Biomarkers for CNS involvement in pediatric lupus

Biomarkers in Medicine

Volumn 9, Issue 6, 2015, Pages 545-558

  Rubinstein, Tamar B ^a   Putterman, Chaim ^a   Goilav, Beatrice ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

biomarkers; CNS; neuropsychiatric; pediatric; systemic lupus erythematosus

Indexed keywords

ALPHA INTERFERON; ANTIBODY; BIOLOGICAL MARKER; CHEMOKINE; CYTOKINE; GELATINASE B; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 1; INTERLEUKIN 17; INTERLEUKIN 6; INTERLEUKIN 8; MICROTUBULE ASSOCIATED PROTEIN 2; MONOCYTE CHEMOTACTIC PROTEIN 1; NEURONAL ANTIBODY; NR2 ANTIBODY; PHOSPHOLIPID ANTIBODY; PROTEIN S100B; RANTES; RIBOSOMAL P ANTIBODY; TNF ASSOCIATED WEAK INDUCER OF APOPOTOSIS; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

CENTRAL NERVOUS SYSTEM DISEASE; CENTRAL NEUROPSYCHIATRIC LUPUS ERYTHEMATOSUS; COST; DIAGNOSTIC TEST; HUMAN; INVASIVE PROCEDURE; MORBIDITY; NEUROIMAGING; NON INVASIVE MEASUREMENT; NONHUMAN; OUTCOME ASSESSMENT; PATHOGENESIS; PATIENT CARE; PEDIATRICS; PSYCHOMETRY; RELIABILITY; REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS; ADOLESCENT; CHILD; METABOLISM; PATHOLOGY; PRESCHOOL CHILD; PSYCHOLOGY;

ADOLESCENT; BIOMARKERS; CENTRAL NERVOUS SYSTEM DISEASES; CHILD; CHILD, PRESCHOOL; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC;

EID: 84931307705     PISSN: 17520363     EISSN: 17520371     Source Type: Journal    
DOI: 10.2217/bmm.15.26     Document Type: Review

References (129)

1. Hiraki LT, Benseler SM, Tyrrell PN, Harvey E, Hebert D, Silverman ED. Ethnic differences in pediatric systemic lupus erythematosus. J. Rheumatol. 36(11), 2539-2546 (2009
2. Kamphuis S, Silverman ED. Prevalence and burden of pediatric-onset systemic lupus erythematosus. Nat. Rev. Rheumatol. 6(9), 538-546 (2010
3. Tucker LB, Menon S, Schaller JG, Isenberg DA. Adult- And childhood-onset systemic lupus erythematosus: a comparison of onset, clinical features, serology, and outcome. Br. J. Rheumatol. 34(9), 866-872 (1995
4. Pons-Estel GJ, Alarcon GS, Scofield L, Reinlib L, Cooper GS. Understanding the epidemiology and progression of systemic lupus erythematosus. Semin. Arthritis Rheum. 39(4), 257-268 (2010
5. Tucker LB, Uribe AG, Fernandez M, et al. Adolescent onset of lupus results in more aggressive disease and worse outcomes: results of a nested matched case-control study within LUMINA, a multiethnic US cohort (LUMINA LVII). Lupus 17(4), 314-322 (2008
6. Mccarty DJ, Manzi S, Medsger TA Jr, Ramsey-Goldman R, Laporte RE, Kwoh CK. Incidence of systemic lupus erythematosus. Race and gender differences. Arthritis Rheum. 38(9), 1260-1270 (1995
7. Cooper GS, Parks CG, Treadwell EL, et al. Differences by race, sex and age in the clinical and immunologic features of recently diagnosed systemic lupus erythematosus patients in the southeastern United States. Lupus 11(3), 161-167 (2002
8. Hanly JG, Urowitz MB, Sanchez-Guerrero J, et al. Neuropsychiatric events at the time of diagnosis of systemic lupus erythematosus: an international inception cohort study. Arthritis Rheum. 56(1), 265-273 (2007
9. Mikdashi J, Handwerger B. Predictors of neuropsychiatric damage in systemic lupus erythematosus: data from the Maryland lupus cohort. Rheumatology (Oxford) 43(12), 1555-1560 (2004
