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Commentary| Volume 41, ISSUE 7, P1355-1365, July 2019

Preventing Rheumatoid Arthritis: A Global Challenge

  • Jessica Widdifield
    Correspondence
    Address correspondence to: Jessica Widdifield, PhD, 2075 Bayview Avenue MG 352, Toronto ON, M4N 3M5, Canada.
    Affiliations
    Sunnybrook Research Institute, Holland Bone & Joint Research Program, Toronto, Ontario, Canada

    Institute of Health Policy, Management and Evaluation, University of Toronto, Toronto, Ontario, Canada

    ICES, Toronto, Ontario, Canada
    Search for articles by this author

      Abstract

      Significant advancements have been made in the discovery of gene signatures, biomarkers, novel therapeutic targets, diagnostic tools, and risk factors that predict the development of rheumatoid arthritis (RA). There is also overwhelming evidence that treatment of early RA can prevent or alter disease progression and potentially lead to drug-free remission. Despite these advancements, there are significant challenges to identifying patients at risk of developing RA on a global scale. This commentary provides an overview of challenges related to the primary, secondary, and tertiary prevention of RA in the context of health care systems. Patient-level, provider-level, and health care system–level barriers to implementing prevention strategies are discussed. Strategies and opportunities to address these challenges, on both a local and global scale, are reported. Benefits as well as potential negative consequences that may be associated with implementation of prevention strategies for RA are discussed in the context of individuals and public health.

      Key Words

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      References

        • Van Baarsen L.G.
        • de Hair M.J.
        • Semmelink J.F.
        • et al.
        Synovial tissue profiling in autoantibody positive at risk individuals reveals gene signatures associated with later development of rheumatoid arthritis.
        Ann Rheum Dis. 2018; 77 (EULAR 2018; Amsterdam: Abstract OP0266)
        • Shervington L.
        • Darekar A.
        • Shaikh M.
        • Mathews R.
        • Shervington A.
        Identifying reliable diagnostic/predictive biomarkers for rheumatoid arthritis.
        Biomarker Insights. 2018; 13 (1177271918801005)
        • Tak P.P.
        • Doorenspleet M.E.
        • de Hair M.J.H.
        • et al.
        Dominant B cell receptor clones in peripheral blood predict onset of arthritis in individuals at risk for rheumatoid arthritis.
        Annals of the Rheumatic Diseases. 2017; 76: 1924-1930
        • Liu C.H.
        • Abrams N.D.
        • Carrick D.M.
        • et al.
        Biomarkers of chronic inflammation in disease development and prevention: challenges and opportunities.
        Nat Immunol. 2017; 18: 1175-1180
        • Humby F.C.
        • Al Balushi F.
        • Lliso G.
        • Cauli A.
        • Pitzalis C.
        Can synovial pathobiology integrate with current clinical and imaging prediction models to achieve personalized health care in rheumatoid arthritis?.
        Front Med. 2017; 4: 41
        • Koenders M.I.
        • van den Berg W.B.
        Novel therapeutic targets in rheumatoid arthritis.
        Trends Pharma Sci. 2015; 36: 189-195
        • van Beers-Tas M.H.
        • Ter Wee M.M.
        • van Tuyl L.H.
        • et al.
        Initial validation and results of the symptoms in persons at risk of rheumatoid arthritis (SPARRA) questionnaire: a EULAR project.
        RMD Open. 2018; 4e000641
        • Avouac J.
        • Gossec L.
        • Dougados M.
        Diagnostic and predictive value of anti-cyclic citrullinated protein antibodies in rheumatoid arthritis: a systematic literature review.
        Ann Rheum Dis. 2006; 65: 845-851
        • Visser H.
        • le Cessie S.
        • Vos K.
        • Breedveld F.C.
        • Hazes J.M.
        How to diagnose rheumatoid arthritis early: a prediction model for persistent (erosive) arthritis.
        Arthritis Rheum. 2002; 46: 357-365
        • Nell V.P.
        • Machold K.P.
        • Stamm T.A.
        • et al.
        Autoantibody profiling as early diagnostic and prognostic tool for rheumatoid arthritis.
        Ann Rheum Dis. 2005; 64: 1731-1736
        • Smolik I.
        • Robinson D.B.
        • Bernstein C.N.
        • El-Gabalawy H.S.
