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Research ArticleArticle
Open Access

Monitoring of Osteonecrosis in Systemic Lupus Erythematosus Patients: A Systematic Review and Metaanalysis

Sara Hussein, Manon Suitner, Sarah Béland-Bonenfant, Alexandra Baril-Dionne, Ben Vandermeer, Nancy Santesso, Stephanie Keeling, Janet E. Pope, Aurore Fifi-Mah and Josiane Bourré-Tessier
The Journal of Rheumatology July 2018, jrheum.170837; DOI: https://doi.org/10.3899/jrheum.170837
Sara Hussein
From the Department of Medicine, University of Montréal, Montréal, Quebec; Alberta Research Center, and Department of Medicine, University of Alberta, Edmonton, Alberta; Department of Clinical Epidemiology and Biostatistics, McMaster University, Hamilton; Department of Medicine, Western University of Canada, London, Ontario; Department of Medicine, University of Calgary, Calgary, Alberta, Canada. S. Hussein, MD, Rheumatology Resident, Department of Medicine, University of Montreal; M. Suitner, MD, Rheumatology Resident, Department of Medicine, University of Montreal; S. Béland-Bonenfant, MD, Internal Medicine Resident, Department of Medicine, University of Montreal; A. Baril-Dionne, MD, Rheumatology Resident, University of Montréal; B. Vandermeer, MSc, biostatistician, Alberta Research Center, University of Alberta; N. Santesso, RD, MLIS, PhD, Assistant Professor, Department of Clinical Epidemiology and Biostatistics, McMaster University; S. Keeling, MD, MSc, FRCPC, Associate Professor, Division of Rheumatology, Department of Medicine, University of Alberta; J.E. Pope, MD, MPH, FRCPC, Professor of Medicine, University of Western Ontario, Division Head, Rheumatology; A. Fifi-Mah, MD, FRCPC, Clinical Assistant Professor, Arthritis Diseases Clinic, University of Calgary; J. Bourré-Tessier, MD, MSc, FRCPC, Clinical Assistant Professor, Division of Rheumatology, Department of Medicine, University of Montreal. Address correspondence to Dr. J. Bourré-Tessier, Service de rhumatologie, CHUM, 264 Blvd. René-Lévesque Est, Montreal, Québec H2X 1P1, Canada. E-mail: josiane.bourre.tessier@umontreal.ca. Full Release Article. For details see Reprints and Permissions at jrheum.org. Accepted for publication February 16, 2018.
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Manon Suitner
From the Department of Medicine, University of Montréal, Montréal, Quebec; Alberta Research Center, and Department of Medicine, University of Alberta, Edmonton, Alberta; Department of Clinical Epidemiology and Biostatistics, McMaster University, Hamilton; Department of Medicine, Western University of Canada, London, Ontario; Department of Medicine, University of Calgary, Calgary, Alberta, Canada. S. Hussein, MD, Rheumatology Resident, Department of Medicine, University of Montreal; M. Suitner, MD, Rheumatology Resident, Department of Medicine, University of Montreal; S. Béland-Bonenfant, MD, Internal Medicine Resident, Department of Medicine, University of Montreal; A. Baril-Dionne, MD, Rheumatology Resident, University of Montréal; B. Vandermeer, MSc, biostatistician, Alberta Research Center, University of Alberta; N. Santesso, RD, MLIS, PhD, Assistant Professor, Department of Clinical Epidemiology and Biostatistics, McMaster University; S. Keeling, MD, MSc, FRCPC, Associate Professor, Division of Rheumatology, Department of Medicine, University of Alberta; J.E. Pope, MD, MPH, FRCPC, Professor of Medicine, University of Western Ontario, Division Head, Rheumatology; A. Fifi-Mah, MD, FRCPC, Clinical Assistant Professor, Arthritis Diseases Clinic, University of Calgary; J. Bourré-Tessier, MD, MSc, FRCPC, Clinical Assistant Professor, Division of Rheumatology, Department of Medicine, University of Montreal. Address correspondence to Dr. J. Bourré-Tessier, Service de rhumatologie, CHUM, 264 Blvd. René-Lévesque Est, Montreal, Québec H2X 1P1, Canada. E-mail: josiane.bourre.tessier@umontreal.ca. Full Release Article. For details see Reprints and Permissions at jrheum.org. Accepted for publication February 16, 2018.
