The frequency and outcome of lupus nephritis: results from an international inception cohort study

doi:10.1093/rheumatology/kev311

Multicenter Study

. 2016 Feb;55(2):252-62.

doi: 10.1093/rheumatology/kev311. Epub 2015 Sep 5.

The frequency and outcome of lupus nephritis: results from an international inception cohort study

John G Hanly¹, Aidan G O'Keeffe², Li Su³, Murray B Urowitz⁴, Juanita Romero-Diaz⁵, Caroline Gordon⁶, Sang-Cheol Bae⁷, Sasha Bernatsky⁸, Ann E Clarke⁹, Daniel J Wallace¹⁰, Joan T Merrill¹¹, David A Isenberg¹², Anisur Rahman¹², Ellen M Ginzler¹³, Paul Fortin¹⁴, Dafna D Gladman⁴, Jorge Sanchez-Guerrero⁴, Michelle Petri¹⁵, Ian N Bruce¹⁶, Mary Anne Dooley¹⁷, Rosalind Ramsey-Goldman¹⁸, Cynthia Aranow¹⁹, Graciela S Alarcón²⁰, Barri J Fessler²⁰, Kristjan Steinsson²¹, Ola Nived²², Gunnar K Sturfelt²², Susan Manzi²³, Munther A Khamashta²⁴, Ronald F van Vollenhoven²⁵, Asad A Zoma²⁶, Manuel Ramos-Casals²⁷, Guillermo Ruiz-Irastorza²⁸, S Sam Lim²⁹, Thomas Stoll³⁰, Murat Inanc³¹, Kenneth C Kalunian³², Diane L Kamen³³, Peter Maddison³⁴, Christine A Peschken³⁵, Soren Jacobsen³⁶, Anca Askanase³⁷, Chris Theriault³⁸, Kara Thompson³⁸, Vernon Farewell³

Affiliations

¹ Division of Rheumatology, Department of Medicine and Department of Pathology, Queen Elizabeth II Health Sciences Centre and Dalhousie University, Halifax, Nova Scotia, Canada, john.hanly@cdha.nshealth.ca.
² Department of Statistical Science, University College London, London.
³ MRC Biostatistics Unit, Institute of Public Health, University Forvie Site, Cambridge, UK.
⁴ Centre for Prognosis Studies in the Rheumatic Diseases, Toronto Western Hospital and University of Toronto, Toronto, ON, Canada.
⁵ Instituto Nacional de Ciencias Medicas y Nutrición, Mexico City, Mexico.
⁶ Rheumatology Research Group, School of Immunity and Infection, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK.
⁷ Department of Rheumatology, Hanyang University Hospital for Rheumatic Diseases, Seoul, Korea.
⁸ Divisions of Rheumatology and Clinical Epidemiology, McGill University Health Centre.
⁹ Division of Rheumatology, University of Calgary, Alberta, Canada.
¹⁰ Cedars-Sinai/David Geffen School of Medicine at UCLA, Los Angeles, CA.
¹¹ Department of Clinical Pharmacology, Oklahoma Medical Research Foundation, Oklahoma City, OK, USA.
¹² Centre for Rheumatology, Department of Medicine, University College London, UK.
¹³ Department of Medicine, SUNY Downstate Medical Center, Brooklyn, NY, USA.
¹⁴ Division of Rheumatology, Centre Hospitalier Universitaire de Québec et Université Laval, Quebec City, Canada.
¹⁵ Division of Rheumatology, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
¹⁶ Arthritis Research UK Epidemiology Unit, Institute of Inflammation and Repair, Manchester Academic Health Sciences Centre, The University of Manchester, Manchester, UK, NIHR Manchester Musculoskeletal Biomedical Research Unit, Central Manchester University Hospitals NHS Foundation Trust, Manchester Academic Health Science Centre, Manchester, UK.
¹⁷ Thurston Arthritis Research Center, University of North Carolina, Chapel Hill, NC.
¹⁸ Northwestern University and Feinberg School of Medicine, Chicago, IL.
¹⁹ Feinstein Institute for Medical Research, Manhasset, NY.
²⁰ Department of Medicine, University of Alabama at Birmingham, Birmingham, AL, USA.
²¹ Center for Rheumatology Research, Landspitali University Hospital, Reykjavik, Iceland.
²² Department of Rheumatology, University Hospital Lund, Lund, Sweden.
²³ Division of Rheumatology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.
²⁴ Lupus Research Unit, The Rayne Institute, St Thomas' Hospital, King's College London School of Medicine, London, UK.
²⁵ Unit for Clinical Therapy Research, Karolinska Institute, Stockholm, Sweden.
²⁶ Lanarkshire Centre for Rheumatology, Hairmyres Hospital, East Kilbride, Scotland, UK.
²⁷ Josep Font Autoimmune Diseases Laboratory, IDIBAPS, Department of Autoimmune Diseases, Hospital Clínic, Barcelona, Spain.
²⁸ Autoimmune Diseases Research Unit, Department of Internal Medicine, BioCruces Health Research Institute, Hospital Universitario Cruces, University of the Basque Country, Barakaldo, Spain.
²⁹ Emory University School of Medicine, Division of Rheumatology, Atlanta, Georgia, USA.
³⁰ Kantonsspital Geissbergstr, Schaffhausen, Switzerland.
³¹ Division of Rheumatology, Department of Internal Medicine, Istanbul Medical Faculty, Istanbul University, Istanbul, Turkey.
³² UCSD School of Medicine, La Jolla, CA.
³³ Medical University of South Carolina, Charleston, SC, USA.
³⁴ Ysbyty Gwynedd Bangor, Gwynedd, North Wales, UK.
³⁵ University of Manitoba, Winnipeg, Manitoba, Canada.
³⁶ Department of Rheumatology, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.
³⁷ Hospital for Joint Diseases, NYU, Seligman Centre for Advanced Therapeutics, New York, NY, USA and.
³⁸ Department of Medicine, Queen Elizabeth II Health Sciences Centre and Dalhousie University, Halifax, Nova Scotia, Canada.