        First-degree relatives of patients with rheumatoid arthritis exhibit high prevalence of joint symptoms.
        J Rheumatol. 2013; 40: 818-824
        • Svendsen A.J.
        • Kyvik K.O.
        • Houen G.
        • et al.
        On the origin of rheumatoid arthritis: the impact of environment and genes—a population based twin study.
        PLoS One. 2013; 8e57304
        • Yarwood A.
        • Huizinga T.W.
        • Worthington J.
        The genetics of rheumatoid arthritis: risk and protection in different stages of the evolution of RA.
        Rheumatology (Oxford, England). 2016; 55: 199-209
        • Barnabe C.
        • Jones C.A.
        • Bernatsky S.
        • et al.
        Inflammatory arthritis prevalence and health services use in the First Nations and Non-First Nations populations of Alberta, Canada.
        Arthritis Care Res. 2017; 69: 467-474
        • McDougall C.
        • Hurd K.
        • Barnabe C.
        Systematic review of rheumatic disease epidemiology in the indigenous populations of Canada, the United States, Australia, and New Zealand.
        Semin Arthritis Rheum. 2017; 46: 675-686
        • Sparks J.A.
        • Karlson E.W.
        The roles of cigarette smoking and the lung in the transitions between phases of preclinical rheumatoid arthritis.
        Curr Rheumatol Rep. 2016; 18: 15
        • Deane K.D.
        Preclinical rheumatoid arthritis and rheumatoid arthritis prevention.
        Curr Rheumatol Rep. 2018; 20: 50
        • Smolen J.S.
        • Landewe R.
        • Bijlsma J.
        • et al.
        EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2016 update.
        Ann Rheum Dis. 2017; 76: 960-977
        • Singh J.A.
        • Saag K.G.
        • Bridges Jr., S.L.
        • et al.
        2015 American College of Rheumatology guideline for the treatment of rheumatoid arthritis.
        Arthritis Rheumatol. 2016; 68: 1-26
        • Combe B.
        • Landewe R.
        • Daien C.I.
        • et al.
        2016 update of the EULAR recommendations for the management of early arthritis.
        Ann Rheum Dis. 2017; 76: 948-959
        • Hughes C.D.
        • Scott D.L.
        • Ibrahim F.
        • TITRATE Programme Investigators
        Intensive therapy and remissions in rheumatoid arthritis: a systematic review.
        BMC Musculoskelet Disord. 2018; 19: 389
        • van Nies J.A.
        • Krabben A.
        • Schoones J.W.
        • Huizinga T.W.
        • Kloppenburg M.
        • van der Helm-van Mil A.H.
        What is the evidence for the presence of a therapeutic window of opportunity in rheumatoid arthritis? A systematic literature review.
        Ann Rheum Dis. 2014; 73: 861-870
        • Karlson E.W.
        • van Schaardenburg D.
        • van der Helm-van Mil A.H.
        Strategies to predict rheumatoid arthritis development in at-risk populations.
        Rheumatology (Oxford). 2016; 55: 6-15
        • Costenbader K.H.
        • Chang S.C.
        • Laden F.
        • Puett R.
        • Karlson E.W.
        Geographic variation in rheumatoid arthritis incidence among women in the United States.
        Arch Intern Med. 2008; 168: 1664-1670
        • Alamanos Y.
        • Voulgari P.V.
        • Drosos A.A.
        Incidence and prevalence of rheumatoid arthritis, based on the 1987 American College of Rheumatology criteria: a systematic review.
        Semin Arthritis Rheum. 2006; 36: 182-188
        • Gabriel S.E.
        • Michaud K.
        Epidemiological studies in incidence, prevalence, mortality, and comorbidity of the rheumatic diseases.
        Arthritis Res Ther. 2009; 11: 229
        • Crowson C.S.
        • Matteson E.L.
        • Myasoedova E.
        • et al.
        The lifetime risk of adult-onset rheumatoid arthritis and other inflammatory autoimmune rheumatic diseases.
        Arthritis Rheum. 2011; 63: 633-639
        • Karlson E.W.
        • Ding B.
        • Keenan B.T.
        • et al.
        Association of environmental and genetic factors and gene-environment interactions with risk of developing rheumatoid arthritis.
        Arthritis Care Res (Hoboken). 2013; 65: 1147-1156
        • Sparks J.A.
        • Chen C.Y.
        • Jiang X.
        • et al.