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Sarah Béland-Bonenfant
From the Department of Medicine, University of Montréal, Montréal, Quebec; Alberta Research Center, and Department of Medicine, University of Alberta, Edmonton, Alberta; Department of Clinical Epidemiology and Biostatistics, McMaster University, Hamilton; Department of Medicine, Western University of Canada, London, Ontario; Department of Medicine, University of Calgary, Calgary, Alberta, Canada. S. Hussein, MD, Rheumatology Resident, Department of Medicine, University of Montreal; M. Suitner, MD, Rheumatology Resident, Department of Medicine, University of Montreal; S. Béland-Bonenfant, MD, Internal Medicine Resident, Department of Medicine, University of Montreal; A. Baril-Dionne, MD, Rheumatology Resident, University of Montréal; B. Vandermeer, MSc, biostatistician, Alberta Research Center, University of Alberta; N. Santesso, RD, MLIS, PhD, Assistant Professor, Department of Clinical Epidemiology and Biostatistics, McMaster University; S. Keeling, MD, MSc, FRCPC, Associate Professor, Division of Rheumatology, Department of Medicine, University of Alberta; J.E. Pope, MD, MPH, FRCPC, Professor of Medicine, University of Western Ontario, Division Head, Rheumatology; A. Fifi-Mah, MD, FRCPC, Clinical Assistant Professor, Arthritis Diseases Clinic, University of Calgary; J. Bourré-Tessier, MD, MSc, FRCPC, Clinical Assistant Professor, Division of Rheumatology, Department of Medicine, University of Montreal. Address correspondence to Dr. J. Bourré-Tessier, Service de rhumatologie, CHUM, 264 Blvd. René-Lévesque Est, Montreal, Québec H2X 1P1, Canada. E-mail: josiane.bourre.tessier@umontreal.ca. Full Release Article. For details see Reprints and Permissions at jrheum.org. Accepted for publication February 16, 2018.
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Alexandra Baril-Dionne
From the Department of Medicine, University of Montréal, Montréal, Quebec; Alberta Research Center, and Department of Medicine, University of Alberta, Edmonton, Alberta; Department of Clinical Epidemiology and Biostatistics, McMaster University, Hamilton; Department of Medicine, Western University of Canada, London, Ontario; Department of Medicine, University of Calgary, Calgary, Alberta, Canada. S. Hussein, MD, Rheumatology Resident, Department of Medicine, University of Montreal; M. Suitner, MD, Rheumatology Resident, Department of Medicine, University of Montreal; S. Béland-Bonenfant, MD, Internal Medicine Resident, Department of Medicine, University of Montreal; A. Baril-Dionne, MD, Rheumatology Resident, University of Montréal; B. Vandermeer, MSc, biostatistician, Alberta Research Center, University of Alberta; N. Santesso, RD, MLIS, PhD, Assistant Professor, Department of Clinical Epidemiology and Biostatistics, McMaster University; S. Keeling, MD, MSc, FRCPC, Associate Professor, Division of Rheumatology, Department of Medicine, University of Alberta; J.E. Pope, MD, MPH, FRCPC, Professor of Medicine, University of Western Ontario, Division Head, Rheumatology; A. Fifi-Mah, MD, FRCPC, Clinical Assistant Professor, Arthritis Diseases Clinic, University of Calgary; J. Bourré-Tessier, MD, MSc, FRCPC, Clinical Assistant Professor, Division of Rheumatology, Department of Medicine, University of Montreal. Address correspondence to Dr. J. Bourré-Tessier, Service de rhumatologie, CHUM, 264 Blvd. René-Lévesque Est, Montreal, Québec H2X 1P1, Canada. E-mail: josiane.bourre.tessier@umontreal.ca. Full Release Article. For details see Reprints and Permissions at jrheum.org. Accepted for publication February 16, 2018.