PMID: 26342222
PMCID: PMC4939728
DOI: 10.1093/rheumatology/kev311

Multicenter Study

The frequency and outcome of lupus nephritis: results from an international inception cohort study

John G Hanly et al. Rheumatology (Oxford). 2016 Feb.

. 2016 Feb;55(2):252-62.

doi: 10.1093/rheumatology/kev311. Epub 2015 Sep 5.

Authors

Affiliations

¹ Division of Rheumatology, Department of Medicine and Department of Pathology, Queen Elizabeth II Health Sciences Centre and Dalhousie University, Halifax, Nova Scotia, Canada, john.hanly@cdha.nshealth.ca.
² Department of Statistical Science, University College London, London.
³ MRC Biostatistics Unit, Institute of Public Health, University Forvie Site, Cambridge, UK.
⁴ Centre for Prognosis Studies in the Rheumatic Diseases, Toronto Western Hospital and University of Toronto, Toronto, ON, Canada.
⁵ Instituto Nacional de Ciencias Medicas y Nutrición, Mexico City, Mexico.
⁶ Rheumatology Research Group, School of Immunity and Infection, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK.
⁷ Department of Rheumatology, Hanyang University Hospital for Rheumatic Diseases, Seoul, Korea.
⁸ Divisions of Rheumatology and Clinical Epidemiology, McGill University Health Centre.
⁹ Division of Rheumatology, University of Calgary, Alberta, Canada.
¹⁰ Cedars-Sinai/David Geffen School of Medicine at UCLA, Los Angeles, CA.
¹¹ Department of Clinical Pharmacology, Oklahoma Medical Research Foundation, Oklahoma City, OK, USA.
¹² Centre for Rheumatology, Department of Medicine, University College London, UK.
¹³ Department of Medicine, SUNY Downstate Medical Center, Brooklyn, NY, USA.
¹⁴ Division of Rheumatology, Centre Hospitalier Universitaire de Québec et Université Laval, Quebec City, Canada.
¹⁵ Division of Rheumatology, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
¹⁶ Arthritis Research UK Epidemiology Unit, Institute of Inflammation and Repair, Manchester Academic Health Sciences Centre, The University of Manchester, Manchester, UK, NIHR Manchester Musculoskeletal Biomedical Research Unit, Central Manchester University Hospitals NHS Foundation Trust, Manchester Academic Health Science Centre, Manchester, UK.
¹⁷ Thurston Arthritis Research Center, University of North Carolina, Chapel Hill, NC.
¹⁸ Northwestern University and Feinberg School of Medicine, Chicago, IL.
¹⁹ Feinstein Institute for Medical Research, Manhasset, NY.
²⁰ Department of Medicine, University of Alabama at Birmingham, Birmingham, AL, USA.
²¹ Center for Rheumatology Research, Landspitali University Hospital, Reykjavik, Iceland.
²² Department of Rheumatology, University Hospital Lund, Lund, Sweden.
²³ Division of Rheumatology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.
²⁴ Lupus Research Unit, The Rayne Institute, St Thomas' Hospital, King's College London School of Medicine, London, UK.
²⁵ Unit for Clinical Therapy Research, Karolinska Institute, Stockholm, Sweden.
²⁶ Lanarkshire Centre for Rheumatology, Hairmyres Hospital, East Kilbride, Scotland, UK.
²⁷ Josep Font Autoimmune Diseases Laboratory, IDIBAPS, Department of Autoimmune Diseases, Hospital Clínic, Barcelona, Spain.
²⁸ Autoimmune Diseases Research Unit, Department of Internal Medicine, BioCruces Health Research Institute, Hospital Universitario Cruces, University of the Basque Country, Barakaldo, Spain.
²⁹ Emory University School of Medicine, Division of Rheumatology, Atlanta, Georgia, USA.
³⁰ Kantonsspital Geissbergstr, Schaffhausen, Switzerland.
³¹ Division of Rheumatology, Department of Internal Medicine, Istanbul Medical Faculty, Istanbul University, Istanbul, Turkey.
³² UCSD School of Medicine, La Jolla, CA.
³³ Medical University of South Carolina, Charleston, SC, USA.
³⁴ Ysbyty Gwynedd Bangor, Gwynedd, North Wales, UK.
³⁵ University of Manitoba, Winnipeg, Manitoba, Canada.
³⁶ Department of Rheumatology, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark.
³⁷ Hospital for Joint Diseases, NYU, Seligman Centre for Advanced Therapeutics, New York, NY, USA and.
³⁸ Department of Medicine, Queen Elizabeth II Health Sciences Centre and Dalhousie University, Halifax, Nova Scotia, Canada.