        Improved performance of epidemiologic and genetic risk models for rheumatoid arthritis serologic phenotypes using family history.
        Ann Rheum Dis. 2015; 74: 1522-1529
        • Lahiri M.
        • Luben R.N.
        • Morgan C.
        • et al.
        Using lifestyle factors to identify individuals at higher risk of inflammatory polyarthritis (results from the European Prospective Investigation of Cancer-Norfolk and the Norfolk Arthritis Register—the EPIC-2-NOAR Study).
        Ann Rheum Dis. 2014; 73: 219-226
        • Hemminki K.
        • Li X.
        • Sundquist J.
        • Sundquist K.
        Familial associations of rheumatoid arthritis with autoimmune diseases and related conditions.
        Arthritis Rheum. 2009; 60: 661-668
        • Lloyd-Jones D.M.
        • Goff Jr., D.C.
        • Stone N.J.
        Guidelines for cardiovascular risk assessment and cholesterol treatment.
        JAMA. 2014; 311: 2235
        • Noble D.
        • Mathur R.
        • Dent T.
        • Meads C.
        • Greenhalgh T.
        Risk models and scores for type 2 diabetes: systematic review.
        BMJ. 2011; 343: d7163
        • Bestermann W.
        • Houston M.C.
        • Basile J.
        • et al.
        Addressing the global cardiovascular risk of hypertension, dyslipidemia, diabetes mellitus, and the metabolic syndrome in the southeastern United States, part II: treatment recommendations for management of the global cardiovascular risk of hypertension, dyslipidemia, diabetes mellitus, and the metabolic syndrome.
        Am J Med Sci. 2005; 329: 292-305
        • Deane K.D.
        Can rheumatoid arthritis be prevented?.
        Best Pract Res Clin Rheumatol. 2013; 27: 467-485
        • van der Helm-van Mil A.H.
        • Detert J.
        • le Cessie S.
        • et al.
        Validation of a prediction rule for disease outcome in patients with recent-onset undifferentiated arthritis: moving toward individualized treatment decision-making.
        Arthritis Rheum. 2008; 58: 2241-2247
        • van der Helm-van Mil A.H.
        • le Cessie S.
        • van Dongen H.
        • Breedveld F.C.
        • Toes R.E.
        • Huizinga T.W.
        A prediction rule for disease outcome in patients with recent-onset undifferentiated arthritis: how to guide individual treatment decisions.
        Arthritis Rheum. 2007; 56: 433-440
        • Kuriya B.
        • Cheng C.K.
        • Chen H.M.
        • Bykerk V.P.
        Validation of a prediction rule for development of rheumatoid arthritis in patients with early undifferentiated arthritis.
        Ann Rheum Dis. 2009; 68: 1482-1485
        • Lloyd-Jones D.M.
        Cardiovascular risk prediction: basic concepts, current status, and future directions.
        Circulation. 2010; 121: 1768-1777
        • Aho K.
        • Heliovaara M.
        Risk factors for rheumatoid arthritis.
        Ann Med. 2004; 36: 242-251
        • Bowes J.
        • Barton A.
        Recent advances in the genetics of RA susceptibility.
        Rheumatology (Oxford). 2008; 47: 399-402
        • Karlson E.W.
        • Deane K.
        Environmental and gene-environment interactions and risk of rheumatoid arthritis.
        Rheum Dis Clin North Am. 2012; 38: 405-426
        • Klareskog L.
        • Gregersen P.K.
        • Huizinga T.W.
        Prevention of autoimmune rheumatic disease: state of the art and future perspectives.
        Ann Rheum Dis. 2010; 69: 2062-2066
        • Klareskog L.
        • Stolt P.
        • Lundberg K.
        • et al.
        A new model for an etiology of rheumatoid arthritis: smoking may trigger HLA-DR (shared epitope)-restricted immune reactions to autoantigens modified by citrullination.
        Arthritis Rheum. 2006; 54: 38-46
        • Mahdi H.
        • Fisher B.A.
        • Kallberg H.
        • et al.
        Specific interaction between genotype, smoking and autoimmunity to citrullinated alpha-enolase in the etiology of rheumatoid arthritis.
        Nat Genet. 2009; 41: 1319-1324
        • Lee H.S.
        • Irigoyen P.
        • Kern M.
        • et al.
        Interaction between smoking, the shared epitope, and anti-cyclic citrullinated peptide: a mixed picture in three large North American rheumatoid arthritis cohorts.
