Abstract
Introduction
Multiple sclerosis (MS) has a variable progression with an early onset of atrophy. Individual longitudinal radiological evaluations (over decades) are difficult to perform due to the limited availability of magnetic resonance imaging (MRI) in the past, patients lost in follow-up, and the continuous updating of scanners. We studied a cohort with widespread disease duration at baseline. The observed individual atrophy rates over time of 10 years represented four decades of disease span.
Methods
Thirty-seven MS patients (age range 24–65 years with disease duration 1–33 years) were consecutively selected and evaluated with MRI at baseline 1995 and in 1996. They were followed up for a decade (mean of 9.25 years, range 7.3–10 years) up to 2003–2005. Brain parenchymal volume and volumes of the supratentorial ventricles were analyzed with semi-automated volumetric measurements at three time points (1995, 1996, and 2003–2005).
Results
Volumetric differences were found over shorter periods of time (1–7 months); however, differences vanished by the end of follow-up. A uniform longitudinal decrease in brain volume and increase in ventricle volumes were found. Frontal horn width (1D) correlated strongest to 3D measures. No statistical differences of atrophy rates between MS courses were found. Supratentorial ventricular volumes were associated with disability and this association persisted during follow-up.
Conclusion
Despite variable clinical courses, the degenerative effects of MS progression expressed in brain atrophy seem to uniformly progress over longer periods of time. These volumetric changes can be detected using 1D and 2D measurements performed on a routine PACS workstation.
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References
Bermel RA, Bakshi R (2006) The measurement and clinical relevance of brain atrophy in multiple sclerosis. Lancet Neurol 5:158–170
Barkhof F (2002) The clinico-radiological paradox in multiple sclerosis revisited. Curr Opin Neurol 15:239–245
Brex PA, Jenkins R, Fox NC, Crum WR, O’Riordan JI, Plant GT, Miller DH (2000) Detection of ventricular enlargement in patients at earliest clinical stage of MS. Neurology 54:1689–1691
Luks TL, Goodkin DE, Nelson SJ, Majumdar S, Bacchetti P, Portnoy D, Sloan R (2000) A longitudinal study of ventricular volume in early relapsing–remitting multiple sclerosis. Mult Scler 6:332
Fisher E, Rudick RA, Simon JH, Cutter G, Baier M, Lee JC, Miller D, Weinstock-Guttman B, Mass MK, Dougherty DS, Simonian NA (2002) Eight-year follow-up study of brain atrophy in patients with MS. Neurology 59:1412–1420
Horakova D, Dwyer MG, Havrdova E, Cox JL, Dolezal O, Bergsland N, Rimes B, Seidl Z, Vaneckova M, Zivadinov R (2009) Gray matter atrophy and disability progression in patients with early relapsing–remitting multiple sclerosis: a 5-year longitudinal study. J Neurol Sci 282:112–119
Fox NC, Jenkins R, Leary SM, Stevenson VL, Losseff NA, Crum WR, Harvey RJ, Rossor MN, Miller DH, Thompson AJ (2000) Progressive cerebral atrophy in MS: a serial study using registered, volumetric MRI. Neurology 54:807–812
Kalkers NF, Ameziane N, Bot JC, Minneboo A, Polman CH, Barkhof F (2002) Longitudinal brain volume measurement in multiple sclerosis: rate of brain atrophy is independent of the disease subtype. Arch Neurol 59:1572–1576
Bermel RA, Sharma J, Tjoa CW, Puli SR, Bakshi R (2003) A semiautomated measure of whole-brain atrophy in multiple sclerosis. J Neurol Sci 208:57–65
Chard DT, Griffin CM, Parker GJ, Kapoor R, Thompson AJ, Miller DH (2002) Brain atrophy in clinically early relapsing–remitting multiple sclerosis. Brain 125:327–337
De Stefano N, Matthews PM, Filippi M, Agosta F, De Luca M, Bartolozzi ML, Guidi L, Ghezzi A, Montanari E, Cifelli A, Federico A, Smith SM (2003) Evidence of early cortical atrophy in MS: relevance to white matter changes and disability. Neurology 60:1157–1162
Lin X, Blumhardt LD, Constantinescu CS (2003) The relationship of brain and cervical cord volume to disability in clinical subtypes of multiple sclerosis: a three-dimensional study. Acta Neurol Scand 108:401–406
Turner B, Ramli N, Blumhardt LD, Jaspan T (2001) Ventricular enlargement in multiple sclerosis: a comparison of three-dimensional and linear MRI estimates. Neuroradiology 43:608–614
Stevenson VL, Miller DH, Leary SM, Rovaris M, Barkhof F, Brochet B, Dousset V, Filippi M, Hintzen R, Montalban X, Polman CH, Rovira A, de Sa J, Thompson AJ (2000) One year follow up study of primary and transitional progressive multiple sclerosis. J Neurol Neurosurg Psychiatry 6:713–718
Pagani E, Rocca MA, Gallo A, Rovaris M, Martinelli V, Comi G, Filippi M (2005) Regional brain atrophy evolves differently in patients with multiple sclerosis according to clinical phenotype. Am J Neuroradiol 26:341–346