10. Yu HH, Lee JH, Wang LC, Yang YH, Chiang BL. Neuropsychiatric manifestations in pediatric systemic lupus erythematosus: a 20-year study. Lupus 15(10), 651-657 (2006
11. Sibbitt WL Jr, Brandt JR, Johnson CR, et al. The incidence and prevalence of neuropsychiatric syndromes in pediatric onset systemic lupus erythematosus. J. Rheumatol. 29(7), 1536-1542 (2002
12. Klein-Gitelman M, Brunner HI. The impact and implications of neuropsychiatric systemic lupus erythematosus in adolescents. Curr. Rheumatol. Rep. 11(3), 212-217 (2009
13. Brunner HI, Silverman ED, To T, Bombardier C, Feldman BM. Risk factors for damage in childhood-onset systemic lupus erythematosus: cumulative disease activity and medication use predict disease damage. Arthritis Rheum. 46(2), 436-444 (2002
14. Hanly JG. Diagnosis and management of neuropsychiatric SLE. Nat. Rev. Rheumatol. 10(6), 338-347 (2014
15. Jeltsch-David H, Muller S. Neuropsychiatric systemic lupus erythematosus: pathogenesis and biomarkers. Nat. Rev. Neurol. 10(10), 579-596 (2014
16. Levy DM, Ardoin SP, Schanberg LE. Neurocognitive impairment in children and adolescents with systemic lupus erythematosus. Nat. Clin. Pract. Rheumatol. 5(2), 106-114 (2009
17. Goldman J, Becker ML, Jones B, Clements M, Leeder JS. Development of biomarkers to optimize pediatric patient management: what makes children different?. Biomark. Med. 5(6), 781-794 (2011
18. Muscal E, Brey RL. Neurologic manifestations of systemic lupus erythematosus in children and adults. Neurol. Clin. 28(1), 61-73 (2010
19. The American College of Rheumatology nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum. 42(4), 599-608 (1999
20. Hanly JG, Urowitz MB, Su L, et al. Prospective analysis of neuropsychiatric events in an international disease inception cohort of patients with systemic lupus erythematosus. Ann. Rheum. Dis. 69(3), 529-535 (2010
21. Brunner HI, Jones OY, Lovell DJ, Johnson AM, Alexander P, Klein-Gitelman MS. Lupus headaches in childhood-onset systemic lupus erythematosus: relationship to disease activity as measured by the systemic lupus erythematosus disease activity index (SLEDAI) and disease damage. Lupus 12(8), 600-606 (2003
22. Luyendijk J, Steens SC, Ouwendijk WJ, et al. Neuropsychiatric systemic lupus erythematosus: lessons learned from magnetic resonance imaging. Arthritis Rheum. 63(3), 722-732 (2011
23. Lim LS, Lefebvre A, Benseler S, Peralta M, Silverman ED. Psychiatric illness of systemic lupus erythematosus in childhood: spectrum of clinically important manifestations. J. Rheumatol. 40(4), 506-512 (2013
24. Johnson RT, Richardson EP. The neurological manifestations of systemic lupus erythematosus. Medicine (Baltimore) 47(4), 337-369 (1968
25. Hanly JG, Walsh NM, Sangalang V. Brain pathology in systemic lupus erythematosus. J. Rheumatol. 19(5), 732-741 (1992
26. Bertsias GK, Ioannidis JP, Aringer M, et al. EULAR recommendations for the management of systemic lupus erythematosus with neuropsychiatric manifestations: report of a task force of the EULAR standing committee for clinical affairs. Ann. Rheum. Dis. 69(12), 2074-2082 (2010
27. Joseph FG, Lammie GA, Scolding NJ. CNS lupus: a study of 41 patients. Neurology 69(7), 644-654 (2007