        Arthritis Rheum. 2007; 56: 1745-1753
        • Gerlag D.M.
        • Raza K.
        • van Baarsen L.G.
        • et al.
        EULAR recommendations for terminology and research in individuals at risk of rheumatoid arthritis: report from the Study Group for Risk Factors for Rheumatoid Arthritis.
        Ann Rheum Dis. 2012; 71: 638-641
        • Finckh A.
        • Deane K.D.
        Prevention of rheumatic diseases: strategies, caveats, and future directions.
        Rheum Dis Clin North Am. 2014; 40: 771-785
      1. Comprehensive Cervical Cancer Control: A Guide to Essential Practice. WHO Guidelines Approved by the Guidelines Review Committee, Geneva2014
        • Sabatino S.A.
        • Burns R.B.
        • Davis R.B.
        • Phillips R.S.
        • Chen Y.H.
        • McCarthy E.P.
        Breast carcinoma screening and risk perception among women at increased risk for breast carcinoma: results from a national survey.
        Cancer. 2004; 100: 2338-2346
        • Forster A.S.
        • Forbes A.
        • Dodhia H.
        • et al.
        Changes in detection of retinopathy in type 2 diabetes in the first 4 years of a population-based diabetic eye screening program: retrospective cohort study.
        Diabetes Care. 2013; 36: 2663-2669
        • Lawler F.H.
        Reasons to exercise caution when considering a screening program for type 2 diabetes mellitus.
        Mayo Clin Proc. 2009; 84: 34-36
        • van der Linden M.P.
        • le Cessie S.
        • Raza K.
        • et al.
        Long-term impact of delay in assessment of patients with early arthritis.
        Arthritis Rheum. 2010; 62: 3537-3546
        • Landewe R.B.M.
        Overdiagnosis and overtreatment in rheumatology: a little caution is in order.
        Ann Rheum Dis. 2018; 77: 1394-1396
        • Esserman L.J.
        • Thompson I.M.
        • Reid B.
        • et al.
        Addressing overdiagnosis and overtreatment in cancer: a prescription for change.
        Lancet Oncol. 2014; 15: e234-e242
        • Welch H.G.
        • Black W.C.
        Overdiagnosis in cancer.
        J Natl Cancer Inst. 2010; 102: 605-613
        • Berwick D.M.
        • Hackbarth A.D.
        Eliminating waste in US health care.
        JAMA. 2012; 307: 1513-1516
        • Rantapaa-Dahlqvist S.
        • de Jong B.A.
        • Berglin E.
        • et al.
        Antibodies against cyclic citrullinated peptide and IgA rheumatoid factor predict the development of rheumatoid arthritis.
        Arthritis Rheum. 2003; 48: 2741-2749
        • Nielen M.M.
        • van der Horst A.R.
        • van Schaardenburg D.
        • et al.
        Antibodies to citrullinated human fibrinogen (ACF) have diagnostic and prognostic value in early arthritis.
        Ann Rheum Dis. 2005; 64: 1199-1204
        • Nielen M.M.
        • van Schaardenburg D.
        • Reesink H.W.
        • et al.
        Specific autoantibodies precede the symptoms of rheumatoid arthritis: a study of serial measurements in blood donors.
        Arthritis Rheum. 2004; 50: 380-386
        • Young K.A.
        • Deane K.D.
        • Derber L.A.
        • et al.
        Relatives without rheumatoid arthritis show reactivity to anti-citrullinated protein/peptide antibodies that are associated with arthritis-related traits: studies of the etiology of rheumatoid arthritis.
        Arthritis Rheum. 2013; 65: 1995-2004
        • Nielsen S.F.
        • Bojesen S.E.
        • Schnohr P.
        • Nordestgaard B.G.
        Elevated rheumatoid factor and long term risk of rheumatoid arthritis: a prospective cohort study.
        BMJ. 2012; 345: e5244
        • Stahl E.A.
        • Raychaudhuri S.
        • Remmers E.F.
        • et al.
        Genome-wide association study meta-analysis identifies seven new rheumatoid arthritis risk loci.
        Nat Genet. 2010; 42: 508-514
        • Okada Y.
        • Wu D.
        • Trynka G.
        • et al.
        Genetics of rheumatoid arthritis contributes to biology and drug discovery.
