New insights into the impact of neuro-inflammation in rheumatoid arthritis

Frontiers in Neuroscience

Volumn 8, Issue OCT, 2014, Pages

  Fuggle, Nicholas R ^a   Howe, Franklyn A ^a   Allen, Rachel ^a   Sofat, Nidhi ^a  

^a ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Infection; Lipopolysaccharide; Neuroimaging; Neuroinflammation; Rheumatoid arthritis; Tumour necrosis factor alpha

Indexed keywords

IMMUNOSUPPRESSIVE AGENT; PROSTAGLANDIN SYNTHASE; PROSTANOID; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA ANTIBODY;

ARTICLE; BACTERIAL INFECTION; HUMAN; INFECTION; INFECTION RISK; META ANALYSIS (TOPIC); MYCOBACTERIOSIS; NERVOUS SYSTEM INFLAMMATION; NEUROIMMUNOLOGY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OPPORTUNISTIC INFECTION; PAIN; PATHOGENESIS; RANDOMIZED CONTROLLED TRIAL (TOPIC); RHEUMATOID ARTHRITIS; SYSTEMATIC REVIEW (TOPIC); VIRUS INFECTION;

EID: 84949116610     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2014.00357     Document Type: Article

References (100)

1. Feldmann M, Maini RN. Anti-TNF therapy, from rationale to standard of care: what lessons has it taught us? J Immunol 2010 Jul 15;185(2):791-794.
2. McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med 2011 Dec 8;365(23):2205-2219.
3. Scott DL, Wolfe F, Huizinga TW. Rheumatoid arthritis. Lancet 2010 Sep 25;376(9746):1094-1108.
4. Firestein GS. Evolving concepts of rheumatoid arthritis. Nature 2003 May 15;423(6937):356-361.
5. Rech J, Hess A, Finzel S, Kreitz S, Sergeeva M, Englbrecht M, et al. Association of brain functional magnetic resonance activity with response to tumor necrosis factor inhibition in rheumatoid arthritis. Arthritis Rheum 2013 Feb;65(2):325-333.
6. O'Callaghan JP, Sriram K, Miller DB. Defining "neuroinflammation". Ann N Y Acad Sci 2008 Oct;1139:318-330.
7. Thomson CA, McColl A, Cavanagh J, Graham GJ. Peripheral inflammation is associated with remote global gene expression changes in the brain. J Neuroinflammation 2014 Apr 8;11:73-2094-11-73.
8. Skelly DT, Hennessy E, Dansereau MA, Cunningham C. A systematic analysis of the peripheral and CNS effects of systemic LPS, IL-1beta, [corrected] TNF-alpha and IL-6 challenges in C57BL/6 mice. PLoS One 2013 Jul 1;8(7):e69123.
9. Chou R, Kane M, Ghimire S, Gautam S. Tumor necrosis factor inhibition reduces the incidence of Alzheimer's disease in rheumatoid arthritis patients. American College of Rheumatology 2010(Abstract 640).
10. Detrait ER, Danis B, Lamberty Y, Foerch P. Peripheral administration of an anti-TNFalpha receptor fusion protein counteracts the amyloid induced elevation of hippocampal TNF-alpha levels and memory deficits in mice. Neurochem Int 2014 Jun;72:10-13.
11. van Vollenhoven RF. New and future agents in the treatment of rheumatoid arthritis. Discov Med 2010 Apr;9(47):319-327.
12. Mahdi H, Fisher BA, Kallberg H, Plant D, Malmstrom V, Ronnelid J, et al. Specific interaction between genotype, smoking and autoimmunity to citrullinated alpha-enolase in the etiology of rheumatoid arthritis. Nat Genet 2009 Dec;41(12):1319-1324.
13. MacGregor AJ, Snieder H, Rigby AS, Koskenvuo M, Kaprio J, Aho K, et al. Characterizing the quantitative genetic contribution to rheumatoid arthritis using data from twins. Arthritis Rheum 2000 Jan;43(1):30-37.
14. Wellcome Trust Case Control Consortium. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 2007 Jun 7;447(7145):661-678.
15. Gregersen PK, Silver J, Winchester RJ. The shared epitope hypothesis. An approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum 1987 Nov;30(11):1205-1213.
16. Panayi GS. Even though T-cell-directed trials have been of limited success, is there reason for optimism? Nat Clin Pract Rheumatol 2006 Feb;2(2):58-59.