28. West SG, Emlen W, Wener MH, Kotzin BL. Neuropsychiatric lupus erythematosus: a 10-year prospective study on the value of diagnostic tests. Am. J. Med. 99(2), 153-163 (1995
29. Olfat MO, Al-Mayouf SM, Muzaffer MA. Pattern of neuropsychiatric manifestations and outcome in juvenile systemic lupus erythematosus. Clin. Rheumatol. 23(5), 395-399 (2004
30. Kozora E, Thompson LL, West SG, Kotzin BL. Analysis of cognitive and psychological deficits in systemic lupus erythematosus patients without overt central nervous system disease. Arthritis Rheum. 39(12), 2035-2045 (1996
31. Monastero R, Bettini P, Del Zotto E, et al. Prevalence and pattern of cognitive impairment in systemic lupus erythematosus patients with and without overt neuropsychiatric manifestations. J. Neurol. Sci. 184(1), 33-39 (2001
32. Kozora E, Ellison MC, West S. Reliability and validity of the proposed American College of Rheumatology neuropsychological battery for systemic lupus erythematosus. Arthritis Rheum. 51(5), 810-818 (2004
33. Ross GS, Zelko F, Klein-Gitelman M, et al A proposed framework to standardize the neurocognitive assessment of patients with pediatric systemic lupus erythematosus. Arthritis Care Res. (Hoboken) 62(7), 1029-1033 (2010
34. Benseler SM, Silverman ED. Neuropsychiatric involvement in pediatric systemic lupus erythematosus. Lupus 16(8), 564-571 (2007
35. Conti F, Alessandri C, Bompane D, et al. Autoantibody profile in systemic lupus erythematosus with psychiatric manifestations: a role for anti-endothelial-cell antibodies. Arthritis Res. Ther. 6(4), R366-R372 (2004
36. Fragoso-Loyo H, Cabiedes J, Orozco-Narvaez A, et al. Serum and cerebrospinal fluid autoantibodies in patients with neuropsychiatric lupus erythematosus. Implications for diagnosis and pathogenesis. PLoS ONE 3(10), e3347 (2008
37. Karassa FB, Ioannidis JP, Touloumi G, Boki KA, Moutsopoulos HM. Risk factors for central nervous system involvement in systemic lupus erythematosus. QJM 93(3), 169-174 (2000
38. Winfield JB, Brunner CM, Koffler D. Serologic studies in patients with systemic lupus erythematosus and central nervous system dysfunction. Arthritis Rheum. 21(3), 289-294 (1978
39. Toledano P, Sarbu N, Espinosa G, Bargallo N, Cervera R. Neuropsychiatric systemic lupus erythematosus: magnetic resonance imaging findings and correlation with clinical and immunological features. Autoimmun. Rev. 12(12), 1166-1170 (2013
40. Yu HH, Wang LC, Lee JH, Lee CC, Yang YH, Chiang BL. Lymphopenia is associated with neuropsychiatric manifestations and disease activity in paediatric systemic lupus erythematosus patients. Rheumatology (Oxford) 46(9), 1492-1494 (2007
41. Elkon K, Skelly S, Parnassa A, et al. Identification and chemical synthesis of a ribosomal protein antigenic determinant in systemic lupus erythematosus. Proc. Natl Acad. Sci. USA 83(19), 7419-7423 (1986
42. Bonfa E, Golombek SJ, Kaufman LD, et al. Association between lupus psychosis and anti-ribosomal P protein antibodies. N. Engl. J. Med. 317(5), 265-271 (1987
43. Arnett FC, Reveille JD, Moutsopoulos HM, Georgescu L, Elkon KB. Ribosomal P autoantibodies in systemic lupus erythematosus. Frequencies in different ethnic groups and clinical and immunogenetic associations. Arthritis Rheum. 39(11), 1833-1839 (1996