        Nature. 2014; 506: 376-381
        • Khoury M.J.
        • McCabe L.L.
        • McCabe E.R.
        Population screening in the age of genomic medicine.
        N Engl J Med. 2003; 348: 50-58
        • Knoppers B.M.
        • Hirtle M.
        • Glass K.C.
        Policy forum: genetic technologies. Commercialization of genetic research and public policy.
        Science. 1999; 286: 2277-2278
        • Kaufert P.A.
        Health policy and the new genetics.
        Soc Sci Med. 2000; 51: 821-829
        • Ojha R.P.
        • Thertulien R.
        Health care policy issues as a result of the genetic revolution: implications for public health.
        Am J Public Health. 2005; 95: 385-388
        • Andermann A.
        • Blancquaert I.
        • Beauchamp S.
        • Dery V.
        Revisiting Wilson and Jungner in the genomic age: a review of screening criteria over the past 40 years.
        Bull World Health Organ. 2008; 86: 317-319
        • Mendis S.
        • Alwan A.E.
        A Prioritized Research Agenda for Prevention and Control of Noncommunicable Diseases: CVD, Cancer, Chronic Respiratory Disease, Diabetes.
        2011 (Geneva)
        • Muir Gray J.A.
        Evidence based policy making.
        BMJ. 2004; 329: 988-989
        • van Steenbergen H.W.
        • Aletaha D.
        • Beaart-van de Voorde L.J.
        • et al.
        EULAR definition of arthralgia suspicious for progression to rheumatoid arthritis.
        Ann Rheum Dis. 2017; 76: 491-496
        • Machado P.
        • Castrejon I.
        • Katchamart W.
        • et al.
        Multinational evidence-based recommendations on how to investigate and follow-up undifferentiated peripheral inflammatory arthritis: integrating systematic literature research and expert opinion of a broad international panel of rheumatologists in the 3E Initiative.
        Ann Rheum Dis. 2011; 70: 15-24
        • Barhamain A.S.
        • Magliah R.F.
        • Shaheen M.H.
        • et al.
        The journey of rheumatoid arthritis patients: a review of reported lag times from the onset of symptoms.
        Open Access Rheumatol. 2017; 9: 139-150
        • Villeneuve E.
        • Kuriya B.
        • Bombardier C.
        Patients considered as having undifferentiated peripheral inflammatory arthritis: a systematic review.
        J Rheumatol Suppl. 2011; 87: 3-9
        • van Aken J.
        • van Dongen H.
        • le Cessie S.
        • Allaart C.F.
        • Breedveld F.C.
        • Huizinga T.W.
        Comparison of long term outcome of patients with rheumatoid arthritis presenting with undifferentiated arthritis or with rheumatoid arthritis: an observational cohort study.
        Ann Rheum Dis. 2006; 65: 20-25
        • Knudtson M.L.
        • Beanlands R.
        • Brophy J.M.
        • et al.
        Treating the right patient at the right time: access to specialist consultation and non-invasive testing.
        Can J Cardiol. 2006; 22: 819-824
        • Simons G.
        • Mallen C.D.
        • Kumar K.
        • Stack R.J.
        • Raza K.
        A qualitative investigation of the barriers to help-seeking among members of the public presented with symptoms of new-onset rheumatoid arthritis.
        J Rheumatol. 2015; 42: 585-592
        • van der Heide I.
        • Poureslami I.
        • Mitic W.
        • Shum J.
        • Rootman I.
        • FitzGerald J.M.
        Health literacy in chronic disease management: a matter of interaction.
        J Clin Epidemiol. 2018; 102: 134-138
        • Bell M.J.
        • Tavares R.
        • Guillemin F.
        • Bykerk V.P.
        • Tugwell P.
        • Wells G.A.
        Development of a self-administered early inflammatory arthritis detection tool.
        BMC Musculoskelet Disord. 2010; 11: 50
        • Potter J.
        • Odutola J.
        • Gonzales C.A.
        • Ward M.M.
        Validation of English and Spanish-language versions of a screening questionnaire for rheumatoid arthritis in an underserved community.
        J Rheumatol. 2008; 35: 1545-1549
        • Maksymowych W.
        Development of a web-based screening tool for early rheumatoid arthritis-ERASE: the E-triage RA study in early arthritis.
        Arthritis Rheumatol. 2008; 59: 1599
        • Khraishi M.
        • Uphall E.
        • Mong J.