17. Weyand CM, Goronzy JJ. Disease-associated human histocompatibility leukocyte antigen determinants in patients with seropositive rheumatoid arthritis. Functional role in antigen-specific and allogeneic T cell recognition. J Clin Invest 1990 Apr;85(4):1051-1057.
18. De Almeida DE, Ling S, Pi X, Hartmann-Scruggs AM, Pumpens P, Holoshitz J. Immune dysregulation by the rheumatoid arthritis shared epitope. J Immunol 2010 Aug 1;185(3):1927-1934.
19. Klareskog L, Ronnelid J, Lundberg K, Padyukov L, Alfredsson L. Immunity to citrullinated proteins in rheumatoid arthritis. Annu Rev Immunol 2008;26:651-675.
20. Symmons DP, Bankhead CR, Harrison BJ, Brennan P, Barrett EM, Scott DG, et al. Blood transfusion, smoking, and obesity as risk factors for the development of rheumatoid arthritis: results from a primary care-based incident case-control study in Norfolk, England. Arthritis Rheum 1997 Nov;40(11):1955-1961.
21. Vincent C, de Keyser F, Masson-Bessiere C, Sebbag M, Veys EM, Serre G. Antiperinuclear factor compared with the so called "antikeratin" antibodies and antibodies to human epidermis filaggrin, in the diagnosis of arthritides. Ann Rheum Dis 1999 Jan;58(1):42-48.
22. Mikuls TR, Payne JB, Yu F, Thiele GM, Reynolds RJ, Cannon GW, et al. Periodontitis and Porphyromonas gingivalis in patients with rheumatoid arthritis. Arthritis Rheumatol 2014 May;66(5):1090-1100.
23. van der Woude D, Rantapaa-Dahlqvist S, Ioan-Facsinay A, Onnekink C, Schwarte CM, Verpoort KN, et al. Epitope spreading of the anti-citrullinated protein antibody response occurs before disease onset and is associated with the disease course of early arthritis. Ann Rheum Dis 2010 Aug;69(8):1554-1561.
24. van Heemst J, van der Woude D, Huizinga TW, Toes RE. HLA and rheumatoid arthritis: How do they connect? Ann Med 2014 Aug;46(5):304-310.
25. De Rycke L, Peene I, Hoffman IE, Kruithof E, Union A, Meheus L, et al. Rheumatoid factor and anticitrullinated protein antibodies in rheumatoid arthritis: diagnostic value, associations with radiological progression rate, and extra-articular manifestations. Ann Rheum Dis 2004 Dec;63(12):1587-1593.
26. Wegner N, Wait R, Sroka A, Eick S, Nguyen KA, Lundberg K, et al. Peptidylarginine deiminase from Porphyromonas gingivalis citrullinates human fibrinogen and alpha-enolase: implications for autoimmunity in rheumatoid arthritis. Arthritis Rheum 2010 Sep;62(9):2662-2672.
27. Scher JU, Ubeda C, Equinda M, Khanin R, Buischi Y, Viale A, et al. Periodontal disease and the oral microbiota in new-onset rheumatoid arthritis. Arthritis Rheum 2012 Oct;64(10):3083-3094.
28. Sokka T, Toloza S, Cutolo M, Kautiainen H, Makinen H, Gogus F, et al. Women, men, and rheumatoid arthritis: analyses of disease activity, disease characteristics, and treatments in the QUEST-RA study. Arthritis Res Ther 2009;11(1):R7.
29. Capellino S, Cosentino M, WolffC, Schmidt M, Grifka J, Straub RH. Catecholamineproducing cells in the synovial tissue during arthritis: modulation of sympathetic neurotransmitters as new therapeutic target. Ann Rheum Dis 2010 Oct;69(10):1853-1860.
30. Mellor R. Cellular origin of rheumatoid factor. J Exp Med 1959;110(6):875-876.
31. Inan AS, Masatlioglu S, Ozyurek SC, Engin D, Erdem I. Unusual central nervous system involvement of rheumatoid arthritis: successful treatment with steroid and azathioprine. Rheumatol Int 2011 Oct;31(10):1383-1385.
32. Markenson JA, McDougal JS, Tsairis P, Lockshin MD, Christian CL. Rheumatoid meningitis: a localized immune process. Ann Intern Med 1979 May;90(5):786-789.
33. Teeling JL, Carare RO, Glennie MJ, Perry VH. Intracerebral immune complex formation induces inflammation in the brain that depends on Fc receptor interaction. Acta Neuropathol 2012 Oct;124(4):479-490.
