2019 European League Against Rheumatism/American College of Rheumatology classification criteria for systemic lupus erythematosus

Martin Aringer; Karen Costenbader; David Daikh; Ralph Brinks; Marta Mosca; Rosalind Ramsey-Goldman; Josef S Smolen; David Wofsy; Dimitrios T Boumpas; Diane L Kamen; David Jayne; Ricard Cervera; Nathalie Costedoat-Chalumeau; Betty Diamond; Dafna D Gladman; Bevra Hahn; Falk Hiepe; Søren Jacobsen; Dinesh Khanna; Kirsten Lerstrøm; Elena Massarotti; Joseph McCune; Guillermo Ruiz-Irastorza; Jorge Sanchez-Guerrero; Matthias Schneider; Murray Urowitz; George Bertsias; Bimba F Hoyer; Nicolai Leuchten; Chiara Tani; Sara K Tedeschi; Zahi Touma; Gabriela Schmajuk; Branimir Anic; Florence Assan; Tak Mao Chan; Ann Elaine Clarke; Mary K Crow; László Czirják; Andrea Doria; Winfried Graninger; Bernadett Halda-Kiss; Sarfaraz Hasni; Peter M Izmirly; Michelle Jung; Gábor Kumánovics; Xavier Mariette; Ivan Padjen; José M Pego-Reigosa; Juanita Romero-Diaz; Íñigo Rúa-Figueroa Fernández; Raphaèle Seror; Georg H Stummvoll; Yoshiya Tanaka; Maria G Tektonidou; Carlos Vasconcelos; Edward M Vital; Daniel J Wallace; Sule Yavuz; Pier Luigi Meroni; Marvin J Fritzler; Ray Naden; Thomas Dörner; Sindhu R Johnson

doi:10.1136/annrheumdis-2018-214819

2019 European League Against Rheumatism/American College of Rheumatology classification criteria for systemic lupus erythematosus

Ann Rheum Dis. 2019 Sep;78(9):1151-1159. doi: 10.1136/annrheumdis-2018-214819. Epub 2019 Aug 5.

Authors

Martin Aringer¹, Karen Costenbader², David Daikh³, Ralph Brinks⁴, Marta Mosca⁵, Rosalind Ramsey-Goldman⁶, Josef S Smolen⁷, David Wofsy⁸, Dimitrios T Boumpas^{9

10}, Diane L Kamen¹¹, David Jayne¹², Ricard Cervera¹³, Nathalie Costedoat-Chalumeau¹⁴, Betty Diamond¹⁵, Dafna D Gladman¹⁶, Bevra Hahn¹⁷, Falk Hiepe¹⁸, Søren Jacobsen¹⁹, Dinesh Khanna²⁰, Kirsten Lerstrøm²¹, Elena Massarotti^{22

23}, Joseph McCune²⁰, Guillermo Ruiz-Irastorza²⁴, Jorge Sanchez-Guerrero^{25

26}, Matthias Schneider²⁷, Murray Urowitz²⁸, George Bertsias²⁹, Bimba F Hoyer^{18

30}, Nicolai Leuchten³¹, Chiara Tani³², Sara K Tedeschi^{23

33}, Zahi Touma³⁴, Gabriela Schmajuk³, Branimir Anic³⁵, Florence Assan³⁶, Tak Mao Chan³⁷, Ann Elaine Clarke³⁸, Mary K Crow³⁹, László Czirják⁴⁰, Andrea Doria⁴¹, Winfried Graninger⁴², Bernadett Halda-Kiss⁴⁰, Sarfaraz Hasni⁴³, Peter M Izmirly⁴⁴, Michelle Jung³⁸, Gábor Kumánovics⁴⁰, Xavier Mariette^{45

46}, Ivan Padjen³⁵, José M Pego-Reigosa⁴⁷, Juanita Romero-Diaz²⁶, Íñigo Rúa-Figueroa Fernández⁴⁸, Raphaèle Seror³⁶, Georg H Stummvoll⁴⁹, Yoshiya Tanaka⁵⁰, Maria G Tektonidou⁵¹, Carlos Vasconcelos⁵², Edward M Vital^{53

54}, Daniel J Wallace⁵⁵, Sule Yavuz⁵⁶, Pier Luigi Meroni⁵⁷, Marvin J Fritzler⁵⁸, Ray Naden⁵⁹, Thomas Dörner¹⁸, Sindhu R Johnson^{60

