2019 European League Against Rheumatism/American College of Rheumatology Classification Criteria for Systemic Lupus Erythematosus

doi:10.1002/art.40930

. 2019 Sep;71(9):1400-1412.

doi: 10.1002/art.40930. Epub 2019 Aug 6.

2019 European League Against Rheumatism/American College of Rheumatology Classification Criteria for Systemic Lupus Erythematosus

Martin Aringer¹, Karen Costenbader², David Daikh³, Ralph Brinks⁴, Marta Mosca⁵, Rosalind Ramsey-Goldman⁶, Josef S Smolen⁷, David Wofsy⁸, Dimitrios T Boumpas⁹, Diane L Kamen¹⁰, David Jayne¹¹, Ricard Cervera¹², Nathalie Costedoat-Chalumeau¹³, Betty Diamond¹⁴, Dafna D Gladman¹⁵, Bevra Hahn¹⁶, Falk Hiepe¹⁷, Søren Jacobsen¹⁸, Dinesh Khanna¹⁹, Kirsten Lerstrøm²⁰, Elena Massarotti², Joseph McCune¹⁹, Guillermo Ruiz-Irastorza²¹, Jorge Sanchez-Guerrero²², Matthias Schneider²³, Murray Urowitz²⁴, George Bertsias²⁵, Bimba F Hoyer²⁶, Nicolai Leuchten¹, Chiara Tani²⁷, Sara K Tedeschi², Zahi Touma¹⁵, Gabriela Schmajuk³, Branimir Anic²⁸, Florence Assan²⁹, Tak Mao Chan³⁰, Ann Elaine Clarke³¹, Mary K Crow³², László Czirják³³, Andrea Doria³⁴, Winfried Graninger³⁵, Bernadett Halda-Kiss³³, Sarfaraz Hasni³⁶, Peter M Izmirly³⁷, Michelle Jung³¹, Gábor Kumánovics³³, Xavier Mariette³⁸, Ivan Padjen²⁸, José M Pego-Reigosa³⁹, Juanita Romero-Diaz⁴⁰, Íñigo Rúa-Figueroa Fernández⁴¹, Raphaèle Seror²⁹, Georg H Stummvoll⁷, Yoshiya Tanaka⁴², Maria G Tektonidou⁴³, Carlos Vasconcelos⁴⁴, Edward M Vital⁴⁵, Daniel J Wallace⁴⁶, Sule Yavuz⁴⁷, Pier Luigi Meroni⁴⁸, Marvin J Fritzler³¹, Ray Naden⁴⁹, Thomas Dörner¹⁷, Sindhu R Johnson⁵⁰