34. Upadhyay J, Baker SJ, Rajagovindan R, Hart M, Chandran P, Hooker BA, et al. Pharmacological modulation of brain activity in a preclinical model of osteoarthritis. Neuroimage 2013 Jan 1;64:341-355.
35. Parks EL, Geha PY, Baliki MN, Katz J, Schnitzer TJ, Apkarian AV. Brain activity for chronic knee osteoarthritis: dissociating evoked pain from spontaneous pain. Eur J Pain 2011 Sep;15(8):843.e1-843.14.
36. Ho L, Purohit D, Haroutunian V, Luterman JD, Willis F, Naslund J, et al. Neuronal cyclooxygenase 2 expression in the hippocampal formation as a function of the clinical progression of Alzheimer disease. Arch Neurol 2001 Mar;58(3):487-492.
37. Hull M, Muksch B, Akundi RS, Waschbisch A, Hoozemans JJ, Veerhuis R, et al. Amyloid beta peptide (25-35) activates protein kinase C leading to cyclooxygenase-2 induction and prostaglandin E2 release in primary midbrain astrocytes. Neurochem Int 2006 Jun;48(8):663-672.
38. Combs CK, Karlo JC, Kao SC, Landreth GE. beta-Amyloid stimulation of microglia and monocytes results in TNFalpha-dependent expression of inducible nitric oxide synthase and neuronal apoptosis. J Neurosci 2001 Feb 15;21(4):1179-1188.
39. Medeiros R, Prediger RD, Passos GF, Pandolfo P, Duarte FS, Franco JL, et al. Connecting TNF-alpha signaling pathways to iNOS expression in a mouse model of Alzheimer's disease: relevance for the behavioral and synaptic deficits induced by amyloid beta protein. J Neurosci 2007 May 16;27(20):5394-5404.
40. Hunter RL, Dragicevic N, Seifert K, Choi DY, Liu M, Kim HC, et al. Inflammation induces mitochondrial dysfunction and dopaminergic neurodegeneration in the nigrostriatal system. J Neurochem 2007 Mar;100(5):1375-1386.
41. Chiu IM, Heesters BA, Ghasemlou N, Von Hehn CA, Zhao F, Tran J, et al. Bacteria activate sensory neurons that modulate pain and inflammation. Nature 2013 Sep 5;501(7465):52-57.
42. Taylor PC. Aetiopathology of rheumatoid arthritis. Medicine 2014;42(5):227-230.
43. Malaviya AP, Ostor AJ. Rheumatoid arthritis and the era of biologic therapy. Inflammopharmacology 2012 Apr;20(2):59-69.
44. Smolen JS, Landewe R, Breedveld FC, Buch M, Burmester G, Dougados M, et al. EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2013 update. Ann Rheum Dis 2014 Mar;73(3):492-509.
45. Harris J, Keane J. How tumour necrosis factor blockers interfere with tuberculosis immunity. Clin Exp Immunol 2010 Jul 1;161(1):1-9.
46. Tracey D, Klareskog L, Sasso EH, Salfeld JG, Tak PP. Tumor necrosis factor antagonist mechanisms of action: a comprehensive review. Pharmacol Ther 2008 Feb;117(2):244-279.
47. Kaltsonoudis E, Zikou AK, Voulgari PV, Konitsiotis S, Argyropoulou MI, Drosos AA. Neurological adverse events in patients receiving anti-TNF therapy: a prospective imaging and electrophysiological study. Arthritis Res Ther 2014 Jun 17;16(3):R125.
48. Germano V, Cattaruzza MS, Osborn J, Tarantino A, Di Rosa R, Salemi S, et al. Infection risk in Rheumatoid Arthritis and Spondyloarthropathy patients under treatment with DMARDs, Corticosteroids and TNF-alpha antagonists. J Transl Med 2014 Mar 22;12:77-5876-12-77.
49. Burmester GR, Panaccione R, Gordon KB, McIlraith MJ, Lacerda AP. Adalimumab: long-term safety in 23 458 patients from global clinical trials in rheumatoid arthritis, juvenile idiopathic arthritis, ankylosing spondylitis, psoriatic arthritis, psoriasis and Crohn's disease. Ann Rheum Dis 2013 Apr;72(4):517-524.
50. Bean AG, Roach DR, Briscoe H, France MP, Korner H, Sedgwick JD, et al. Structural deficiencies in granuloma formation in TNF gene-targeted mice underlie the heightened susceptibility to aerosol Mycobacterium tuberculosis infection, which is not compensated for by lymphotoxin. J Immunol 1999 Mar 15;162(6):3504-3511.
