Brain morphometric changes associated with childhood-onset systemic lupus erythematosus and neurocognitive deficit

Arthritis and Rheumatism

Volumn 65, Issue 8, 2013, Pages 2190-2200

  Gitelman, Darren R ^a   Klein Gitelman, Marisa S ^a   Ying, Jun ^b   Sagcal Gironella, Anna Carmela P ^b   Zelko, Frank ^a   Beebe, Dean W ^b   Difrancesco, Mark ^b   Parrish, Todd ^a   Hummel, Jessica ^b   Beckwith, Travis ^b   Brunner, Hermine I ^b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ARTICLE; BRAIN REGION; BRAIN SIZE; CHILDHOOD DISEASE; CLINICAL ARTICLE; COGNITION; COGNITIVE DEFECT; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE DURATION; FEMALE; GLOBAL CHANGE; GRAY MATTER; HUMAN; LONGITUDINAL STUDY; MALE; NEUROIMAGING; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; ONSET AGE; PRIORITY JOURNAL; PROBABILITY; PSYCHOMOTOR PERFORMANCE; SYSTEMIC LUPUS ERYTHEMATOSUS; VOXEL BASED MORPHOMETRY; WHITE MATTER; WORKING MEMORY;

ADMINISTRATION, ORAL; ADOLESCENT; AGE OF ONSET; ANTIHYPERTENSIVE AGENTS; BRAIN; COGNITION DISORDERS; COMORBIDITY; DRUG THERAPY, COMBINATION; GLUCOCORTICOIDS; HUMANS; ILLINOIS; IMMUNOSUPPRESSIVE AGENTS; INJECTIONS, INTRAVENOUS; LONGITUDINAL STUDIES; LUPUS ERYTHEMATOSUS, SYSTEMIC; MAGNETIC RESONANCE IMAGING; MALE; NERVE FIBERS, MYELINATED; NERVE FIBERS, UNMYELINATED; NEUROPSYCHOLOGICAL TESTS; OHIO; PSYCHIATRIC STATUS RATING SCALES;

EID: 84881331022     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.38009     Document Type: Article

References (50)