Affiliations

¹ University Medical Center and Faculty of Medicine Carl Gustav Carus, TU Dresden, Dresden, Germany.
² Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts.
³ VA Medical Center and University of California, San Francisco.
⁴ Heinrich Heine University Dusseldorf, Dusseldorf, Germany.
⁵ University of Pisa, Pisa, Italy.
⁶ Northwestern University Feinberg School of Medicine, Chicago, Illinois.
⁷ Medical University of Vienna, Vienna, Austria.
⁸ University of California, San Francisco.
⁹ National and Kapodestrian University of Athens Medical School and Biomedical Research Foundation of the Academy of Athens, Athens, Greece, and University of Cyprus Medical School, Nicosia, Cyprus.
¹⁰ Medical University of South Carolina, Charleston.
¹¹ University of Cambridge, Cambridge, UK.
¹² Hospital Clínic, University of Barcelona, Barcelona, Spain.
¹³ Cochin Hospital, Center de référence maladies auto-immunes et systémiques rares d'île de France, Paris, France.
¹⁴ The Feinstein Institute for Medical Research, Manhasset, New York.
¹⁵ Toronto Western Hospital, University of Toronto, Toronto, Ontario, Canada.
¹⁶ University of California, Los Angeles.
¹⁷ Charité-Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin Institute of Health, Berlin, Germany.
¹⁸ Copenhagen Lupus and Vasculitis Clinic, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.
¹⁹ University of Michigan, Ann Arbor.
²⁰ Lupus Europe, Essex, UK.
²¹ Hospital Universitario Cruces, UPV/EHU, Barakaldo, Spain.
²² Mount Sinai Hospital/University Health Network, University of Toronto, Toronto, Ontario, Canada, and Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico.
²³ Heinrich-Heine-University, Duesseldorf, Germany.
²⁴ Toronto Western Hospital, University of Toronto, Lupus Clinic, Toronto, Ontario, Canada.
²⁵ University of Crete Medical School, Heraklion, Crete, Greece.
²⁶ Charité - Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin Institute of Health, Berlin, Germany, and University of Schleswig-Holstein at Kiel, Kiel, Germany.
²⁷ Azienda Ospedaliero Universitaria Pisana, University of Pisa, Pisa, Italy.
²⁸ University of Zagreb School of Medicine and University Hospital Center Zagreb, Zagreb, Croatia.
²⁹ Université Paris Sud, Hôpitaux Universitaires Paris-Sud, AP-HP, INSERM 1184, Le Kremlin-Bicêtre, France.
³⁰ University of Hong Kong, Hong Kong, China.
³¹ Cumming School of Medicine, University of Calgary, Calgary, Alberta, Canada.
³² Hospital for Special Surgery, New York, New York.
³³ University of Pécs, Pécs, Hungary.
³⁴ University of Padova, Padova, Italy.
³⁵ Medical University of Graz, Graz, Austria.
³⁶ National Institute of Arthritis and Musculoskeletal and Skin Diseases, NIH, Bethesda, Maryland.
³⁷ New York University School of Medicine, New York, New York.
³⁸ AP-HP, Hôpitaux universitaires Paris-Sud - Hôpital Bicêtre, and Université Paris-Sud, INSERM UMR 1184, Université Paris-Saclay, Le Kremlin Bicêtre, France.
³⁹ University Hospital of Vigo, IRIDIS Group, Instituto de Investigación Sanitaria Galicia Sur (IISGS), Vigo, Spain.
⁴⁰ Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico.
⁴¹ Doctor Negrín University Hospital, Las Palmas de Gran Canaria, Las Palmas, Spain.
⁴² University of Occupational and Environmental Health, Japan, Kitakyushu, Japan.
⁴³ National and Kapodistrian University of Athens Medical School, Athens, Greece.
⁴⁴ Centro Hospitalar do Porto, University of Porto, Porto, Portugal.
⁴⁵ University of Leeds, NIHR Leeds Biomedical Research Center, Leeds Teaching Hospitals NHS Trust, Leeds, UK.
⁴⁶ Cedars-Sinai Medical Center, Los Angeles, California.
⁴⁷ Istanbul Bilim University, Istanbul, Turkey.
⁴⁸ IRCCS Istituto Auxologico Italiano, Milan, Italy.
⁴⁹ McMaster University, Hamilton, Ontario, Canada.
⁵⁰ Toronto Western Hospital, University Health Network, Mount Sinai Hospital, University of Toronto, Toronto, Ontario, Canada.

PMID: 31385462
PMCID: PMC6827566
DOI: 10.1002/art.40930

2019 European League Against Rheumatism/American College of Rheumatology Classification Criteria for Systemic Lupus Erythematosus

Martin Aringer et al. Arthritis Rheumatol. 2019 Sep.

. 2019 Sep;71(9):1400-1412.

doi: 10.1002/art.40930. Epub 2019 Aug 6.