51. Senaldi G, Yin S, Shaklee CL, Piguet PF, Mak TW, Ulich TR. Corynebacterium parvum- and Mycobacterium bovis bacillus Calmette-Guerin-induced granuloma formation is inhibited in TNF receptor I (TNF-RI) knockout mice and by treatment with soluble TNF-RI. J Immunol 1996 Dec 1;157(11):5022-5026.
52. Keane J, Gershon S, Wise RP, Mirabile-Levens E, Kasznica J, Schwieterman WD, et al. Tuberculosis associated with infliximab, a tumor necrosis factor alpha-neutralizing agent. N Engl J Med 2001 Oct 11;345(15):1098-1104.
53. Tubach F, Salmon D, Ravaud P, Allanore Y, Goupille P, Breban M, et al. Risk of tuberculosis is higher with anti-tumor necrosis factor monoclonal antibody therapy than with soluble tumor necrosis factor receptor therapy: The three-year prospective French Research Axed on Tolerance of Biotherapies registry. Arthritis Rheum 2009 Jul;60(7):1884-1894.
54. Ramiro S, Gaujoux-Viala C, Nam JL, Smolen JS, Buch M, Gossec L, et al. Safety of synthetic and biological DMARDs: a systematic literature review informing the 2013 update of the EULAR recommendations for management of rheumatoid arthritis. Ann Rheum Dis 2014 Mar;73(3):529-535.
55. Salmon-Ceron D, Tubach F, Lortholary O, Chosidow O, Bretagne S, Nicolas N, et al. Drug-specific risk of non-tuberculosis opportunistic infections in patients receiving anti-TNF therapy reported to the 3-year prospective French RATIO registry. Ann Rheum Dis 2011 Apr;70(4):616-623.
56. Wolfe F, Michaud K, Chakravarty EF. Rates and predictors of herpes zoster in patients with rheumatoid arthritis and non-inflammatory musculoskeletal disorders. Rheumatology (Oxford) 2006 Nov;45(11):1370-1375.
57. Strangfeld A, Listing J, Herzer P, Liebhaber A, Rockwitz K, Richter C, et al. Risk of herpes zoster in patients with rheumatoid arthritis treated with anti-TNF-alpha agents. JAMA 2009 Feb 18;301(7):737-744.
58. Wallis RS, Broder MS, Wong JY, Hanson ME, Beenhouwer DO. Granulomatous infectious diseases associated with tumor necrosis factor antagonists. Clin Infect Dis 2004 May 1;38(9):1261-1265.
59. Lipsky PE, van der Heijde DM, St Clair EW, Furst DE, Breedveld FC, Kalden JR, et al. Infliximab and methotrexate in the treatment of rheumatoid arthritis. Anti-Tumor Necrosis Factor Trial in Rheumatoid Arthritis with Concomitant Therapy Study Group. N Engl J Med 2000 Nov 30;343(22):1594-1602.
60. Keystone EC, Kavanaugh AF, Sharp JT, Tannenbaum H, Hua Y, Teoh LS, et al. Radiographic, clinical, and functional outcomes of treatment with adalimumab (a human antitumor necrosis factor monoclonal antibody) in patients with active rheumatoid arthritis receiving concomitant methotrexate therapy: a randomized, placebo-controlled, 52-week trial. Arthritis Rheum 2004 May;50(5):1400-1411.
61. Doran MF, Crowson CS, Pond GR, O'Fallon WM, Gabriel SE. Frequency of infection in patients with rheumatoid arthritis compared with controls: a population-based study. Arthritis Rheum 2002 Sep;46(9):2287-2293.
62. Ni Mhuircheartaigh OM, Matteson EL, Green AB, Crowson CS. Trends in serious infections in rheumatoid arthritis. J Rheumatol 2013 May;40(5):611-616.
63. Doran MF, Crowson CS, Pond GR, O'Fallon WM, Gabriel SE. Predictors of infection in rheumatoid arthritis. Arthritis Rheum 2002 Sep;46(9):2294-2300.
64. Jacobs AH, Tavitian B, INMiND consortium. Noninvasive molecular imaging of neuroinflammation. J Cereb Blood Flow Metab 2012 Jul;32(7):1393-1415.
65. Nishioku T, Furusho K, Tomita A, Ohishi H, Dohgu S, Shuto H, et al. Potential role for S100A4 in the disruption of the blood-brain barrier in collagen-induced arthritic mice, an animal model of rheumatoid arthritis. Neuroscience 2011 Aug 25;189:286-292.