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Ben Vandermeer
From the Department of Medicine, University of Montréal, Montréal, Quebec; Alberta Research Center, and Department of Medicine, University of Alberta, Edmonton, Alberta; Department of Clinical Epidemiology and Biostatistics, McMaster University, Hamilton; Department of Medicine, Western University of Canada, London, Ontario; Department of Medicine, University of Calgary, Calgary, Alberta, Canada. S. Hussein, MD, Rheumatology Resident, Department of Medicine, University of Montreal; M. Suitner, MD, Rheumatology Resident, Department of Medicine, University of Montreal; S. Béland-Bonenfant, MD, Internal Medicine Resident, Department of Medicine, University of Montreal; A. Baril-Dionne, MD, Rheumatology Resident, University of Montréal; B. Vandermeer, MSc, biostatistician, Alberta Research Center, University of Alberta; N. Santesso, RD, MLIS, PhD, Assistant Professor, Department of Clinical Epidemiology and Biostatistics, McMaster University; S. Keeling, MD, MSc, FRCPC, Associate Professor, Division of Rheumatology, Department of Medicine, University of Alberta; J.E. Pope, MD, MPH, FRCPC, Professor of Medicine, University of Western Ontario, Division Head, Rheumatology; A. Fifi-Mah, MD, FRCPC, Clinical Assistant Professor, Arthritis Diseases Clinic, University of Calgary; J. Bourré-Tessier, MD, MSc, FRCPC, Clinical Assistant Professor, Division of Rheumatology, Department of Medicine, University of Montreal. Address correspondence to Dr. J. Bourré-Tessier, Service de rhumatologie, CHUM, 264 Blvd. René-Lévesque Est, Montreal, Québec H2X 1P1, Canada. E-mail: josiane.bourre.tessier@umontreal.ca. Full Release Article. For details see Reprints and Permissions at jrheum.org. Accepted for publication February 16, 2018.
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Nancy Santesso
From the Department of Medicine, University of Montréal, Montréal, Quebec; Alberta Research Center, and Department of Medicine, University of Alberta, Edmonton, Alberta; Department of Clinical Epidemiology and Biostatistics, McMaster University, Hamilton; Department of Medicine, Western University of Canada, London, Ontario; Department of Medicine, University of Calgary, Calgary, Alberta, Canada. S. Hussein, MD, Rheumatology Resident, Department of Medicine, University of Montreal; M. Suitner, MD, Rheumatology Resident, Department of Medicine, University of Montreal; S. Béland-Bonenfant, MD, Internal Medicine Resident, Department of Medicine, University of Montreal; A. Baril-Dionne, MD, Rheumatology Resident, University of Montréal; B. Vandermeer, MSc, biostatistician, Alberta Research Center, University of Alberta; N. Santesso, RD, MLIS, PhD, Assistant Professor, Department of Clinical Epidemiology and Biostatistics, McMaster University; S. Keeling, MD, MSc, FRCPC, Associate Professor, Division of Rheumatology, Department of Medicine, University of Alberta; J.E. Pope, MD, MPH, FRCPC, Professor of Medicine, University of Western Ontario, Division Head, Rheumatology; A. Fifi-Mah, MD, FRCPC, Clinical Assistant Professor, Arthritis Diseases Clinic, University of Calgary; J. Bourré-Tessier, MD, MSc, FRCPC, Clinical Assistant Professor, Division of Rheumatology, Department of Medicine, University of Montreal. Address correspondence to Dr. J. Bourré-Tessier, Service de rhumatologie, CHUM, 264 Blvd. René-Lévesque Est, Montreal, Québec H2X 1P1, Canada. E-mail: josiane.bourre.tessier@umontreal.ca. Full Release Article. For details see Reprints and Permissions at jrheum.org. Accepted for publication February 16, 2018.
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Stephanie Keeling
From the Department of Medicine, University of Montréal, Montréal, Quebec; Alberta Research Center, and Department of Medicine, University of Alberta, Edmonton, Alberta; Department of Clinical Epidemiology and Biostatistics, McMaster University, Hamilton; Department of Medicine, Western University of Canada, London, Ontario; Department of Medicine, University of Calgary, Calgary, Alberta, Canada. S. Hussein, MD, Rheumatology Resident, Department of Medicine, University of Montreal; M. Suitner, MD, Rheumatology Resident, Department of Medicine, University of Montreal; S. Béland-Bonenfant, MD, Internal Medicine Resident, Department of Medicine, University of Montreal; A. Baril-Dionne, MD, Rheumatology Resident, University of Montréal; B. Vandermeer, MSc, biostatistician, Alberta Research Center, University of Alberta; N. Santesso, RD, MLIS, PhD, Assistant Professor, Department of Clinical Epidemiology and Biostatistics, McMaster University; S. Keeling, MD, MSc, FRCPC, Associate Professor, Division of Rheumatology, Department of Medicine, University of Alberta; J.E. Pope, MD, MPH, FRCPC, Professor of Medicine, University of Western Ontario, Division Head, Rheumatology; A. Fifi-Mah, MD, FRCPC, Clinical Assistant Professor, Arthritis Diseases Clinic, University of Calgary; J. Bourré-Tessier, MD, MSc, FRCPC, Clinical Assistant Professor, Division of Rheumatology, Department of Medicine, University of Montreal. Address correspondence to Dr. J. Bourré-Tessier, Service de rhumatologie, CHUM, 264 Blvd. René-Lévesque Est, Montreal, Québec H2X 1P1, Canada. E-mail: josiane.bourre.tessier@umontreal.ca. Full Release Article. For details see Reprints and Permissions at jrheum.org. Accepted for publication February 16, 2018.