PMID: 26342222
PMCID: PMC4939728
DOI: 10.1093/rheumatology/kev311

Abstract

Objective: To determine nephritis outcomes in a prospective multi-ethnic/racial SLE inception cohort.

Methods: Patients in the Systemic Lupus International Collaborating Clinics inception cohort (≤15 months of SLE diagnosis) were assessed annually for estimated glomerular filtration rate (eGFR), proteinuria and end-stage renal disease (ESRD). Health-related quality of life was measured by the Short Form (36 questions) health survey questionnaire (SF-36) subscales, mental and physical component summary scores.

Results: There were 1827 patients, 89% females, mean (s.d.) age 35.1 (13.3) years. The mean (s.d.) SLE duration at enrolment was 0.5 (0.3) years and follow-up 4.6 (3.4) years. LN occurred in 700 (38.3%) patients: 566/700 (80.9%) at enrolment and 134/700 (19.1%) during follow-up. Patients with nephritis were younger, more frequently men and of African, Asian and Hispanic race/ethnicity. The estimated overall 10-year incidence of ESRD was 4.3% (95% CI: 2.8%, 5.8%), and with nephritis was 10.1% (95% CI: 6.6%, 13.6%). Patients with nephritis had a higher risk of death (HR = 2.98, 95% CI: 1.48, 5.99; P = 0.002) and those with eGFR <30 ml/min at diagnosis had lower SF-36 physical component summary scores (P < 0.01) and lower Physical function, Physical role and Bodily pain scores. Over time, patients with abnormal eGFR and proteinuria had lower SF-36 mental component summary (P ≤ 0.02) scores compared to patients with normal values.

Conclusion: LN occurred in 38.3% of SLE patients, frequently as the initial presentation, in a large multi-ethnic inception cohort. Despite current standard of care, nephritis was associated with ESRD and death, and renal insufficiency was linked to lower health-related quality of life. Further advances are required for the optimal treatment of LN.

Keywords: inception cohort; lupus; nephritis; outcomes research; systemic lupus erythematosus.

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Figures

F<sc>ig</sc>. 1 — **Fig. 1**
Onset of lupus nephritis following enrolment into the SLICC cohort

F<sc>ig</sc>. 2 — **Fig. 2**
Estimated cumulative incidence of end-stage renal disease and death End-stage renal disease (all causes) in the total SLICC cohort (A) and in those with (B) and without (C) LN. The estimated cumulative incidence of death (all causes) for those with LN at enrolment and those who never developed nephritis (D). ESRD: end stage renal disease.