44. Reichlin M, Broyles TF, Hubscher O, et al. Prevalence of autoantibodies to ribosomal P proteins in juvenile-onset systemic lupus erythematosus compared with the adult disease. Arthritis Rheum. 42(1), 69-75 (1999
45. Aldar H, Lapa AT, Bellini B, et al. Prevalence and clinical significance of anti-ribosomal P antibody in childhood-onset systemic lupus erythematosus. Lupus 21(11), 1225-1231 (2012
46. Press J, Palayew K, Laxer RM, et al. Antiribosomal P antibodies in pediatric patients with systemic lupus erythematosus and psychosis. Arthritis Rheum. 39(4), 671-676 (1996
47. Katzav A, Solodeev I, Brodsky O, et al. Induction of autoimmune depression in mice by anti-ribosomal P antibodies via the limbic system. Arthritis Rheum. 56(3), 938-948 (2007
48. Haddouk S, Marzouk S, Jallouli M, et al. Clinical and diagnostic value of ribosomal P autoantibodies in systemic lupus erythematosus. Rheumatology (Oxford) 48(8), 953-957 (2009
49. Hanly JG, Urowitz MB, Su L, et al. Autoantibodies as biomarkers for the prediction of neuropsychiatric events in systemic lupus erythematosus. Ann. Rheum. Dis. 70(10), 1726-1732 (2011
50. Carlomagno S, Migliaresi S, Ambrosone L, Sannino M, Sanges G, Di Iorio G. Cognitive impairment in systemic lupus erythematosus: a follow-up study. J. Neurol. 247(4), 273-279 (2000
51. Schenatto CB, Xavier RM, Bredemeier M, et al. Raised serum S100B protein levels in neuropsychiatric lupus. Ann. Rheum. Dis. 65(6), 829-831 (2006
52. Adhikari T, Piatti A, Luggen M. Cognitive dysfunction in SLE: development of a screening tool. Lupus 20(11), 1142-1146 (2011
53. Pamfil C, Fanouriakis A, Damian L, et al. EULAR recommendations for neuropsychiatric systemic lupus erythematosus vs usual care: results from two European centres. Rheumatology (Oxford) pii: keu482 (2015) (Epub ahead of print
54. Ouvrier RA, Goldsmith RF, Ouvrier S, Williams IC. The value of the Mini-Mental State Examination in childhood: a preliminary study. J. Child Neurol. 8(2), 145-148 (1993
55. Hanly JG. New insights into central nervous system lupus: a clinical perspective. Curr. Rheumatol. Rep. 9(2), 116-124 (2007
56. Pendlebury ST, Cuthbertson FC, Welch SJ, Mehta Z, Rothwell PM. Underestimation of cognitive impairment by Mini-Mental State Examination versus the Montreal Cognitive Assessment in patients with transient ischemic attack and stroke: a population-based study. Stroke 41(6), 1290-1293 (2010
57. Nasreddine ZS, Phillips NA, Bedirian V, et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J. Am. Geriatr. Soc. 53(4), 695-699 (2005
58. Alarcon GS, Cianfrini L, Bradley LA, et al. Systemic lupus erythematosus in three ethnic groups. X. Measuring cognitive impairment with the cognitive symptoms inventory. Arthritis Rheum. 47(3), 310-319 (2002
59. Hanly JG, Su L, Omisade A, Farewell VT, Fisk JD. Screening for cognitive impairment in systemic lupus erythematosus. J. Rheumatol. 39(7), 1371-1377 (2012
60. Vega-Fernandez P, Zelko FA, Klein-Gitelman M, et al. Value of questionnaire-based screening as a proxy for neurocognitive testing in childhood-onset systemic lupus erythematosus. Arthritis Care Res. (Hoboken) 66(6), 943-948 (2014
61. Mosca M, Govoni M, Tomietto P, et al. The development of a simple questionnaire to screen patients with SLE for the presence of neuropsychiatric symptoms in routine clinical practice. Lupus 20(5), 485-492 (2011