66. Bongartz T, Sutton AJ, Sweeting MJ, Buchan I, Matteson EL, Montori V. Anti-TNF antibody therapy in rheumatoid arthritis and the risk of serious infections and malignancies: systematic review and meta-analysis of rare harmful effects in randomized controlled trials. JAMA 2006 May 17;295(19):2275-2285.
67. Listing J, Strangfeld A, Kary S, Rau R, von Hinueber U, Stoyanova-Scholz M, et al. Infections in patients with rheumatoid arthritis treated with biologic agents. Arthritis Rheum 2005 Nov;52(11):3403-3412.
68. Alten R, Kaine J, Keystone E, Nash P, Delaet I, Genovese MC. Long-term safety of subcutaneous abatacept in rheumatoid arthritis: Integrated analysis of clinical trial data of up to 4.75 years of treatment. Arthritis Rheumatol 2014 Apr 29.
69. Leombruno JP, Einarson TR, Keystone EC. The safety of anti-tumour necrosis factor treatments in rheumatoid arthritis: meta and exposure-adjusted pooled analyses of serious adverse events. Ann Rheum Dis 2009 Jul;68(7):1136-1145.
70. Schoels M, Aletaha D, Smolen JS, Wong JB. Comparative effectiveness and safety of biological treatment options after tumour necrosis factor alpha inhibitor failure in rheumatoid arthritis: systematic review and indirect pairwise meta-analysis. Ann Rheum Dis 2012 Aug;71(8):1303-1308.
71. Salliot C, Dougados M, Gossec L. Risk of serious infections during rituximab, abatacept and anakinra treatments for rheumatoid arthritis: meta-analyses of randomised placebocontrolled trials. Ann Rheum Dis 2009 Jan;68(1):25-32.
72. Burmester GR, Kivitz AJ, Kupper H, Arulmani U, Florentinus S, Goss SL, et al. Efficacy and safety of ascending methotrexate dose in combination with adalimumab: the randomised CONCERTO trial. Ann Rheum Dis 2014 Feb 18.
73. Serrats J, Sawchenko PE. How T-cell-dependent and -independent challenges access the brain: vascular and neural responses to bacterial lipopolysaccharide and staphylococcal enterotoxin B. Brain Behav Immun 2009 Oct;23(7):1038-1052.
74. Nadeau S, Rivest S. Effects of circulating tumor necrosis factor on the neuronal activity and expression of the genes encoding the tumor necrosis factor receptors (p55 and p75) in the rat brain: a view from the blood-brain barrier. Neuroscience 1999;93(4):1449-1464.
75. Askling J, Dixon W. The safety of anti-tumour necrosis factor therapy in rheumatoid arthritis. Curr Opin Rheumatol 2008 Mar;20(2):138-144.
76. Rosenblum H, Amital H. Anti-TNF therapy: safety aspects of taking the risk. Autoimmun Rev 2011 Jul;10(9):563-568.
77. Meseguer V, Alpizar YA, Luis E, Tajada S, Denlinger B, Fajardo O, et al. TRPA1 channels mediate acute neurogenic inflammation and pain produced by bacterial endotoxins. Nat Commun 2014;5:3125.
78. Woolf CJ. Evidence for a central component of post-injury pain hypersensitivity. Nature 1983 Dec 15-21;306(5944):686-688.
79. Morris VH, Cruwys SC, Kidd BL. Characterisation of capsaicin-induced mechanical hyperalgesia as a marker for altered nociceptive processing in patients with rheumatoid arthritis. Pain 1997 Jun;71(2):179-186.
80. Lee YC, Nassikas NJ, Clauw DJ. The role of the central nervous system in the generation and maintenance of chronic pain in rheumatoid arthritis, osteoarthritis and fibromyalgia. Arthritis Res Ther 2011 Apr 28;13(2):211.
81. Wendler J, Hummel T, Reissinger M, Manger B, Pauli E, Kalden JR, et al. Patients with rheumatoid arthritis adapt differently to repetitive painful stimuli compared to healthy controls. J Clin Neurosci 2001 May;8(3):272-277.
82. Schweinhardt P, Kalk N, Wartolowska K, Chessell I, Wordsworth P, Tracey I. Investigation into the neural correlates of emotional augmentation of clinical pain. Neuroimage 2008 Apr 1;40(2):759-766.
