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Remission and low disease activity are associated with lower healthcare costs: results from the Systemic Lupus International Collaborating Clinics (SLICC) inception cohort
  1. Megan R W Barber1,
  2. Manuel Francisco Ugarte-Gil2,3,
  3. John G Hanly4,5,
  4. Murray B Urowitz6,7,
  5. Yvan St-Pierre8,
  6. Caroline Gordon9,
  7. Sang-Cheol Bae10,11,
  8. Juanita Romero-Diaz12,
  9. Jorge Sanchez-Guerrero13,14,
  10. Sasha Bernatsky8,
  11. Daniel J Wallace15,
  12. David A Isenberg16,
  13. Anisur Rahman16,
  14. Joan T Merrill17,
  15. Paul R Fortin18,
  16. Dafna D Gladman7,19,
  17. Ian N Bruce20,21,
  18. Michelle Petri22,
  19. Ellen M Ginzler23,
  20. Mary Anne Dooley24,
  21. Rosalind Ramsey-Goldman25,
  22. Susan Manzi26,
  23. Andreas Jönsen27,
  24. Ronald F van Vollenhoven28,
  25. Cynthia Aranow29,
  26. Meggan Mackay30,
  27. Guillermo Ruiz-Irastorza31,
  28. S Sam Lim32,
  29. Murat Inanc33,
  30. Kenneth C Kalunian34,
  31. Søren Jacobsen35,
  32. Christine A Peschken36,
  33. Diane L Kamen37,
  34. Anca Askanase38,
  35. Bernardo A Pons-Estel39,
  36. Francesca S Cardwell40,
  37. Graciela S Alarcón41,
  38. Ann E Clarke1
  1. 1Cumming School of Medicine, University of Calgary, Calgary, Alberta, Canada
  2. 2Grupo Peruano de Estudio de Enfermedades Autoinmunes Sistémicas, Universidad Cientifica del Sur, Lima, Peru
  3. 3Rheumatology, Hospital Nacional Guillermo Almenara Irigoyen, EsSalud, Lima, Peru
  4. 4Division of Rheumatology, Department of Medicine and Department of Pathology, Queen Elizabeth II Health Sciences Centre, Halifax, Nova Scotia, Canada
  5. 5Dalhousie University, Halifax, Nova Scotia, Canada
  6. 6Lupus Program, Centre for Prognosis Studies in the Rheumatic Diseases, University of Toronto, Toronto Western Hospital, Toronto, Ontario, Canada
  7. 7Krembil Research Institute, Toronto, Ontario, Canada
  8. 8Research Institute of the McGill University Health Center, Montreal, Quebec, Canada
  9. 9Rheumatology Research Group, Birmingham University Medical School, Birmingham, UK
  10. 10Rheumatology, Hanyang University Hospital for Rheumatic Diseases, Seoul, Korea (the Republic of)
  11. 11Hanyang Institute of Bioscience and Biotechnology, Seoul, Korea (the Republic of)
  12. 12Immunology and Rheumatology, Instituto Nacional de Ciencias Medicas y Nutricion Salvador Zubiran, Tlalpan, Mexico
  13. 13University Health Network, Toronto, Ontario, Canada
  14. 14Mount Sinai Hospital, Toronto, Ontario, Canada
  15. 15Division of Rheumatology, Cedars-Sinai Medical Center, Los Angeles, California, USA
  16. 16Centre for Rheumatology, Department of Medicine, University College London, London, UK
  17. 17Department of Clinical Pharmacology, Oklahoma Medical Research Foundation, Oklahoma City, Oklahoma, USA
  18. 18Centre ARThrite, CHU de Québec, Université Laval, Quebec City, Quebec, Canada
  19. 19Lupus Program, Centre for Prognosis in The Rheumatic Diseases, University of Toronto, Toronto, Ontario, Canada
  20. 20Centre for Musculoskeletal Research, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK
  21. 21The Kellgren Centre for Rheumatology, Central Manchester University Hospitals NHS Foundation Trust, Manchester, UK
  22. 22Division of Rheumatology, School of Medicine, Johns Hopkins University, Baltimore, Maryland, USA
  23. 23Department of Medicine, SUNY Downstate Medical Center, Brooklyn, New York, USA
  24. 24Thurston Arthritis Research Centre, University of North Carolina, Chapel Hill, North Carolina, USA
  25. 25Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA
  26. 26Lupus Center of Excellence, Allegheny Health Network, Pittsburgh, Pennsylvania, USA
  27. 27Lund University, Clinical Sciences, Lund, Sweden
  28. 28Rheumatology and Immunology Center, University of Amsterdam, Amsterdam, The Netherlands
  29. 29The Feinstein Institute for Medical Research, Manhasset, New York, USA
  30. 30Feinstein Institute for Medical Research, Manhasset, New York, USA
  31. 31Biobizkaia Health Research Institute, Hospital Universitario Cruces, Barakaldo, Spain
  32. 32School of Medicine, Emory University, Atlanta, Georgia, USA
  33. 33Division of Rheumatology, Department of Internal Medicine, Istanbul University, Istanbul Medical Faculty, Capa, Istanbul, Turkey
  34. 34University of California School of Medicine, La Jolla, California, USA
  35. 35Copenhagen Lupus and Vasculitis Clinic, Center for Rheumatology and Spine Diseases, Rigshospitalet, Copenhagen, Denmark
  36. 36University of Manitoba, Winnipeg, Manitoba, Canada
  37. 37Medical University of South Carolina, Charleston, South Carolina, USA
  38. 38Division of Rheumatology, Columbia University Lupus Center, Columbia University College of Physicians & Surgeons, New York, New York, USA
  39. 39Grupo Oroño, Centro Regional de Enfermedades Autonmunes y Reumáticas, Rosario, Argentina
  40. 40Geography & Environmental Management, University of Waterloo, Waterloo, Ontario, Canada
  41. 41Department of Medicine, Division of Clinical Immunology and Rheumatology, School of Medicine, The University of Alabama, Birmingham, Alabama, USA
  1. Correspondence to Dr Ann E Clarke, Division of Rheumatology, University of Calgary, Calgary, AB T2N 4Z6, Canada; aeclarke{at}