Authors

Affiliations

¹ University Medical Center and Faculty of Medicine Carl Gustav Carus, TU Dresden, Dresden, Germany.
² Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts.
³ VA Medical Center and University of California, San Francisco.
⁴ Heinrich Heine University Dusseldorf, Dusseldorf, Germany.
⁵ University of Pisa, Pisa, Italy.
⁶ Northwestern University Feinberg School of Medicine, Chicago, Illinois.
⁷ Medical University of Vienna, Vienna, Austria.
⁸ University of California, San Francisco.
⁹ National and Kapodestrian University of Athens Medical School and Biomedical Research Foundation of the Academy of Athens, Athens, Greece, and University of Cyprus Medical School, Nicosia, Cyprus.
¹⁰ Medical University of South Carolina, Charleston.
¹¹ University of Cambridge, Cambridge, UK.
¹² Hospital Clínic, University of Barcelona, Barcelona, Spain.
¹³ Cochin Hospital, Center de référence maladies auto-immunes et systémiques rares d'île de France, Paris, France.
¹⁴ The Feinstein Institute for Medical Research, Manhasset, New York.
¹⁵ Toronto Western Hospital, University of Toronto, Toronto, Ontario, Canada.
¹⁶ University of California, Los Angeles.
¹⁷ Charité-Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin Institute of Health, Berlin, Germany.
¹⁸ Copenhagen Lupus and Vasculitis Clinic, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.
¹⁹ University of Michigan, Ann Arbor.
²⁰ Lupus Europe, Essex, UK.
²¹ Hospital Universitario Cruces, UPV/EHU, Barakaldo, Spain.
²² Mount Sinai Hospital/University Health Network, University of Toronto, Toronto, Ontario, Canada, and Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico.
²³ Heinrich-Heine-University, Duesseldorf, Germany.
²⁴ Toronto Western Hospital, University of Toronto, Lupus Clinic, Toronto, Ontario, Canada.
²⁵ University of Crete Medical School, Heraklion, Crete, Greece.
²⁶ Charité - Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, Berlin Institute of Health, Berlin, Germany, and University of Schleswig-Holstein at Kiel, Kiel, Germany.
²⁷ Azienda Ospedaliero Universitaria Pisana, University of Pisa, Pisa, Italy.
²⁸ University of Zagreb School of Medicine and University Hospital Center Zagreb, Zagreb, Croatia.
²⁹ Université Paris Sud, Hôpitaux Universitaires Paris-Sud, AP-HP, INSERM 1184, Le Kremlin-Bicêtre, France.
³⁰ University of Hong Kong, Hong Kong, China.
³¹ Cumming School of Medicine, University of Calgary, Calgary, Alberta, Canada.
³² Hospital for Special Surgery, New York, New York.
³³ University of Pécs, Pécs, Hungary.
³⁴ University of Padova, Padova, Italy.
³⁵ Medical University of Graz, Graz, Austria.
³⁶ National Institute of Arthritis and Musculoskeletal and Skin Diseases, NIH, Bethesda, Maryland.
³⁷ New York University School of Medicine, New York, New York.
³⁸ AP-HP, Hôpitaux universitaires Paris-Sud - Hôpital Bicêtre, and Université Paris-Sud, INSERM UMR 1184, Université Paris-Saclay, Le Kremlin Bicêtre, France.
³⁹ University Hospital of Vigo, IRIDIS Group, Instituto de Investigación Sanitaria Galicia Sur (IISGS), Vigo, Spain.
⁴⁰ Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico.
⁴¹ Doctor Negrín University Hospital, Las Palmas de Gran Canaria, Las Palmas, Spain.
⁴² University of Occupational and Environmental Health, Japan, Kitakyushu, Japan.
⁴³ National and Kapodistrian University of Athens Medical School, Athens, Greece.
⁴⁴ Centro Hospitalar do Porto, University of Porto, Porto, Portugal.
⁴⁵ University of Leeds, NIHR Leeds Biomedical Research Center, Leeds Teaching Hospitals NHS Trust, Leeds, UK.
⁴⁶ Cedars-Sinai Medical Center, Los Angeles, California.
⁴⁷ Istanbul Bilim University, Istanbul, Turkey.
⁴⁸ IRCCS Istituto Auxologico Italiano, Milan, Italy.
⁴⁹ McMaster University, Hamilton, Ontario, Canada.
⁵⁰ Toronto Western Hospital, University Health Network, Mount Sinai Hospital, University of Toronto, Toronto, Ontario, Canada.