        The self-administered rheumatoid arthritis (RA) screening questionnaire (RASQ) is a simple and simple and effective tool to detect RA patients [abstract].
        Ann Rheum Dis. 2010; 69: 374
        • EULAR
        The EULAR Campaign 2017/2018.
        2018
        • Villeneuve E.
        • Nam J.L.
        • Bell M.J.
        • et al.
        A systematic literature review of strategies promoting early referral and reducing delays in the diagnosis and management of inflammatory arthritis.
        Ann Rheum Dis. 2013; 72: 13-22
        • Landewé R.B.M.
        Response to: 'Early identification of rheumatoid arthritis; the risk of overtreatment in perspective' by Landewé.
        Ann Rheum Dis. 2018 Aug 10; https://doi.org/10.1136/annrheumdis-2018-214172
        • Bernatsky S.
        • Feldman D.
        • Shrier I.
        • et al.
        Care pathways in early rheumatoid arthritis.
        Can Fam Physician. 2006; 52: 1444-1445
        • Garneau K.
        • Iversen M.
        • Tsao H.
        • Solomon D.
        Primary care physicians' perspectives towards managing rheumatoid arthritis: room for improvement.
        Arthritis Res Ther. 2011; 13: R189
        • Johnson K.L.
        • Hertz D.
        • Stobbe G.
        • et al.
        Project Extension for Community Healthcare Outcomes (ECHO) in multiple sclerosis: increasing clinician capacity.
        Int J MS Care. 2017; 19: 283-289
        • Glass L.M.
        • Waljee A.K.
        • McCurdy H.
        • Su G.L.
        • Sales A.
        Specialty care access network-extension of community healthcare outcomes model program for liver disease improves specialty care access.
        Dig Dis Sci. 2017; 62: 3344-3349
        • Arora S.
        • Thornton K.
        • Murata G.
        • et al.
        Outcomes of treatment for hepatitis C virus infection by primary care providers.
        N Engl J Med. 2011; 364: 2199-2207
        • Harrington J.T.
        • Walsh M.B.
        Pre-appointment management of new patient referrals in rheumatology: a key strategy for improving health care delivery.
        Arthritis Rheum. 2001; 45: 295-300
        • Ukachukwu V.
        • Alam A.
        • Baskar S.
        • Price T.
        • Venkatachalam S.
        How adequate are rheumatology referral letters? A prospective review of referrals to a secondary care rheumatology service.
        Rheumatology (Oxford, England). 2014; 53: i81-i82
        • Jack C.
        • Hazel E.
        • Bernatsky S.
        Something's missing here: a look at the quality of rheumatology referral letters.
        Rheumatol Int. 2012; 32: 1083-1085
        • Murray K.
        • Rutledge N.
        • Shah Q.
        • et al.
        AB1251 Quality of inpatient referrals to rheumatology in an Irish tertiary referral hospital.
        Ann Rheum Dis. 2018; 77: 1721
        • Rydz A.
        • Fu F.
        • Drew M.
        • Rumsey D.
        • Yuan Y.
        • Chan M.
        Quality of referral letters to pediatric rheumatology and its impact on access to care [abstract].
        Arthritis Rheumatol. 2017; 69
        • Graydon S.L.
        • Thompson A.E.
        Triage of referrals to an outpatient rheumatology clinic: analysis of referral information and triage.
        J Rheumatol. 2008; 35: 1378-1383
        • Bachali A.
        • Sahli H.
        • Tekaya R.
        • Mahmoud I.
        • Hedhili S.
        • Abdelmoula L.
        Analysis of referral letters to rheumatology consultation in Tunisia.
        Egypt Rheumatologist. 2017; 39: 179-182
        • Doddrell C.
        • MacPhie E.
        What makes a good quality referral for patients with suspected inflammatory arthritis? [abstract].
        Rheumatology. 2017; 56 (p.kex062.183)
        • Widdifield J.
        • Tu K.
        • Carter Thorne J.
        • et al.
        Patterns of care among patients referred to rheumatologists in Ontario, Canada.
        Arthritis Care Res (Hoboken). 2017; 69: 104-114
        • Harrington J.T.
        A view of our future: the case for redesigning rheumatology practice.
        Arthritis Rheum. 2003; 49: 716-719
        • Stainkey L.A.
        • Seidl I.A.
        • Johnson A.J.
        • Tulloch G.E.