62. Saylor CF, Finch AJ Jr, Spirito A, Bennett B. The childrens depression inventory: a systematic evaluation of psychometric properties. J. Consult. Clin. Psychol. 52(6), 955-967 (1984
63. Kroenke K, Spitzer RL, Williams JB. The PHQ-9: validity of a brief depression severity measure. J. Gen. Intern. Med. 16(9), 606-613 (2001
64. Birmaher B, Khetarpal S, Brent D, et al. The Screen for Child Anxiety Related Emotional Disorders (SCARED): scale construction and psychometric characteristics. J. Am. Acad. Child Adolesc. Psychiatry 36(4), 545-553 (1997
65. Spitzer RL, Kroenke K, Williams JB, Lowe B A brief measure for assessing generalized anxiety disorder: the GAD-7. Arch. Intern. Med. 166(10), 1092-1097 (2006
66. Nicassio PM, Carr FN, Moldovan I. An overview of psychological functioning in systemic lupus erythematosus. Int. J. Clin. Rheumatol. 6(5), 569-581 (2011
67. Smarr KL, Keefer AL. Measures of depression and depressive symptoms: Beck Depression Inventory-II (BDI-II), Center for Epidemiologic Studies Depression Scale (CES-D), Geriatric Depression Scale (GDS), Hospital Anxiety and Depression Scale (HADS), and Patient Health Questionnaire-9 (PHQ-9). Arthritis Care Res. (Hoboken). 63(Suppl 11), S454-S466 (2011
68. Knight A, Weiss P, Morales K, et al. Depression and anxiety and their association with healthcare utilization in pediatric lupus and mixed connective tissue disease patients: a crosssectional study. Pediatr. Rheumatol. Online J. 12, 42 (2014
69. Brunner HI, Ruth NM, German A, et al. Initial validation of the Pediatric Automated Neuropsychological Assessment Metrics for childhood-onset systemic lupus erythematosus. Arthritis Rheum. 57(7), 1174-1182 (2007
70. Brooks BL, Sherman EMS. Computerized neuropsychological testing to rapidly evaluate cognition in pediatric patients with neurologic disorders. J. Child Neurol. 27(8), 982-991 (2012
71. Brunner HI, Klein-Gitelman MS, Zelko F, et al. Validation of the Pediatric Automated Neuropsychological Assessment Metrics in childhood-onset systemic lupus erythematosus. Arthritis Care Res. (Hoboken) 65(3), 372-381 (2013
72. Vega-Fernandez P, Vanderburgh White S, Zelko F, et al. Cognitive performance scores for the pediatric automated neuropsychological assessment metrics in childhood-onset systemic lupus erythematosus. Arthritis Care Res. (Hoboken) doi:10.1002/acr.22571 (2015) (Epub ahead of print
73. Mortilla M, Ermini M, Nistri M, Dal Pozzo G, Falcini F. Brain study using magnetic resonance imaging and proton MR spectroscopy in pediatric onset systemic lupus erythematosus. Clin. Exp. Rheumatol. 21(1), 129-135 (2003
74. Difrancesco MW, Holland SK, Ris MD, et al. Functional magnetic resonance imaging assessment of cognitive function in childhood-onset systemic lupus erythematosus: a pilot study. Arthritis Rheum. 56(12), 4151-4163 (2007
75. Difrancesco MW, Gitelman DR, Klein-Gitelman MS, et al. Functional neuronal network activity differs with cognitive dysfunction in childhood-onset systemic lupus erythematosus. Arthritis Res. Ther. 15(2), R40 (2013
76. Byars AW, Holland SK, Strawsburg RH, et al. Practical aspects of conducting large-scale functional magnetic resonance imaging studies in children. J. Child Neurol. 17(12), 885-890 (2002