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Janet E. Pope
From the Department of Medicine, University of Montréal, Montréal, Quebec; Alberta Research Center, and Department of Medicine, University of Alberta, Edmonton, Alberta; Department of Clinical Epidemiology and Biostatistics, McMaster University, Hamilton; Department of Medicine, Western University of Canada, London, Ontario; Department of Medicine, University of Calgary, Calgary, Alberta, Canada. S. Hussein, MD, Rheumatology Resident, Department of Medicine, University of Montreal; M. Suitner, MD, Rheumatology Resident, Department of Medicine, University of Montreal; S. Béland-Bonenfant, MD, Internal Medicine Resident, Department of Medicine, University of Montreal; A. Baril-Dionne, MD, Rheumatology Resident, University of Montréal; B. Vandermeer, MSc, biostatistician, Alberta Research Center, University of Alberta; N. Santesso, RD, MLIS, PhD, Assistant Professor, Department of Clinical Epidemiology and Biostatistics, McMaster University; S. Keeling, MD, MSc, FRCPC, Associate Professor, Division of Rheumatology, Department of Medicine, University of Alberta; J.E. Pope, MD, MPH, FRCPC, Professor of Medicine, University of Western Ontario, Division Head, Rheumatology; A. Fifi-Mah, MD, FRCPC, Clinical Assistant Professor, Arthritis Diseases Clinic, University of Calgary; J. Bourré-Tessier, MD, MSc, FRCPC, Clinical Assistant Professor, Division of Rheumatology, Department of Medicine, University of Montreal. Address correspondence to Dr. J. Bourré-Tessier, Service de rhumatologie, CHUM, 264 Blvd. René-Lévesque Est, Montreal, Québec H2X 1P1, Canada. E-mail: josiane.bourre.tessier@umontreal.ca. Full Release Article. For details see Reprints and Permissions at jrheum.org. Accepted for publication February 16, 2018.
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Aurore Fifi-Mah
From the Department of Medicine, University of Montréal, Montréal, Quebec; Alberta Research Center, and Department of Medicine, University of Alberta, Edmonton, Alberta; Department of Clinical Epidemiology and Biostatistics, McMaster University, Hamilton; Department of Medicine, Western University of Canada, London, Ontario; Department of Medicine, University of Calgary, Calgary, Alberta, Canada. S. Hussein, MD, Rheumatology Resident, Department of Medicine, University of Montreal; M. Suitner, MD, Rheumatology Resident, Department of Medicine, University of Montreal; S. Béland-Bonenfant, MD, Internal Medicine Resident, Department of Medicine, University of Montreal; A. Baril-Dionne, MD, Rheumatology Resident, University of Montréal; B. Vandermeer, MSc, biostatistician, Alberta Research Center, University of Alberta; N. Santesso, RD, MLIS, PhD, Assistant Professor, Department of Clinical Epidemiology and Biostatistics, McMaster University; S. Keeling, MD, MSc, FRCPC, Associate Professor, Division of Rheumatology, Department of Medicine, University of Alberta; J.E. Pope, MD, MPH, FRCPC, Professor of Medicine, University of Western Ontario, Division Head, Rheumatology; A. Fifi-Mah, MD, FRCPC, Clinical Assistant Professor, Arthritis Diseases Clinic, University of Calgary; J. Bourré-Tessier, MD, MSc, FRCPC, Clinical Assistant Professor, Division of Rheumatology, Department of Medicine, University of Montreal. Address correspondence to Dr. J. Bourré-Tessier, Service de rhumatologie, CHUM, 264 Blvd. René-Lévesque Est, Montreal, Québec H2X 1P1, Canada. E-mail: josiane.bourre.tessier@umontreal.ca. Full Release Article. For details see Reprints and Permissions at jrheum.org. Accepted for publication February 16, 2018.