1. Brunner HI, Bishnoi A, Barron AC, Houk LJ, Ware A, Farhey Y, et al. Disease outcomes and ovarian function of childhood-onset systemic lupus erythematosus. Lupus 2006; 15: 198-206.
2. Fragoso-Loyo HE, Sanchez-Guerrero J,. Effect of severe neuropsychiatric manifestations on short-term damage in systemic lupus erythematosus. J Rheumatol 2007; 34: 76-80.
3. ACR Ad Hoc Committee on Neuropsychiatric Lupus Nomenclature. The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum 1999; 42: 599-608.
4. Sanna G, Bertolaccini ML, Cuadrado MJ, Laing H, Khamashta MA, Mathieu A, et al. Neuropsychiatric manifestations in systemic lupus erythematosus: prevalence and association with antiphospholipid antibodies. J Rheumatol 2003; 30: 985-92.
5. Sibbitt WL Jr, Brandt JR, Johnson CR, Maldonado ME, Patel SR, Ford CC, et al. The incidence and prevalence of neuropsychiatric syndromes in pediatric onset systemic lupus erythematosus. J Rheumatol 2002; 29: 1536-42.
6. Ainiala H, Loukkola J, Peltola J, Korpela M, Hietaharju A,. The prevalence of neuropsychiatric syndromes in systemic lupus erythematosus. Neurology 2001; 57: 496-500.
7. Monastero R, Bettini P, Del Zotto E, Cottini E, Tincani A, Balestrieri G, et al. Prevalence and pattern of cognitive impairment in systemic lupus erythematosus patients with and without overt neuropsychiatric manifestations. J Neurol Sci 2001; 184: 33-9.
8. Muscal E, Brey RL,. Neurologic manifestations of systemic lupus erythematosus in children and adults. Neurol Clin 2010; 28: 61-73.
9. Ainiala H, Dastidar P, Loukkola J, Lehtimaki T, Korpela M, Peltola J, et al. Cerebral MRI abnormalities and their association with neuropsychiatric manifestations in SLE: a population-based study. Scand J Rheumatol 2005; 34: 376-82.
10. Bosma GP, Middelkoop HA, Rood MJ, Bollen EL, Huizinga TW, van Buchem MA,. Association of global brain damage and clinical functioning in neuropsychiatric systemic lupus erythematosus. Arthritis Rheum 2002; 46: 2665-72.
11. Muscal E, Bloom DR, Hunter JV, Myones BL,. Neurocognitive deficit and neuroimaging abnormalities are prevalent in children with lupus: clinical and research experiences at a US pediatric institution. Lupus 2010; 19: 268-79.
12. Muscal E, Traipe E, de Guzman MM, Myones BL, Brey RL, Hunter JV,. Cerebral and cerebellar volume loss in children and adolescents with systemic lupus erythematosus: a review of clinically acquired brain magnetic resonance imaging. J Rheumatol 2010; 37: 1768-75.
13. Prismich G, Hilario MO, Len CA, Terreri MT, Quaresma MR, Alonso G, et al. Use of single photon emission computed tomography and magnetic resonance to evaluate central nervous system involvement in patients with juvenile systemic lupus erythematosus. Braz J Med Biol Res 2002; 35: 805-10.
14. Appenzeller S, Bonilha L, Rio PA, Min Li L, Costallat LT, Cendes F,. Longitudinal analysis of gray and white matter loss in patients with systemic lupus erythematosus. Neuroimage 2007; 34: 694-701.
15. Cagnoli PC, Sundgren PC, Kairys A, Graft CC, Clauw DJ, Gebarski S, et al. Changes in regional brain morphology in neuropsychiatric systemic lupus erythematosus. J Rheumatol 2012; 39: 959-67.
16. Jung RE, Segall JM, Grazioplene RG, Qualls C, Sibbitt WL, Roldan CA,. Cortical thickness and subcortical gray matter reductions in neuropsychiatric systemic lupus erythematosus. PLoS One 2010; 5: e9302.
17. Ashburner J, Friston KJ,. Voxel-based morphometry-the methods. Neuroimage 2000; 11: 805-21.
18. Zelko F, Beebe D, Baker A, Nelson SM, Ali A, Cedeno A, et al. Academic outcomes in childhood-onset systemic lupus erythematosus. Arthritis Care Res (Hoboken) 2012; 64: 1167-74.
19. Hochberg MC, for the Diagnostic and Therapeutic Criteria Committee of the American College of Rheumatology. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus [letter]. Arthritis Rheum 1997; 40: 1725.
20. Bartels A, Zeki S,. The neural correlates of maternal and romantic love. Neuroimage 2004; 21: 1155-66.
21. Ross GS, Zelko F, Klein-Gitelman M, Levy DM, Muscal E, Schanberg LE, et al, for the Childhood Arthritis & Rheumatology Research Alliance Ad-Hoc Neurocognitive Lupus Committee. A proposed framework to standardize the neurocognitive assessment of patients with pediatric systemic lupus erythematosus. Arthritis Care Res (Hoboken) 2010; 62: 1029-33.
22. Wechsler D,. WASI: Wechsler Abbreviated Scale of Intelligence. San Antonio (TX): Psych Corp; 1999.
23. Cooper S,. The clinical use and interpretation of the Wechsler intelligence scale for children: revised. 3rd ed. Springfield (IL): Charles C. Thomas; 1995.
24. Wechsler D,. WAIS-IV: Wechsler Adult Intelligence Scale. 4th ed. San Antonio (TX): Pearson Education/PsychCorp; 2008.