F<sc>ig</sc>. 3 — **Fig. 3**
Spidergram of SF-36 subscale scores at diagnosis of lupus nephritis in three eGFR states PF: physical functioning; RP: role physical; BP: bodily pain; GH: general health; VT: vitality; SF: social functioning; RE: role emotional; MH: mental health; eGFR: estimated glomerular filtration rate.

See this image and copyright information in PMC

Comment in

Outcome of lupus glomerulonephritis: the role of prospective observational cohort studies.
Mak A, Tay SH. Mak A, et al. Rheumatology (Oxford). 2016 Feb;55(2):195-6. doi: 10.1093/rheumatology/kev220. Epub 2015 Sep 5. Rheumatology (Oxford). 2016. PMID: 26342225 No abstract available.

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References

1. Rovin BH, Stillman I. Kidney. In: Lahita R, ed. Systemic Lupus Erythematosus, 5th ed. San Diego, CA, USA: Academic Press, 2011: 769–814.
1. Dooley MA. Clinical and epidemiologic features of lupus nephritis. In: Wallace DJ, Hahn BH, eds. Dubois’ Lupus Erythematosus and related syndromes. Philadelphia, PA, USA: Elsevier Saunders, 2013: 438–54.
1. Costenbader KH, Desai A, Alarcon GS, et al. Trends in the incidence, demographics, and outcomes of end-stage renal disease due to lupus nephritis in the US from 1995 to 2006. Arthritis Rheum 2011;63:1681–8. - PMC - PubMed
1. Croca SC, Rodrigues T, Isenberg DA. Assessment of a lupus nephritis cohort over a 30-year period. Rheumatology 2011;50:1424–30. - PubMed
1. Houssiau F, Vasconcelos C, D’Cruz D, et al. Immunosuppressive therapy in lupus nephritis: the Euro-Lupus Nephritis Trial, a randomized trial of low-dose versus high-dose intravenous cyclophosphamide. Arthritis Rheum 2002;46:2121–31. - PubMed

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[1] Rovin BH, Stillman I. Kidney. In: Lahita R, ed. Systemic Lupus Erythematosus, 5th ed. San Diego, CA, USA: Academic Press, 2011: 769–814.

[2] Rovin BH, Stillman I. Kidney. In: Lahita R, ed. Systemic Lupus Erythematosus, 5th ed. San Diego, CA, USA: Academic Press, 2011: 769–814.

[3] Dooley MA. Clinical and epidemiologic features of lupus nephritis. In: Wallace DJ, Hahn BH, eds. Dubois’ Lupus Erythematosus and related syndromes. Philadelphia, PA, USA: Elsevier Saunders, 2013: 438–54.

[4] Dooley MA. Clinical and epidemiologic features of lupus nephritis. In: Wallace DJ, Hahn BH, eds. Dubois’ Lupus Erythematosus and related syndromes. Philadelphia, PA, USA: Elsevier Saunders, 2013: 438–54.

[5] Costenbader KH, Desai A, Alarcon GS, et al. Trends in the incidence, demographics, and outcomes of end-stage renal disease due to lupus nephritis in the US from 1995 to 2006. Arthritis Rheum 2011;63:1681–8. - PMC - PubMed

[6] Costenbader KH, Desai A, Alarcon GS, et al. Trends in the incidence, demographics, and outcomes of end-stage renal disease due to lupus nephritis in the US from 1995 to 2006. Arthritis Rheum 2011;63:1681–8. - PMC - PubMed

[7] Croca SC, Rodrigues T, Isenberg DA. Assessment of a lupus nephritis cohort over a 30-year period. Rheumatology 2011;50:1424–30. - PubMed

[8] Croca SC, Rodrigues T, Isenberg DA. Assessment of a lupus nephritis cohort over a 30-year period. Rheumatology 2011;50:1424–30. - PubMed

[9] Houssiau F, Vasconcelos C, D’Cruz D, et al. Immunosuppressive therapy in lupus nephritis: the Euro-Lupus Nephritis Trial, a randomized trial of low-dose versus high-dose intravenous cyclophosphamide. Arthritis Rheum 2002;46:2121–31. - PubMed

[10] Houssiau F, Vasconcelos C, D’Cruz D, et al. Immunosuppressive therapy in lupus nephritis: the Euro-Lupus Nephritis Trial, a randomized trial of low-dose versus high-dose intravenous cyclophosphamide. Arthritis Rheum 2002;46:2121–31. - PubMed

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The frequency and outcome of lupus nephritis: results from an international inception cohort study

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The frequency and outcome of lupus nephritis: results from an international inception cohort study

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