        • Pain T.
        The challenge of long waiting lists: how we implemented a GP referral system for non-urgent specialist' appointments at an Australian public hospital.
        BMC Health Serv Res. 2010; 10: 303
        • Clarke A.
        • Blundell N.
        • Forde I.
        • et al.
        Can guidelines improve referral to elective surgical specialties for adults? A systematic review.
        Qual Saf Health Care. 2010; 19: 187-194
        • Goeb V.
        • Smolen J.
        • Emery P.
        • Marzo-Ortega H.
        Early inflammatory clinics. Experience with early arthritis/back pain clinics.
        Clin Exp Rheumatol. 2009; 27: S74-S79
        • Ahluwalia V.
        • Larsen T.L.H.
        • Kennedy C.A.
        • Inrig T.
        • Lundon K.
        An advanced clinician practitioner in arthritis care can improve access to rheumatology care in community-based practice.
        J Multidiscip Healthc. 2019; 12: 63-71
        • Carpenter T.
        • Katz S.J.
        Review of a rheumatology triage system: simple, accurate, and effective.
        Clin Rheumatol. 2014; 33: 247-252
        • Farrer C.
        • Abraham L.
        • Jerome D.
        • Hochman J.
        • Gakhal N.
        Triage of rheumatology referrals facilitates wait time benchmarks.
        J Rheumatol. 2016; 43: 2064-2067
        • Suter E.
        • Birney A.
        • Charland P.
        • et al.
        Optimizing the interprofessional workforce for centralized intake of patients with osteoarthritis and rheumatoid disease: case study.
        Hum Resour Health. 2015; 13: 41
        • Garner S.
        • Lopatina E.
        • Rankin J.A.
        • Marshall D.A.
        Nurse-led care for patients with rheumatoid arthritis: a systematic review of the effect on quality of care.
        J Rheumatol. 2017; 44: 757-765
        • Gartner M.
        • Fabrizii J.P.
        • Koban E.
        • et al.
        Immediate access rheumatology clinic: efficiency and outcomes.
        Ann Rheum Dis. 2012; 71: 363-368
        • Valenzuela O.
        • Ibanez Vodnizza S.E.
        How to reduce the waiting time for the first consultation with the rheumatologist as a first step for a timely treatment.
        Ann Rheum Dis. 2019; 78: 279
        • Kulcsar Z.
        • Albert D.
        • Ercolano E.
        • Mecchella J.N.
        Telerheumatology: a technology appropriate for virtually all.
        Semin Arthritis Rheum. 2016; 46: 380-385
        • McDougall J.A.
        • Ferucci E.D.
        • Glover J.
        • Fraenkel L.
        Telerheumatology: a systematic review.
        Arthritis Care Res. 2017; 69: 1546-1557
        • Piga M.
        • Cangemi I.
        • Mathieu A.
        • Cauli A.
        Telemedicine for patients with rheumatic diseases: systematic review and proposal for research agenda.
        Semin Arthritis Rheum. 2017; 47: 121-128
        • Poulsen K.A.
        • Millen C.M.
        • Lakshman U.I.
        • Buttner P.G.
        • Roberts L.J.
        Satisfaction with rural rheumatology telemedicine service.
        Int J Rheum Dis. 2015; 18: 304-314
        • Aletaha D.
        • Neogi T.
        • Silman A.J.
        • et al.
        2010 Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League against Rheumatism collaborative initiative.
        Arthritis Rheum. 2010; 62: 2569-2581
        • Radner H.
        • Neogi T.
        • Smolen J.S.
        • Aletaha D.
        Performance of the 2010 ACR/EULAR classification criteria for rheumatoid arthritis: a systematic literature review.
        Ann Rheum Dis. 2014; 73: 114-123
        • Sun J.
        • Zhang Y.
        • Liu L.
        • Liu G.
        Diagnostic accuracy of combined tests of anti cyclic citrullinated peptide antibody and rheumatoid factor for rheumatoid arthritis: a meta-analysis.
        Clin Exp Rheumatol. 2014; 32: 11-21
        • Aggarwal R.
        • Ringold S.
        • Khanna D.
        • et al.
        Distinctions between diagnostic and classification criteria?.
        Arthritis Care Res (Hoboken). 2015; 67: 891-897
        • Smolen J.S.
        • Aletaha D.
        • Grisar J.
        • Redlich K.