25. Woodcock R, Mather N,. Tests of cognitive ability: standard and supplemental batteries. Park Allen (TX): DLM Teaching Resources; 1989.
26. Adams W, Sheslow D,. WRAML2: Wide Range Assessment of Memory and Learning: administration and technical manual. 2nd ed. Wilmington (DE): Wide Range; 2003.
27. Delis DC, Kaplan E, Kramer JH,. The Delis-Kaplan executive function system: technical manual. San Antonio (TX): Psychological Corporation; 2001.
28. Conners CK,. Conners continuous performance task: computer program for Windows. North Tonwanda (NY): Multi-Health Systems; 1995.
29. Daleo DV, Lopez BR, Cole JC, Kaufman AS, Kaufman NL, Newcomer BL, et al. K-ABC simultaneous processing, DAS nonverbal reasoning, and Horn's expanded fluid-crystallized theory. Psychol Rep 1999; 84: 563-74.
30. Kaufman AS, O'Neal MR, Avant AH, Long SW,. Introduction to the Kaufman Assessment Battery for Children (K-ABC) for pediatric neuroclinicians. J Child Neurol 1987; 2: 3-16.
31. Williams TS, Aranow C, Ross GS, Barsdorf A, Imundo LF, Eichenfield AH, et al. Neurocognitive impairment in childhood-onset systemic lupus erythematosus: measurement issues in diagnosis. Arthritis Care Res (Hoboken) 2011; 63: 1178-87.
32. Brunner HI, Ruth NM, German A, Nelson S, Passo MH, Roebuck-Spencer T, et al. Initial validation of the pediatric Automated Neuropsychological Assessment Metrics for childhood-onset systemic lupus erythematosus. Arthritis Rheum 2007; 57: 1174-82.
33. Mikdashi JA, Esdaile JM, Alarcon GS, Crofford L, Fessler BJ, Shanberg L, et al, Ad Hoc Committee on Lupus Response Criteria, Cognition Sub-Committee. Proposed response criteria for neurocognitive impairment in systemic lupus erythematosus clinical trials. Lupus 2007; 16: 418-25.
34. Ashburner J, Friston KJ,. Unified segmentation. Neuroimage 2005; 26: 839-51.
35. Rajapakse JC, Giedd JN, Rapoport JL,. Statistical approach to segmentation of single-channel cerebral MR images. IEEE Trans Med Imaging 1997; 16: 176-86.
36. Tohka J, Zijdenbos A, Evans A,. Fast and robust parameter estimation for statistical partial volume models in brain MRI. Neuroimage 2004; 23: 84-97.
37. Ashburner J,. A fast diffeomorphic image registration algorithm. Neuroimage 2007; 38: 95-113.
38. Manjon JV, Coupe P, Marti-Bonmati L, Collins DL, Robles M,. Adaptive non-local means denoising of MR images with spatially varying noise levels. J Magn Reson Imaging 2010; 31: 192-203.
39. Buckner RL, Snyder AZ, Sanders AL, Raichle ME, Morris JC,. Functional brain imaging of young, nondemented, and demented older adults. J Cogn Neurosci 2000; 12 Suppl 2: 24-34.
40. Smith SM, Nichols TE,. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 2009; 44: 83-98.
41. Hayasaka S, Nichols TE,. Validating cluster size inference: random field and permutation methods. Neuroimage 2003; 20: 2343-56.
42. DiFrancesco MW, Holland SK, Ris MD, Adler CM, Nelson S, DelBello MP, et al. Functional magnetic resonance imaging assessment of cognitive function in childhood-onset systemic lupus erythematosus: a pilot study. Arthritis Rheum 2007; 56: 4151-63.
43. Appenzeller S, Carnevalle AD, Li LM, Costallat LT, Cendes F,. Hippocampal atrophy in systemic lupus erythematosus. Ann Rheum Dis 2006; 65: 1585-9.
44. Appenzeller S, Rondina JM, Li LM, Costallat LT, Cendes F,. Cerebral and corpus callosum atrophy in systemic lupus erythematosus. Arthritis Rheum 2005; 52: 2783-9.
45. Appenzeller S, Vasconcelos Faria A, Li LM, Costallat LT, Cendes F,. Quantitative magnetic resonance imaging analyses and clinical significance of hyperintense white matter lesions in systemic lupus erythematosus patients. Ann Neurol 2008; 64: 635-43.
46. Guiducci C, Gong M, Xu Z, Gill M, Chaussabel D, Meeker T, et al. TLR recognition of self nucleic acids hampers glucocorticoid activity in lupus. Nature 2010; 465: 937-41.
47. Xu J, Cheng Y, Chai P, Lu Z, Li H, Luo C, et al. White-matter volume reduction and the protective effect of immunosuppressive therapy in systemic lupus erythematosus patients with normal appearance by conventional magnetic resonance imaging. J Rheumatol 2010; 37: 974-86.
48. Jednorog K, Altarelli I, Monzalvo K, Fluss J, Dubois J, Billard C, et al. The influence of socioeconomic status on children's brain structure. PLoS One 2012; 7: e42486.
49. Du MY, Wu QZ, Yue Q, Li J, Liao Y, Kuang WH, et al. Voxelwise meta-analysis of gray matter reduction in major depressive disorder. Prog Neuropsychopharmacol Biol Psychiatry 2012; 36: 11-6.
50. Klein-Gitelman MS, Zelko F, Kress A, Hunter S, Wagner-Weiner L,. Comparison of neuro-cognitive function in children with pediatric systemic lupus erythematosus (pSLE) and their peers: second year follow up [abstract]. Arthritis Rheum 2002; 46 Suppl: S216.