Objectives This study aims to determine the independent impact of definitions of remission/low disease activity (LDA) on direct/indirect costs (DCs, ICs) in a multicentre inception cohort.

Methods Patients from 31 centres in 10 countries were enrolled within 15 months of diagnosis and assessed annually. Five mutually exclusive disease activity states (DAS) were defined as (1) remission off-treatment: clinical (c) SLEDAI-2K=0, without prednisone/immunosuppressants; (2) remission on-treatment: cSLEDAI-2K=0, prednisone ≤5 mg/day and/or maintenance immunosuppressants; (3) LDA-Toronto Cohort (TC): cSLEDAI-2K≤2, without prednisone/immunosuppressants; (4) modified lupus LDA state (mLLDAS): SLEDAI-2K≤4, no activity in major organs/systems, no new activity, prednisone ≤7.5 mg/day and/or maintenance immunosuppressants and (5) active: all remaining assessments.

At each assessment, patients were stratified into the most stringent DAS fulfilled and the proportion of time in a DAS since cohort entry was determined. Annual DCs/ICs (2021 Canadian dollars) were based on healthcare use and lost workforce/non-workforce productivity over the preceding year.

The association between the proportion of time in a DAS and annual DC/IC was examined through multivariable random-effects linear regressions.

Results 1692 patients were followed a mean of 9.7 years; 49.0% of assessments were active. Remission/LDA (per 25% increase in time in a remission/LDA state vs active) were associated with lower annual DC/IC: remission off-treatment (DC −$C1372; IC −$C2507), remission on-treatment (DC −$C973; IC −$C2604,) LDA-TC (DC −$C1158) and mLLDAS (DC −$C1040). There were no cost differences between remission/LDA states.

Conclusions Our data suggest that systemic lupus erythematosus patients who achieve remission, both off and on-therapy, and reductions in disease activity incur lower costs than those experiencing persistent disease activity.

  • Lupus Erythematosus, Systemic
  • Economics
  • Risk Factors
  • Health services research
  • Epidemiology

Data availability statement

All data relevant to the study are included in the article or uploaded as online supplemental information. Not applicable.

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Data availability statement

All data relevant to the study are included in the article or uploaded as online supplemental information. Not applicable.

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  • Handling editor Josef S Smolen

  • X @mugartegil

  • Presented at The data within this manuscript were presented at ACR Convergence 2022 (abstract number 2086) and Lupus in the 21st Century 2022.

  • Contributors MRWB, MFU-G and AEC provided substantial contributions to the conception and design of the work, the acquisition, analysis and interpretation of the work, and drafting and revising the work for important intellectual content. YS-P contributed substantially to the analysis and interpretation. JGH, MU, CG, S-CB, JR-D, JS-G, SB, DJW, DAI, AR, JTM, PRF, DDG, INB, MP, EMG, MAD, RR-G, SM, AJ, RFvV, CA, MM, GR-I, SL, MI, KK, SJ, CP, DLK, AA, BAP-E and GSA provided substantial contributions to the design of the work and data acquisition. FSC contributed to drafting and revising the work. All authors provided final approval of the version to be published. AEC is the guarantor of this work.