83. Ogawa S, Lee TM, Kay AR, Tank DW. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci U S A 1990 Dec;87(24):9868-9872.
84. Diamond B, Tracey KJ. Mapping the immunological homunculus. Proc Natl Acad Sci U S A 2011 Mar 1;108(9):3461-3462.
85. Norheim KB, Harboe E, Goransson LG, Omdal R. Interleukin-1 inhibition and fatigue in primary Sjogren's syndrome--a double blind, randomised clinical trial. PLoS One 2012;7(1):e30123.
86. Detrait ER, Danis B, Lamberty Y, Foerch P. Peripheral administration of an anti-TNFalpha receptor fusion protein counteracts the amyloid induced elevation of hippocampal TNF-alpha levels and memory deficits in mice. Neurochem Int 2014 Jun;72:10-13.
87. Cheng X, Shen Y, Li R. Targeting TNF: a therapeutic strategy for Alzheimer's disease. Drug Discov Today 2014 Jul 4.
88. Akasbi M, Berenguer J, Saiz A, Brito-Zeron P, Perez-De-Lis M, Bove A, et al. White matter abnormalities in primary Sjogren syndrome. QJM 2012 May;105(5):433-443.
89. Lauvsnes MB, Beyer MK, Appenzeller S, Greve OJ, Harboe E, Goransson LG, et al. Loss of cerebral white matter in primary Sjogren's syndrome: a controlled volumetric magnetic resonance imaging study. Eur J Neurol 2014 Jun 19.
90. Axford JS, Howe FA, Heron C, Griffiths JR. Sensitivity of quantitative (1)H magnetic resonance spectroscopy of the brain in detecting early neuronal damage in systemic lupus erythematosus. Ann Rheum Dis 2001 Feb;60(2):106-111.
91. Zivadinov R, Shucard JL, Hussein S, Durfee J, Cox JL, Bergsland N, et al. Multimodal imaging in systemic lupus erythematosus patients with diffuse neuropsychiatric involvement. Lupus 2013 Jun;22(7):675-683.
92. Hamed SA, Selim ZI, Elattar AM, Elserogy YM, Ahmed EA, Mohamed HO. Assessment of biocorrelates for brain involvement in female patients with rheumatoid arthritis. Clin Rheumatol 2012 Jan;31(1):123-132.
93. Steens SC, Steup-Beekman GM, Bosma GP, Admiraal-Behloul F, Olofsen H, Doornbos J, et al. The effect of corticosteroid medication on quantitative MR parameters of the brain. AJNR Am J Neuroradiol 2005 Nov-Dec;26(10):2475-2480.
94. Emmer BJ, van der Bijl AE, Huizinga TW, Breedveld FC, Steens SC, Th Bosma GP, et al. Brain involvement in rheumatoid arthritis: a magnetic resonance spectroscopy study. Arthritis Rheum 2009 Nov;60(11):3190-3195.
95. King KS, Peshock RM, Rossetti HC, McColl RW, Ayers CR, Hulsey KM, et al. Effect of normal aging versus hypertension, abnormal body mass index, and diabetes mellitus on white matter hyperintensity volume. Stroke 2014 Jan;45(1):255-257.
96. Bekkelund SI, Pierre-Jerome C, Husby G, Mellgren SI. Quantitative cerebral MR in rheumatoid arthritis. AJNR Am J Neuroradiol 1995 Apr;16(4):767-772.
97. Wartolowska K, Hough MG, Jenkinson M, Andersson J, Wordsworth BP, Tracey I. Structural changes of the brain in rheumatoid arthritis. Arthritis Rheum 2012 Feb;64(2):371-379.
98. Barrick TR, Charlton RA, Clark CA, Markus HS. White matter structural decline in normal ageing: a prospective longitudinal study using tract-based spatial statistics. Neuroimage 2010 Jun;51(2):565-577.
99. Fayed N, Garcia-Campayo J, Magallon R, Andres-Bergareche H, Luciano JV, Andres E, et al. Localized 1H-NMR spectroscopy in patients with fibromyalgia: a controlled study of changes in cerebral glutamate/glutamine, inositol, choline, and N-acetylaspartate. Arthritis Res Ther 2010;12(4):R134.
100. Gussew A, Rzanny R, Erdtel M, Scholle HC, Kaiser WA, Mentzel HJ, et al. Timeresolved functional 1H MR spectroscopic detection of glutamate concentration changes in the brain during acute heat pain stimulation. Neuroimage 2010 Jan 15;49(2):1895-1902