77. Falcini F, De Cristofaro MT, Ermini M, et al. Regional cerebral blood flow in juvenile systemic lupus erythematosus: a prospective SPECT study. Single photon emission computed tomography. J. Rheumatol. 25(3), 583-588 (1998
78. Reiff A, Miller J, Shaham B, Bernstein B, Szer IS. Childhood central nervous system lupus; longitudinal assessment using single photon emission computed tomography. J. Rheumatol. 24(12), 2461-2465 (1997
79. Russo R, Gilday D, Laxer RM, Eddy A, Silverman ED. Single photon emission computed tomography scanning in childhood systemic lupus erythematosus. J. Rheumatol. 25(3), 576-582 (1998
80. Fahey FH, Treves ST, Adelstein SJ. Minimizing and communicating radiation risk in pediatric nuclear medicine. J. Nucl. Med. 52(8), 1240-1251 (2011
81. Lancaster E, Dalmau J. Neuronal autoantigens -pathogenesis, associated disorders and antibody testing. Nat. Rev. Neurol. 8(7), 380-390 (2012
82. Bluestein HG, Williams GW, Steinberg AD. Cerebrospinal fluid antibodies to neuronal cells: association with neuropsychiatric manifestations of systemic lupus erythematosus. Am. J. Med. 70(2), 240-246 (1981
83. Wilson HA, Winfield JB, Lahita RG, Koffler D. Association of IgG anti-brain antibodies with central nervous system dysfunction in systemic lupus erythematosus. Arthritis Rheum. 22(5), 458-462 (1979
84. Hanly JG, Walsh NM, Fisk JD, et al. Cognitive impairment and autoantibodies in systemic lupus erythematosus. Br. J. Rheumatol. 32(4), 291-296 (1993
85. Long AA, Denburg SD, Carbotte RM, Singal DP, Denburg JA. Serum lymphocytotoxic antibodies and neurocognitive function in systemic lupus erythematosus. Ann. Rheum. Dis. 49(4), 249-253 (1990
86. Papero PH, Bluestein HG, White P, Lipnick RN. Neuropsychologic deficits and antineuronal antibodies in pediatric systemic lupus erythematosus. Clin. Exp. Rheumatol. 8(4), 417-424 (1990
87. Muscal E, Minta AA, Myones BL. Anti-neuronal, antiribosomal P, and anti-phospholipid antibodies in pediatric neuropsychiatric lupus. Arthritis Rheum. 52(9S), S621 (2005
88. Mostafa GA, Nazif HK, El-Shahawi HH, Abd El Aziz MM, Hassan MA. Antineuronal antibodies and electroneurophysiological studies in pediatric patients with neuropsychiatric systemic lupus erythematosus. Pediatr. Allergy Immunol. 20(2), 192-199 (2009
89. Isshi K, Hirohata S. Differential roles of the anti-ribosomal P antibody and antineuronal antibody in the pathogenesis of central nervous system involvement in systemic lupus erythematosus. Arthritis Rheum. 41(10), 1819-1827 (1998
90. Putterman, C, Diamond B. Immunization with a peptide surrogate for double-stranded DNA (dsDNA) induces autoantibody production and renal immunoglobulin deposition. J. Exp. Med. 188(1), 29-38 (1998
91. Degiorgio LA, Konstantinov KN, Lee SC, Hardin JA, Volpe BT, Diamond B A subset of lupus anti-DNA antibodies cross-reacts with the NR2 glutamate receptor in systemic lupus erythematosus. Nat. Med. 7(11), 1189-1193 (2001
92. Arinuma Y, Yanagida T, Hirohata S. Association of cerebrospinal fluid anti-NR2 glutamate receptor antibodies with diffuse neuropsychiatric systemic lupus erythematosus. Arthritis Rheum. 58(4), 1130-1135 (2008