  • Funding JGH’s work was supported by the Canadian Institutes of Health Research (grant MOP-88526). CG’s work was supported by Lupus UK, Sandwell and West Birmingham Hospitals NHS Trust, and the Birmingham NIHR/Wellcome Trust Clinical Research Facility in Birmingham. S-CB is supported in part by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2021R1A6A1A03038899). SB holds a James McGill Research Chair. The Montreal General Hospital Lupus Clinic is partially supported by the Singer Family Fund for Lupus Research. DAI and Dr. AR are supported by the National Institute for Health Research University College London Hospitals Biomedical Research Center. PRF presently holds a tier 1 Canada Research Chair on Systemic Autoimmune Rheumatic Diseases at Université Laval. INB is a National Institute for Health Research (NIHR) Senior Investigator Emeritus and is funded by the NIHR Manchester Biomedical Research Centre (NIHR203308). The Hopkins Lupus Cohort is supported by NIH grants AR043727 and AR069572. MAD’s work was supported by NIH grant RR00046. RR-G’s work was supported by the NIH (grants 1U54TR001353 formerly 8UL1TR000150 and UL-1RR-025741, K24-AR-02318 and P60AR064464 formerly P60-AR-48098). SM is supported by grants R01 AR046588 and K24 AR002213. GR-I is supported by the Department of Education of the Basque Government, research grant IT 1512-22. SJ is supported by the Danish Rheumatism Association (A1028) and the Novo Nordisk Foundation (A05990). AEC holds the Arthritis Society Chair in Rheumatic Diseases at the University of Calgary.

  • Disclaimer The views expressed in this publication are those of the author(s) and not necessarily those of the NHS, the NIHR, or the Department of Health.

  • Competing interests MRWB has received consulting fees, speaking fees and/or honoraria from AbbVie, AstraZeneca, GlaxoSmithKline, Janssen and Sanofi Genzyme. MFU-G has received consulting and/or speaking fees from AstraZeneca, GlaxoSmithKline, Ferrer and a research grant from Janssen. CG has received consulting fees, speaking fees, and/or honoraria from AstraZeneca, Abbvie, Amgen, Sanofi, and UCB (less than $10 000 each). DJW has received consulting fees from Merck, EMD Serono, Pfizer, Lilly and Glenmark (less than $10 000 each). PRF has received consulting fees from AstraZeneca and GlaxoSmithKline (less than $10 000 each). DDG received consulting fees and/or honoraria from GlaxoSmithKline and AstraZeneca (less than $10 000). INB has received consulting fees, speaking fees, and/or honoraria from Eli Lilly, UCB, Roche, Merck Serono, MedImmune (less than $10 000 each) and grants from UCB, Genzyme Sanofi, and GlaxoSmithKline. EMG has paid consultation with investment analysts Guidepoint Global Gerson Lerman Group. RR-G has received consulting fees from Cabaletta, BristolMyersSquibb, Biogen, Merck, and Ampel Solutions (all less than $10 000 each). RFvV has received consulting fees, speaking fees and/or honoraria from AbbVie, AstraZeneca, Biotest, Bristol Myers Squibb, Celgene, GlaxoSmithKline, Janssen, Lilly, Novartis, Pfizer, and UCB (less than $10 000 each) and research support from AbbVie, Bristol Myers Squibb, GlaxoSmithKline, Pfizer and UCB. MI has received consulting fees from UCB and Amgen (less than $10 000 each). KK has received grants from UCB, Human Genome Sciences/GlaxoSmithKline, Takeda, Ablynx, Bristol-Myers Squibb, Pfizer, and Kyowa Hakko Kirin, and has received consulting fees from Exagen Diagnostics, Genentech, Eli Lilly, Bristol-Myers Squibb and Anthera (less than $10 000 each). AEC has received consulting fees, speaking fees, and/or honoraria from AstraZeneca, BristolMyersSquibb, GlaxoSmithKline, Roche and Otsuka (less than $10 000 each) and a research grant from GlaxoSmithKline. No other disclosures relevant to this article were reported.

  • Patient and public involvement Patients and/or the public were not involved in the design, or conduct, or reporting, or dissemination plans of this research.

  • Provenance and peer review Not commissioned; externally peer reviewed.

  • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.