoonheim MM, Geurts JJ, Landi D, Douw L, van der Meer ML, Vrenken H, Polman CH, Barkhof F, Stam CJ (2013): Functional connectivity changes in multiple sclerosis patients: A graph analytical study of MEG resting state data. Hum Brain Mapp 34:52-61.
40. Schoonheim MM, Popescu V, Rueda Lopes FC, Wiebenga OT, Vrenken H, Douw L, Polman CH, Geurts JJ, Barkhof F (2012): Subcortical atrophy and cognition: Sex effects in multiple sclerosis. Neurology 79:1754-1761.
41. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, Behrens TE (2006): Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487-1505.
42. Smith SM, Nichols TE (2009): Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44:83-98.
43. Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, Armstrong RC (2005): Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 26:132-140.
44. Sumowski JF, Wylie GR, Chiaravalloti N, Deluca J (2010a): Intellectual enrichment lessens the effect of brain atrophy on learning and memory in multiple sclerosis. Neurology 74:1942-1945.
45. Sumowski JF, Wylie GR, Deluca J, Chiaravalloti N (2010b): Intellectual enrichment is linked to cerebral efficiency in multiple sclerosis: Functional magnetic resonance imaging evidence for cognitive reserve. Brain 133:362-374.
46. Van Hecke W., Nagels G, Leemans A, Vandervliet E, Sijbers J, Parizel PM (2010): Correlation of cognitive dysfunction and diffusion tensor MRI measures in patients with mild and moderate multiple sclerosis. J Magn Reson Imaging 31:1492-1498.
47. Vrenken H, Pouwels PJ, Geurts JJ, Knol DL, Polman CH, Barkhof F, Castelijns JA (2006): Altered diffusion tensor in multiple sclerosis normal-appearing brain tissue: Cortical diffusion changes seem related to clinical deterioration. J Magn Reson Imaging 23:628-636.
48. Yu HJ, Christodoulou C, Bhise V, Greenblatt D, Patel Y, Serafin D, Maletic-Savatic M, Krupp LB, Wagshul M (2011): Multiple white matter tract abnormalities underlie cognitive impairment in RRMS. Neuroimage 59:3713-3722.