93. Massardo L, Bravo-Zehnder M, Calderon J, et al. Anti N-methyl-D-Aspartate receptor and anti-ribosomal-P autoantibodies contribute to cognitive dysfunction in systemic lupus erythematosus. Lupus 24(6), 558-568 (2014
94. Levy DM. Anti-NR-2 antibodies are prevalent in childhoodonset SLE (cSLE), but do not predict neurocognitive dysfunction. Arthritis Rheum. 55, S143 (2007
95. Huerta PT, Kowal C, Degiorgio LA, Volpe BT, Diamond B. Immunity and behavior: antibodies alter emotion. Proc. Natl Acad. Sci. USA 103(3), 678-683 (2006
96. Aranow C, Diamond B, Mackay M. Glutamate receptor biology and its clinical significance in neuropsychiatric systemic lupus erythematosus. Rheum. Dis. Clin. North Am. 36(1), 187-201 (2010
97. Santer DM, Yoshio T, Minota S, Moller T, Elkon KB. Potent induction of IFN-Alpha and chemokines by autoantibodies in the cerebrospinal fluid of patients with neuropsychiatric lupus. J. Immunol. 182(2), 1192-1201 (2009
98. Hirohata S, Kanai Y, Mitsuo A, Tokano Y, Hashimoto H, Subcommittee NR. Accuracy of cerebrospinal fluid IL-6 testing for diagnosis of lupus psychosis A multicenter retrospective study. Clin. Rheumatol. 28(11), 1319-1323 (2009
99. Harel L, Sandborg C, Lee T, Von Scheven E. Neuropsychiatric manifestations in pediatric systemic lupus erythematosus and association with antiphospholipid antibodies. J. Rheumatol. 33(9), 1873-1877 (2006
100. Avcin T, Benseler SM, Tyrrell PN, Cucnik S, Silverman ED A followup study of antiphospholipid antibodies and associated neuropsychiatric manifestations in 137 children with systemic lupus erythematosus. Arthritis Rheum. 59(2), 206-213 (2008
101. Von Scheven E, Glidden DV, Elder ME. Anti-beta2 glycoprotein I antibodies in pediatric systemic lupus erythematosus and antiphospholipid syndrome. Arthritis Rheum. 47(4), 414-420 (2002
102. Brey RL, Muscal E, Chapman J. Antiphospholipid antibodies and the brain: a consensus report. Lupus 20(2), 153-157 (2011
103. Katzav A, Shoenfeld Y, Chapman J. The pathogenesis of neural injury in animal models of the antiphospholipid syndrome. Clin. Rev. Allergy Immunol. 38(2-3), 196-200 (2010
104. Lee T, Von Scheven E, Sandborg C. Systemic lupus erythematosus and antiphospholipid syndrome in children and adolescents. Curr. Opin. Rheumatol. 13(5), 415-421 (2001
105. Menon S, Jameson-Shortall E, Newman SP, Hall-Craggs MR, Chinn R, Isenberg DA A longitudinal study of anticardiolipin antibody levels and cognitive functioning in systemic lupus erythematosus. Arthritis Rheum. 42(4), 735-741 (1999
106. Hanly JG, Hong C, Smith S, Fisk JD A prospective analysis of cognitive function and anticardiolipin antibodies in systemic lupus erythematosus. Arthritis Rheum. 42(4), 728-734 (1999
107. Denburg SD, Denburg JA. Cognitive dysfunction and antiphospholipid antibodies in systemic lupus erythematosus. Lupus 12(12), 883-890 (2003
108. Whitelaw DA, Spangenberg JJ, Rickman R, Hugo FH, Roberts M. The association between the antiphospholipid antibody syndrome and neuropsychological impairment in SLE. Lupus 8(6), 444-448 (1999
109. Sanna G, Piga M, Terryberry JW, et al. Central nervous system involvement in systemic lupus erythematosus: cerebral imaging and serological profile in patients with and without overt neuropsychiatric manifestations. Lupus 9(8), 573-583 (2000