61}

Affiliations

¹ Medicine III, University Medical Center and Faculty of Medicine Carl Gustav Carus, TU Dresden, Dresden, Germany [email protected] [email protected].
² Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.
³ University of California at San Francisco and VA Medical Center, San Francisco, California, USA.
⁴ Policlinic and Hiller Research Unit for Rheumatology, Medical Faculty, Heinrich-Heine-University Duesseldorf, Duesseldorf, Germany.
⁵ Department of Clinical and Experimental Medicine, Azienda Ospedaliero Universitaria Pisana, University of Pisa, Pisa, Italy.
⁶ Department of Medicine, Division of Rheumatology, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.
⁷ Department of Rheumatology, Medicine III, Medical University of Vienna, Vienna, Austria.
⁸ Department of Medicine, Russell/Engleman Rheumatology Research Center, University of California at San Francisco, San Francisco, California, USA.
⁹ Joint Academic Rheumatology Program, Medical School, National and Kapodestrian University of Athens, and Biomedical Research Foundation of the Athens Academy, Athens, Greece.
¹⁰ Departments of Internal Medicine and Rheumatology, Clinical Immunology and Allergy, Medical School, University of Cyprus, Nicosia, Cyprus.
¹¹ Department of Medicine, Medical University of South Carolina, Charleston, South Carolina, USA.
¹² Department of Medicine, University of Cambridge, Cambridge, UK.
¹³ Department of Autoimmune Diseases, Hospital Clínic, University of Barcelona, Barcelona, Spain.
¹⁴ Medicine, Toronto Western Hospital, University Health Network, Mount Sinai Hospital, University of Toronto, Toronto Scleroderma Research Program, Toronto, Ontario, Canada.
¹⁵ Center for Autoimmune, Musculoskeletal and Hematopoietic Diseases, The Feinstein Institute for Medical Research, Manhasset, New York, USA.
¹⁶ Division of Rheumatology, Department of Medicine, Toronto Western Hospital, University of Toronto, Toronto, Ontario, Canada.
¹⁷ Division of Rheumatology, David Geffen School of Medicine, University of California at Los Angeles, Los Angeles, California, USA.
¹⁸ Department of Rheumatology and Clinical Immunology, Charité - Universitätsmedizin Berlin, Corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.
¹⁹ Copenhagen Lupus and Vasculitis Clinic, Center for Rheumatology and Spine Diseases, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.
²⁰ Division of Rheumatology, University of Michigan, Ann Arbor, Michigan, USA.
²¹ Lupus Europe, Co-Opted Trustee for Research, Essex, UK.
²² Medicine, Brigham and Women's Hospital, Boston, Massachusetts, USA.
²³ Department of Medicine, Harvard Medical School, Boston, Massachusetts, USA.
²⁴ Autoimmune Diseases Research Unit, Department of Internal Medicine, Biocruces Bizkaia Health Research Institute, Hospital Universitario Cruces, UPV/EHU, Bizkaia, The Basque Country, Spain.
²⁵ Division of Rheumatology, Department of Medicine, Mount Sinai Hospital/University Health Network, University of Toronto, Toronto, Ontario, Canada.
²⁶ Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico.
²⁷ Policlinic and Hiller Research Unit for Rheumatology, Medical Faculty, Heinrich-Heine-University, Duesseldorf, Germany.
²⁸ Center for Prognosis Studies in the Rheumatic Diseases, Toronto Western Hospital, University of Toronto, Lupus Clinic, Toronto, Ontario, Canada.
²⁹ Rheumatology, Clinical Immunology and Allergy, University of Crete Medical School, Heraklion, Crete, Greece.
³⁰ Department of Medicine III, University of Schleswig-Holstein at Kiel, Kiel, Germany.
³¹ Medicine III, University Medical Center and Faculty of Medicine Carl Gustav Carus, TU Dresden, Dresden, Germany.
³² Department of Clinical and Experimental Medicine, Rheumatology Unit, Azienda Ospedaliero Universitaria Pisana, University of Pisa, Pisa, Italy.
³³ Department of Medicine, Brigham and Women's Hospital, Boston, Massachusetts, USA.
³⁴ Division of Rheumatology, Department of Medicine, Toronto Western Hospital, Institute of Health Policy, Management and Evaluation, University of Toronto, Toronto, Ontario, Canada.
³⁵ Division of Clinical Immunology and Rheumatology, University of Zagreb School of Medicine and University Hospital Centre Zagreb, Zagreb, Croatia.
³⁶ Department of Rheumatology, Université Paris Sud, Hôpitaux Universitaires Paris-Sud, AP-HP, INSERM UMR 1184, Le Kremlin-Bicêtre, France.
³⁷ Department of Medicine, University of Hong Kong, Hong Kong, China.
³⁸ Division of Rheumatology, Cumming School of Medicine, University of Calgary, Calgary, Alberta, Canada.
³⁹ Hospital for Special Surgery, Ney York, New York, USA.
⁴⁰ Department of Rheumatology and Immunology, University of Pécs, Pécs, Hungary.
⁴¹ Rheumatology Unit, Department of Medicine (DIMED), University of Padova, Padova, Italy.
⁴² Internal Medicine, Medical University of Graz, Graz, Austria.
⁴³ Lupus Clinical Research Program, Office of the Clinical Director, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, Maryland, USA.
⁴⁴ Rheumatology, New York University School of Medicine, New York, New York, USA.
⁴⁵ Rheumatology, Assistance Publique-Hôpitaux de Paris (AP-HP), Hôpitaux universitaires Paris-Sud - Hôpital Bicêtre, Le Kremlin Bicêtre, France.
⁴⁶ Department of Rheumatology, Université Paris-Sud, Center for Immunology of Viral Infections and Auto-immune Diseases (IMVA), Institut pour la Santé et la Recherche Médicale (INSERM) UMR 1184, Université Paris-Saclay, Le Kremlin Bicêtre, France.
⁴⁷ Department of Rheumatology, University Hospital of Vigo, IRIDIS Group, Instituto de Investigación Sanitaria Galicia Sur (IISGS), Vigo, Spain.
⁴⁸ Rheumatology, Doctor Negrín University Hospital, Las Palmas de Gran Canaria, Las Palmas, Spain.
⁴⁹ Rheumatology, Medical University of Vienna, Vienna, Austria.
⁵⁰ First Department of Internal Medicine, University of Occupational and Environmental Health, Japan, Kitakyushu, Japan.
⁵¹ Medical School, National and Kapodistrian University of Athens, Athens, Greece.
⁵² Clinical Immunology Unit, Centro Hospitalar do Porto, ICBAS, University of Porto, Porto, Portugal.
⁵³ Leeds Institute of Rheumatic and Musculoskeletal Medicine, University of Leeds, Leeds, UK.
⁵⁴ NIHR Leeds Biomedical Research Centre, Leeds Teaching Hospitals NHS Trust, Leeds, UK.
⁵⁵ Division of Rheumatology, Cedars-Sinai Medical Center, Los Angeles, California, USA.
⁵⁶ Department of Rheumatology, Istanbul Bilim University, Istanbul, Turkey.
⁵⁷ Clinical Immunology and Rheumatology Unit, IRCCS Istituto Auxologico Italiano, Milan, Italy.
⁵⁸ Faculty of Medicine, Cumming School of Medicine, University of Calgary, Calgary, Alberta, Canada.
⁵⁹ Maternal-Fetal Medicine, McMaster University Faculty of Health Sciences, Hamilton, Ontario, Canada.
⁶⁰ Internal Medicine Department, Centre de référence maladies auto-immunes et systémiques rares d'île deFrance, Cochin Hospital, Université Paris Descartes-Sorbonne Paris Cité, INSERM U1153, Center for Epidemiology and Statistics Sorbonne Paris Cité (CRESS), Paris, France [email protected] [email protected].
⁶¹ Institute of Health Policy, Management and Evaluation, University of Toronto, Toronto, Ontario, Canada.