Sharma J, Sanfilipo MP, Benedict RH, Weinstock-Guttman B, Munschauer FE 3rd, Bakshi R (2004) Whole-brain atrophy in multiple sclerosis measured by automated versus semiautomated MR imaging segmentation. Am J Neuroradiol 25:985–996
Butzkueven H, Kolbe SC, Jolley DJ, Brown JY, Cook MJ, van der Mei IA, Groom PS, Carey J, Eckholdt J, Rubio JP, Taylor BV, Mitchell PJ, Egan GF, Kilpatrick TJ (2008) Validation of linear cerebral atrophy markers in multiple sclerosis. J Clin Neurosci 15:130–137
Kurtzke JF (1983) Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 33:1444–1452
Roxburgh RH, Seaman SR, Masterman T, Hensiek AE, Sawcer SJ, Vukusic S, Achiti I, Confavreux C, Coustans M, le Page E, Edan G, McDonnell GV, Hawkins S, Trojano M, Liquiri M, Cocco E, Marruso MG, Tesser F, Leone MA, Weber A, Zipp F, Miterski B, Epplen JT, Oturai A, Sørensen PS, Celius EG, Lara NT, Montalban X, Villoslada P, Silva AM, Marta M, Leite I, Dubois B, Rubio J, Butzkueven H, Kilpatrick T, Mycko MP, Selmaj KW, Rio ME, Sá M, Salemi G, Savettieri G, Hillert J, Compston DA (2005) Multiple sclerosis severity score: using disability and disease duration to rate disease severity. Neurology 64:1144–1151
Poser CM, Paty DW, Scheinberg L, McDonald WI, Davis FA, Ebers GC, Johnson KP, Sibley WA, Silberberg DH, Tourtellotte WW (1983) New diagnostic criteria for multiple sclerosis: guidelines for research protocols. Ann Neurol 13:227–231
Polman CH, Reingold SC, Edan G, Filippi M, HP Hartung, Kappos L, Lublin FD, Metz LM, McFarland HF, O’Connor PW, Sandberg-Wollheim M, Thompson AJ, Weinshenker BG, Wolinsky JS (2005) Diagnostic criteria for multiple sclerosis: 2005 revisions to the “McDonald Criteria”. Ann Neurol 58:840–846
Martola J, Stawiarz L, Fredrikson S, Hillert J, Bergström J, Flodmark O, Kristoffersen Wiberg M (2007) Progression of non-age-related callosal brain atrophy in multiple sclerosis: a 9-year longitudinal MRI study representing four decades of disease development. J Neurol Neurosurg Psychiatry 78:375–380
Martola J, Stawiarz L, Fredrikson S, Hillert J, Bergstrom J, Flodmark O, Aspelin P, Kristoffersen Wiberg M (2008) Rate of ventricular enlargement in multiple sclerosis: a nine-year magnetic resonance imaging follow-up study. Acta Radiol 49:570–579
Martola J, Stawiarz L, Fredrikson S, Hillert J, Bergström J, Flodmark O, Aspelin P, Kristoffersen Wiberg M (2009) One-dimensional-ratio measures of atrophy progression in multiple sclerosis as evaluated by longitudinal magnetic resonance imaging. Acta Radiol 1–9
Armatige P, Berry G, Matthews JNS (2002) Statistical methods in medical research, 4th edn. Blackwell, Oxford, p 496
Anderson VM, Fox NC, Miller DH (2006) Magnetic resonance imaging measures of brain atrophy in multiple sclerosis. J Magn Res Imaging 23:605–618
Hobart J, Freeman J, Thompson A (2000) Kurtzke scales revisited: the application of psychometric methods to clinical intuition. Brain 123:1027–1040
Scahill RI, Frost C, Jenkins R, Whitwell JL, Rossor MN, Fox NC (2003) A longitudinal study of brain volume changes in normal aging using serial registered magnetic resonance imaging. Arch Neurol 60:989–994
Bozalli M, Cercignani M, Caltagirone C (2008) Brain volumetrics to investigate aging and the principal forms of degenerative cognitive decline: a brief report. Magn Reson Imaging 26:1065–1070
Kochunov P, Thompson PM, Coyle TR, Lancaster JL, Kochunov V, Royall D, Mangin JF, Rivière D, Fox PT (2008) Relationship among neuroimaging indices of cerebral health during normal aging. Hum Brain Mapp 29:36–45
Horsfield MA, Rovaris M, Rocca MA, Rossi P, Benedict RH, Filippi M, Bakshi R (2003) Whole-brain atrophy in multiple sclerosis measured by two segmentation processes from various MRI sequences. J Neurol Sci 216:169–177
Molyneux PD, Kappos L, Polman C, Pozzilli C, Barkhof F, Filippi M, Yousry T, Hahn D, Wagner K, Ghazi M, Beckmann K, Dahlke F, Losseff N, Barker GJ, Thompson AJ, Miller DH (2000) The effect of interferon beta-1b treatment on MRI measures of cerebral atrophy in secondary progressive multiple sclerosis. European Study Group on interferon beta-1b in secondary progressive multiple sclerosis. Brain 123:2256–2263
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Martola, J., Bergström, J., Fredrikson, S. et al. A longitudinal observational study of brain atrophy rate reflecting four decades of multiple sclerosis: a comparison of serial 1D, 2D, and volumetric measurements from MRI images. Neuroradiology 52, 109–117 (2010). https://doi.org/10.1007/s00234-009-0593-9
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DOI: https://doi.org/10.1007/s00234-009-0593-9