110. Williams RC Jr, Sugiura K, Tan EM. Antibodies to microtubule-Associated protein 2 in patients with neuropsychiatric systemic lupus erythematosus. Arthritis Rheum. 50(4), 1239-1247 (2004
111. Abbott NJ, Ronnback L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 7(1), 41-53 (2006
112. Dillon MJ, Tizard EJ. Anti-neutrophil cytoplasmic antibodies and anti-endothelial cell antibodies. Pediatr. Nephrol. 5(2), 256-259 (1991
113. Wen J, Xia Y, Stock A, et al. Neuropsychiatric disease in murine lupus is dependent on the TWEAK/Fn14 pathway. J. Autoimmun. 43, 44-54 (2013
114. Stock AD, Wen J, Putterman C. Neuropsychiatric lupus, the blood brain barrier, and the TWEAK/Fn14 pathway. Front. Immunol. 4, 484 (2013
115. Trysberg E, Su L, Michaelson JS, Putterman C. CSF TWEAK: a novel biomarker for neuropsychiatric SLE?. Arthritis Rheum. 56, S750 (2007
116. Trysberg E, Nylen K, Rosengren LE, Tarkowski A. Neuronal and astrocytic damage in systemic lupus erythematosus patients with central nervous system involvement. Arthritis Rheum. 48(10), 2881-2887 (2003
117. Jeltsch-David H, Muller S. Neuropsychiatric systemic lupus erythematosus: pathogenesis and biomarkers. Nat. Rev. Neurol. 10(10), 579-596 (2014
118. Ainiala H, Hietaharju A, Dastidar P, et al. Increased serum matrix metalloproteinase 9 levels in systemic lupus erythematosus patients with neuropsychiatric manifestations and brain magnetic resonance imaging abnormalities. Arthritis Rheum. 50(3), 858-865 (2004
119. Abbott NJ, Mendonca LL, Dolman DE. The blood-brain barrier in systemic lupus erythematosus. Lupus 12(12), 908-915 (2003
120. Zetterberg H, Smith DH, Blennow K. Biomarkers of mild traumatic brain injury in cerebrospinal fluid and blood. Nat. Rev. Neurol. 9(4), 201-210 (2013
121. Donato R. S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int. J. Biochem. Cell Biol. 33(7), 637-668 (2001
122. Marenholz I, Heizmann CW, Fritz G. S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature). Biochem. Biophys. Res. Commun. 322(4), 1111-1122 (2004
123. Sen J, Belli A. S100B in neuropathologic states: the CRP of the brain?. J. Neurosci. Res. 85(7), 1373-1380 (2007
124. Portela LV, Brenol JC, Walz R, et al. Serum S100B levels in patients with lupus erythematosus: preliminary observation. Clin. Diagn. Lab. Immunol. 9(1), 164-166 (2002
125. Yang XY, Lin J, Lu XY, Zhao XY. Expression of S100B protein levels in serum and cerebrospinal fluid with different forms of neuropsychiatric systemic lupus erythematosus. Clin. Rheumatol. 27(3), 353-357 (2008
126. Fragoso-Loyo H, Cabiedes J, Atisha-Fregoso Y, Llorente L, Sanchez-Guerrero J. Utility of serum S100B protein for identification of central nervous system involvement in systemic lupus erythematosus. J. Rheumatol. 37(11), 2280-2285 (2010
127. Brunner HI, Klein-Gitelman MS, Zelko F, et al. Blood-based candidate biomarkers of the presence of neuropsychiatric systemic lupus erythematosus in children. Lupus Sci. Med. 1(1), e000038 (2014
128. Portela LV, Tort AB, Schaf DV, et al. The serum S100B concentration is age dependent. Clin. Chem. 48(6 Pt 1), 950-952 (2002
129. Steiner J, Schiltz K, Walter M, et al. S100B serum levels are closely correlated with body mass index: an important caveat in neuropsychiatric research. Psychoneuroendocrinology 35(2), 321-324 (2010