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Nitrated nucleosome levels and neuropsychiatric events in systemic lupus erythematosus; a multi-center retrospective case-control study

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Ferreira I1, Croca S1, Raimondo MG1, Matharu M2, Miller S2, Giles I1, Isenberg D1,3, Ioannou Y1,3, Hanly JG4, Urowitz MB5, Anderson N5, Aranow C6, Askanase A7, Bae SC8, Bernatsky S9, Bruce IN10, Buyon J11, Clarke AE12, Dooley MA13, Fortin P14, Ginzler E15, Gladman D5, Gordon C16, Inanc M17, Jacobsen S18, Kalunian K19, Kamen D20, Khamashta M21, Lim S22, Manzi S23, Merrill J24, Nived O25, Peschken C26, Petri M27, Ramsey-Goldman R28, Ruiz-Irastorza G29, Sanchez-Guerrero J30, Steinson K31, Sturfelt GK25, van Vollenhoven R32, Wallace DJ33, Zoma A34, Rahman A35. Arthritis Res Ther. 2017 Dec 22;19(1):287. doi: 10.1186/s13075-017-1495-6.


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1 Centre for Rheumatology Research, University College London, Fourth Floor Rayne Institute, 5 University Street, London, WC1E 6JF, UK.

2 Headache Group, Institute of Neurology and The National Hospital for Neurology and Neurosurgery, Queen Square, London, UK.

3 Arthritis Research UK Centre for Adolescent Rheumatology, UCL/UCLH/Great Ormond Street Hospital, London, UK.

4 Division of Rheumatology, Dalhousie University and Queen Elizabeth II Health Sciences Center, Halifax, NS, Canada.

5 Lupus Program, Centre for Prognosis Studies in The Rheumatic Disease and Krembil Research Institute, Toronto Western Hospital, University of Toronto, Toronto, ON, Canada.

6 Feinstein Institute for Medical Research, Manhasset, NY, USA.

7 Rheumatology, Columbia University, New York, NY, USA.

8 Department of Rheumatology, Hanyang University Hospital for Rheumatic Diseases, Seoul, South Korea.

9 Divisions of Clinical Epidemiology and Rheumatology, McGill University Health Centre, Montreal, QC, Canada.

10 Arthritis Research UK Centre for Epidemiology, Centre for Musculoskeletal Research, The University of Manchester, and NIHR Manchester Musculoskeletal Biomedical Research Unit, Central Manchester University Hospitals NHS Foundation Trust, Manchester Academic Health Science Centre, Manchester, UK.

11 New York School of Medicine, New York, NY, USA.

12 Division of Rheumatology, Cumming School of Medicine, University of Calgary, Calgary, AB, Canada.

13 Thurston Arthritis Research Center, University of North Carolina, Chapel Hill, NC, USA.

14 Centre Hospitalier de l'Université Laval (CHUL), Québec, QC, Canada.

15 Downstate Medical Center Rheumatology, Brooklyn, New York, NY, USA.

16 Rheumatology Research Group, Institute of Inflammation and Ageing, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK.

17 Department of Internal Medicine, Istanbul University, Istanbul, Turkey.

18 Copenhagen Lupus and Vasculitis Clinic, Centre For Rheumatology and Spine Diseases, Rigshospitalet, Copenhagen, Denmark.

19 University of California, San Diego, La Jolla, CA, USA.

20 Division of Rheumatology and Immunology, Medical University of South Carolina, Charleston, SC, USA.

21 FRCP Division of Women's Health, King's College, London, UK.

22 Department of Medicine, Emory University, Atlanta, GA, USA.

23 Allegheny Health Network, Pittsburgh, PA, USA.

24 Clinical Pharmacology, Oklahoma Medical Research Foundation, Oklahoma City, OK, USA.

25 Department of Rheumatology, Lund University, Lund, Sweden.

26 Department of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, MB, Canada.

27 Johns Hopkins University School of Medicine, Baltimore, MD, USA.

28 Northwestern University, Feinberg School of Medicine, Chicago, IL, USA.

29 Autoimmune Diseases Research Unit, Department of Internal Medicine, BioCruces Health Research Institute. Hospital Universitario Cruces, University of the Basque Country, Barakaldo, Bizkaia, Spain.

30 Mount Sinai Hospital and University Health Network, University of Toronto, Toronto, ON, Canada.

31 Department of Rheumatology, Landspitali University Hospital, Reykjavik, Iceland.

32 Rheumatology Unit, Department of Medicine, Karolinska University Hospital, Solna, Sweden.

33 Cedars-Sinai Medical Center/David Geffen School of Medicine at UCLA, Los Angeles, CA, USA.

34 Department of Rheumatology Hairmyres Hospital, East Kilbride, Scotland, UK.

35 Centre for Rheumatology Research, University College London, Fourth Floor Rayne Institute, 5 University Street, London, WC1E 6JF, UK. anisur.rahman@ucl.ac.uk.



In patients with systemic lupus erythematosus (SLE) there is no serological test that will reliably distinguish neuropsychiatric (NP) events due to active SLE from those due to other causes. Previously we showed that serum levels of nitrated nucleosomes (NN) were elevated in a small number of patients with NPSLE. Here we measured serum NN in samples from a larger population of patients with SLE and NP events to see whether elevated serum NN could be a marker for NPSLE.


We obtained serum samples from patients in the Systemic Lupus International Collaborative Clinics (SLICC) inception cohort. This included 216 patients with NP events and two matched controls with SLE but no NP events for each of these patients. For the NP patients we tested samples taken before, during and after the NP event.


Twenty-six patients had events attributed to SLE according to the most stringent SLICC attribution rule. In these patients there was no association between onset of event and elevated serum NN. In 190 patients in whom events were not attributed to SLE by the SLICC rules, median serum NN was elevated at the onset of event (P = 0.006). The predominant clinical features in this group of 190 patients were headache, mood disorders and anxiety.


Serum NN levels rise at the time of an NP event in a proportion of patients with SLE. Further studies are needed to determine the value of serum NN as a biomarker for NPSLE.