PMID: 31385462
PMCID: PMC6827566
DOI: 10.1002/art.40930

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 1,001 subjects and validation compared with previous criteria in a new validation cohort of 1,270 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 7 clinical (constitutional, hematologic, neuropsychiatric, mucocutaneous, serosal, musculoskeletal, renal) and 3 immunologic (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 reflects current thinking about SLE and provides an improved foundation for SLE research.

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Figures

**Figure 1.**
Development and validation of SLE classification criteria

**Figure 2.**
Classification criteria for systemic lupus erythematosus Note: * In an assay with ≥ 90% specificity against relevant disease controls § Additional criteria items within the same domain will not be counted.

See this image and copyright information in PMC

Comment in

European League against Rheumatism/American College of Rheumatology classification criteria for systemic lupus erythematosus: the laboratory immunologist's point of view.
Infantino M, Manfredi M, Bizzaro N; Study Group on Autoimmune Diseases of the Italian Society of Clinical Pathology and Laboratory Medicine. Infantino M, et al. Ann Rheum Dis. 2021 Dec;80(12):e188. doi: 10.1136/annrheumdis-2019-216591. Epub 2019 Nov 22. Ann Rheum Dis. 2021. PMID: 31757781 No abstract available.
Does Leukopenia Influence Performance of the New European League Against Rheumatism/American College of Rheumatology Classification Criteria in an African-Descendent Population With Childhood-Onset Systemic Lupus Erythematosus? Comment on the Article by Aringer et al.
Fonseca AR, Rodrigues MCF, Sztajnbok F, Land MGP, de Oliveira SKF. Fonseca AR, et al. Arthritis Rheumatol. 2020 Apr;72(4):694-695. doi: 10.1002/art.41178. Epub 2020 Feb 11. Arthritis Rheumatol. 2020. PMID: 31769215 No abstract available.
Reply.
Aringer M, Costenbader KH, Dörner T, Johnson SR. Aringer M, et al. Arthritis Rheumatol. 2020 Apr;72(4):695-696. doi: 10.1002/art.41177. Epub 2020 Feb 11. Arthritis Rheumatol. 2020. PMID: 31769217 No abstract available.
Response to: 'European League against Rheumatism/American College of Rheumatology classification criteria for systemic lupus erythematosus: the laboratory immunologist's point of view' by Infantino et al.
Aringer M, Costenbader KH, Dörner T, Johnson SR. Aringer M, et al. Ann Rheum Dis. 2021 Dec;80(12):e189. doi: 10.1136/annrheumdis-2019-216700. Epub 2019 Dec 12. Ann Rheum Dis. 2021. PMID: 31831507 No abstract available.
Reply.
Aringer M, Costenbader KH, Dörner T, Johnson SR. Aringer M, et al. Arthritis Rheumatol. 2020 May;72(5):860-861. doi: 10.1002/art.41226. Epub 2020 Mar 17. Arthritis Rheumatol. 2020. PMID: 32067359 No abstract available.
Cell-Bound Complement Activation Products Are Superior to Serum Complement C3 and C4 Levels to Detect Complement Activation in Systemic Lupus Erythematosus: Comment on the Article by Aringer et al.
Weinstein A. Weinstein A. Arthritis Rheumatol. 2020 May;72(5):860. doi: 10.1002/art.41227. Epub 2020 Mar 18. Arthritis Rheumatol. 2020. PMID: 32067409 No abstract available.
Exclusion of Cutaneous Lupus Erythematosus Subtypes From the 2019 European League Against Rheumatism/American College of Rheumatology Classifi cation Criteria for Systemic Lupus Erythematosus: Comment on the Article by Aringer et al.
Zapata L Jr, Chong BF. Zapata L Jr, et al. Arthritis Rheumatol. 2020 Aug;72(8):1403. doi: 10.1002/art.41296. Epub 2020 Jun 9. Arthritis Rheumatol. 2020. PMID: 32336046 No abstract available.
Reply.
Aringer M, Costenbader KH, Dörner T, Johnson SR. Aringer M, et al. Arthritis Rheumatol. 2020 Aug;72(8):1404. doi: 10.1002/art.41295. Epub 2020 Jun 5. Arthritis Rheumatol. 2020. PMID: 32336049 No abstract available.