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Josiane Bourré-Tessier
From the Department of Medicine, University of Montréal, Montréal, Quebec; Alberta Research Center, and Department of Medicine, University of Alberta, Edmonton, Alberta; Department of Clinical Epidemiology and Biostatistics, McMaster University, Hamilton; Department of Medicine, Western University of Canada, London, Ontario; Department of Medicine, University of Calgary, Calgary, Alberta, Canada. S. Hussein, MD, Rheumatology Resident, Department of Medicine, University of Montreal; M. Suitner, MD, Rheumatology Resident, Department of Medicine, University of Montreal; S. Béland-Bonenfant, MD, Internal Medicine Resident, Department of Medicine, University of Montreal; A. Baril-Dionne, MD, Rheumatology Resident, University of Montréal; B. Vandermeer, MSc, biostatistician, Alberta Research Center, University of Alberta; N. Santesso, RD, MLIS, PhD, Assistant Professor, Department of Clinical Epidemiology and Biostatistics, McMaster University; S. Keeling, MD, MSc, FRCPC, Associate Professor, Division of Rheumatology, Department of Medicine, University of Alberta; J.E. Pope, MD, MPH, FRCPC, Professor of Medicine, University of Western Ontario, Division Head, Rheumatology; A. Fifi-Mah, MD, FRCPC, Clinical Assistant Professor, Arthritis Diseases Clinic, University of Calgary; J. Bourré-Tessier, MD, MSc, FRCPC, Clinical Assistant Professor, Division of Rheumatology, Department of Medicine, University of Montreal. Address correspondence to Dr. J. Bourré-Tessier, Service de rhumatologie, CHUM, 264 Blvd. René-Lévesque Est, Montreal, Québec H2X 1P1, Canada. E-mail: josiane.bourre.tessier@umontreal.ca. Full Release Article. For details see Reprints and Permissions at jrheum.org. Accepted for publication February 16, 2018.
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Abstract

Objective Nontraumatic osteonecrosis (ON) is a well-recognized complication causing disability and affecting quality of life in patients with systemic lupus erythematosus (SLE). The aim of this study was to identify the risk factors for ON, and to identify the minimal investigation(s) needed to optimally monitor the risk of ON in patients with SLE.

Methods A systematic review was conducted using MEDLINE and EMBASE. These databases were searched up to January 2016 using the Medical Subject Heading (MeSH) terms “Osteonecrosis,” “Systemic lupus erythematosus,” and synonymous text words. Randomized controlled trials, case control, cohort, and cross-sectional studies were included. Risk factors for ON in patients with SLE were compiled. The quality of each study was assessed using the Newcastle-Ottawa scale for nonrandomized studies. The quality of evidence of each risk factor was assessed using the Grading of Recommendations, Assessment, Development, and Evaluation method.

Results Of the 545 references yielded, 50 met inclusion criteria. Corticosteroid (CS) use may be strongly associated with ON in patients with SLE. Other clinical variables were moderately associated, including hypertension, serositis, renal disease, vasculitis, arthritis, and central nervous system disease. However, the evidence was low to very low in quality.

Conclusion Based on the best evidence available, CS use may be strongly associated with ON in patients with SLE. Results of this review were considered in the development of recommendations for the diagnosis and monitoring of patients with SLE in Canada and will guide clinicians in their assessment of these patients.

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Monitoring of Osteonecrosis in Systemic Lupus Erythematosus Patients: A Systematic Review and Metaanalysis
Sara Hussein, Manon Suitner, Sarah Béland-Bonenfant, Alexandra Baril-Dionne, Ben Vandermeer, Nancy Santesso, Stephanie Keeling, Janet E. Pope, Aurore Fifi-Mah, Josiane Bourré-Tessier
The Journal of Rheumatology Jul 2018, jrheum.170837; DOI: 10.3899/jrheum.170837

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Monitoring of Osteonecrosis in Systemic Lupus Erythematosus Patients: A Systematic Review and Metaanalysis
Sara Hussein, Manon Suitner, Sarah Béland-Bonenfant, Alexandra Baril-Dionne, Ben Vandermeer, Nancy Santesso, Stephanie Keeling, Janet E. Pope, Aurore Fifi-Mah, Josiane Bourré-Tessier
The Journal of Rheumatology Jul 2018, jrheum.170837; DOI: 10.3899/jrheum.170837
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