        • Steiner G.
        • Wagner O.
        The need for prognosticators in rheumatoid arthritis. Biological and clinical markers: where are we now?.
        Arthritis Res Ther. 2008; 10: 208
        • Nishimura K.
        • Sugiyama D.
        • Kogata Y.
        • et al.
        Meta-analysis: diagnostic accuracy of anti-cyclic citrullinated peptide antibody and rheumatoid factor for rheumatoid arthritis.
        Ann Intern Med. 2007; 146: 797-808
        • Van Hoovels L.
        • Bossuyt X.
        Harmonisation of laboratory tests for rheumatic diseases: still a long way to go.
        Ann Rheum Dis. 2018 Dec 4; https://doi.org/10.1136/annrheumdis-2018-214696
        • Global Burden of Disease Study 2013 Collaborators
        Global, regional, and national incidence, prevalence, and years lived with disability for 301 acute and chronic diseases and injuries in 188 countries, 1990-2013: a systematic analysis for the Global Burden of Disease Study 2013.
        Lancet. 2015; 386: 743-800
        • Smith E.
        • Hoy D.G.
        • Cross M.
        • et al.
        The global burden of other musculoskeletal disorders: estimates from the Global Burden of Disease 2010 study.
        Ann Rheum Dis. 2014; 73: 1462-1469
        • Al Maini M.
        • Adelowo F.
        • Al Saleh J.
        • et al.
        The global challenges and opportunities in the practice of rheumatology: white paper by the World Forum on Rheumatic and Musculoskeletal Diseases.
        Clin Rheumatol. 2015; 34: 819-829
        • Deal C.L.
        • Hooker R.
        • Harrington T.
        • et al.
        The United States rheumatology workforce: supply and demand, 2005-2025.
        Arthritis Rheum. 2007; 56: 722-729
        • Widdifield J.
        • Paterson J.M.
        • Bernatsky S.
        • et al.
        The rising burden of rheumatoid arthritis surpasses rheumatology supply in Ontario.
        Can J Public Health. 2013; 104: e450-e455
        • Battafarano D.F.
        • Ditmyer M.
        • Bolster M.B.
        • et al.
        2015 American college of rheumatology workforce study: supply and demand projections of adult rheumatology workforce, 2015-2030.
        Arthritis Care Res (Hoboken). 2018; 70: 617-626
        • Barber C.E.
        • Jewett L.
        • Badley E.M.
        • et al.
        Stand up and be counted: measuring and mapping the rheumatology workforce in Canada.
        J Rheumatol. 2017; 44: 248-257
        • Barber C.E.H.
        • Nasr M.
        • Barnabe C.
        • et al.
        Planning for the rheumatologist workforce: factors associated with work hours and volumes.
        J Clin Rheumatol. 2019; 25: 142-146
        • Namageyo-Funa A.
        • Nanavati P.
        The challenges of addressing primary prevention of diabetes: a response to recommendations from the chronic disease directors' project.
        J Public Health Manag Pract. 2008; 14: 26-28
        • Bello A.K.
        • Nwankwo E.
        • El Nahas A.M.
        Prevention of chronic kidney disease: a global challenge.
        Kidney Int Suppl. 2005; : S11-S17
        • Schenk D.
        Current challenges for the successful treatment and prevention of Alzheimer's disease: treating the pathologies of the disease to change its clinical course.
        Alzheimer Dement. 2008; 4: S119-S121
        • Smolen J.S.
        • Aletaha D.
        • McInnes I.B.
        Rheumatoid arthritis.
        Lancet. 2016; 388: 2023-2038
        • Morris Z.S.
        • Wooding S.
        • Grant J.
        The answer is 17 years, what is the question: understanding time lags in translational research.
        J R Soc Med. 2011; 104: 510-520
        • Trochim W.
        • Kane C.
        • Graham M.J.
        • Pincus H.A.
        Evaluating translational research: a process marker model.
        Clin Translat Sci. 2011; 4: 153-162
        • de Jong T.D.
        • Vosslamber S.
        • Verweij C.L.
        Moving towards personalized medicine in rheumatoid arthritis.
        Arthritis Res Ther. 2014; 16: 110
        • Baynam G.
        • Bowman F.
        • Lister K.
        • et al.
        Improved diagnosis and care for rare diseases through implementation of precision public health framework.
        Adv Exp Med Biol. 2017; 1031: 55-94