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References

1. Bertsias GK, Pamfil C, Fanouriakis A, Boumpas DT. Diagnostic criteria for systemic lupus erythematosus: has the time come? Nat Rev Rheumatol 2013; 9: 687–94. - PubMed
1. Rahman A, Isenberg DA. Systemic lupus erythematosus. N Engl J Med 2008; 358: 929–39. - PubMed
1. Tsokos GC. Systemic lupus erythematosus. N Engl J Med 2011; 365: 2110–21. - PubMed
1. Johnson SR, Goek ON, Singh-Grewal D, Vlad SC, Feldman BM, Felson DT et al. Classification criteria in rheumatic diseases: a review of methodologic properties. Arthritis Rheum 2007; 57: 1119–33. - PubMed
1. Aggarwal R, Ringold S, Khanna D, Neogi T, Johnson SR, Miller A et al. Distinctions between diagnostic and classification criteria? Arthritis Care Res (Hoboken ) 2015; 67: 891–7. - PMC - PubMed

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[1] Bertsias GK, Pamfil C, Fanouriakis A, Boumpas DT. Diagnostic criteria for systemic lupus erythematosus: has the time come? Nat Rev Rheumatol 2013; 9: 687–94. - PubMed

[2] Bertsias GK, Pamfil C, Fanouriakis A, Boumpas DT. Diagnostic criteria for systemic lupus erythematosus: has the time come? Nat Rev Rheumatol 2013; 9: 687–94. - PubMed

[3] Rahman A, Isenberg DA. Systemic lupus erythematosus. N Engl J Med 2008; 358: 929–39. - PubMed

[4] Rahman A, Isenberg DA. Systemic lupus erythematosus. N Engl J Med 2008; 358: 929–39. - PubMed

[5] Tsokos GC. Systemic lupus erythematosus. N Engl J Med 2011; 365: 2110–21. - PubMed

[6] Tsokos GC. Systemic lupus erythematosus. N Engl J Med 2011; 365: 2110–21. - PubMed

[7] Johnson SR, Goek ON, Singh-Grewal D, Vlad SC, Feldman BM, Felson DT et al. Classification criteria in rheumatic diseases: a review of methodologic properties. Arthritis Rheum 2007; 57: 1119–33. - PubMed

[8] Johnson SR, Goek ON, Singh-Grewal D, Vlad SC, Feldman BM, Felson DT et al. Classification criteria in rheumatic diseases: a review of methodologic properties. Arthritis Rheum 2007; 57: 1119–33. - PubMed

[9] Aggarwal R, Ringold S, Khanna D, Neogi T, Johnson SR, Miller A et al. Distinctions between diagnostic and classification criteria? Arthritis Care Res (Hoboken ) 2015; 67: 891–7. - PMC - PubMed

[10] Aggarwal R, Ringold S, Khanna D, Neogi T, Johnson SR, Miller A et al. Distinctions between diagnostic and classification criteria? Arthritis Care Res (Hoboken ) 2015; 67: 891–7. - PMC - PubMed

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2019 European League Against Rheumatism/American College of Rheumatology Classification Criteria for Systemic Lupus Erythematosus

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2019 European League Against Rheumatism/American College of Rheumatology Classification Criteria for Systemic Lupus Erythematosus

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