PMID: 31383717
DOI: 10.1136/annrheumdis-2018-214819

Abstract

Objective: To develop new classification criteria for systemic lupus erythematosus (SLE) jointly supported by the European League Against Rheumatism (EULAR) and the American College of Rheumatology (ACR).

Methods: This international initiative had four phases. (1) Evaluation of antinuclear antibody (ANA) as an entry criterion through systematic review and meta-regression of the literature and criteria generation through an international Delphi exercise, an early patient cohort and a patient survey. (2) Criteria reduction by Delphi and nominal group technique exercises. (3) Criteria definition and weighting based on criterion performance and on results of a multi-criteria decision analysis. (4) Refinement of weights and threshold scores in a new derivation cohort of 1001 subjects and validation compared with previous criteria in a new validation cohort of 1270 subjects.

Results: The 2019 EULAR/ACR classification criteria for SLE include positive ANA at least once as obligatory entry criterion; followed by additive weighted criteria grouped in seven clinical (constitutional, haematological, neuropsychiatric, mucocutaneous, serosal, musculoskeletal, renal) and three immunological (antiphospholipid antibodies, complement proteins, SLE-specific antibodies) domains, and weighted from 2 to 10. Patients accumulating ≥10 points are classified. In the validation cohort, the new criteria had a sensitivity of 96.1% and specificity of 93.4%, compared with 82.8% sensitivity and 93.4% specificity of the ACR 1997 and 96.7% sensitivity and 83.7% specificity of the Systemic Lupus International Collaborating Clinics 2012 criteria.

Conclusion: These new classification criteria were developed using rigorous methodology with multidisciplinary and international input, and have excellent sensitivity and specificity. Use of ANA entry criterion, hierarchically clustered and weighted criteria reflect current thinking about SLE and provide an improved foundation for SLE research.

Keywords: classification criteria; consensus methods; lupus; multi-criteria decision analysis; systemic lupus erythematosus; validation.

Publication types

Research Support, Non-U.S. Gov't
Review

MeSH terms

Humans
Lupus Erythematosus, Systemic / classification*
Rheumatic Diseases*
Rheumatology*
Societies, Medical*

Abstract

Publication types

MeSH terms

Grants and funding