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ERS clinical practice guidelines on treatment of sarcoidosis

Robert P. Baughman, Dominique Valeyre, Peter Korsten, Alexander G. Mathioudakis, Wim A. Wuyts, Athol Wells, Paola Rottoli, Hiliaro Nunes, Elyse E. Lower, Marc A. Judson, Dominique Israel-Biet, Jan C. Grutters, Marjolein Drent, Daniel A. Culver, Francesco Bonella, Katerina Antoniou, Filippo Martone, Bernd Quadder, Ginger Spitzer, Blin Nagavci, Thomy Tonia, David Rigau, Daniel R. Ouellette
European Respiratory Journal 2021 58: 2004079; DOI: 10.1183/13993003.04079-2020
Robert P. Baughman
1Dept of Medicine, University of Cincinnati Medical Center, Cincinnati, OH, USA
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  • For correspondence: bob.baughman@uc.edu
Dominique Valeyre
2INSERM UMR 1272, Université Sorbonne Paris Nord, AP-HP, Hôpital Avicenne, Bobigny, Groupe Hospitalier Paris-Saint Joseph, Paris, France
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Peter Korsten
3Dept of Nephrology and Rheumatology, University Medical Center Göttingen, Göttingen, Germany
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Alexander G. Mathioudakis
4North West Lung Centre, Wythenshawe Hospital, Manchester University NHS Foundation Trust, and Division of Infection, Immunity and Respiratory Medicine, The University of Manchester, Manchester, UK
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Wim A. Wuyts
5Unit for Interstitial Lung Diseases, Dept of Respiratory Medicine, University Hospitals Leuven, Leuven, Belgium
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Athol Wells
6Royal Brompton Hospital, London, UK
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Paola Rottoli
7Specialization School of Respiratory Diseases, Dept of Medical, Surgical and Neurological Sciences, Siena University, Siena, Italy
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Hiliaro Nunes
8INSERM UMR 1272, Université Sorbonne Paris Nord, Service de Pneumologie, Centre de Référence des Maladies Pulmonaires Rares, AP-HP, Hôpital Avicenne, Bobigny, France
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Elyse E. Lower
1Dept of Medicine, University of Cincinnati Medical Center, Cincinnati, OH, USA
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Marc A. Judson
9Dept of Medicine, Albany Medical College, Albany, NY, USA
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Dominique Israel-Biet
10Université de Paris, Centre de Compétences Maladies Rares Pulmonaires, AP-HP, Hôpital Européen Georges Pompidou, Paris, France
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Jan C. Grutters
11ILD Center of Excellence, Dept of Pulmonology, St Antonius Hospital, Nieuwegein, The Netherlands
12Division of Heart and Lungs, University Medical Center Utrecht, Utrecht, The Netherlands
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Marjolein Drent
11ILD Center of Excellence, Dept of Pulmonology, St Antonius Hospital, Nieuwegein, The Netherlands
13Dept of Pharmacology and Toxicology, Faculty of Health and Life Sciences, Maastricht University, Maastricht, The Netherlands
14ILD Care Foundation Research Team, Ede, The Netherlands
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Daniel A. Culver
15Cleveland Clinic, Cleveland, OH, USA
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Francesco Bonella
16Center for Interstitial and Rare Lung Diseases, Pneumology Dept, Ruhrlandklinik, University Hospital, University of Essen, Essen, Germany
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Katerina Antoniou
17Dept of Respiratory Medicine, Laboratory of Molecular and Cellular Pneumonology, Medical School, University of Crete, Heraklion, Greece
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Filippo Martone
18Amici Contro la Sarcoidosi Italia ONLUS, Bologna, Italy
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Bernd Quadder
19Deutsche Sarkoidose-Vereinigung eV (DSV), Meerbusch, Germany
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Ginger Spitzer
20Foundation for Sarcoidosis Research, Chicago, IL, USA
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Blin Nagavci
21Institute for Evidence in Medicine, Medical Center and Faculty of Medicine, University of Freiburg, Freiburg, Germany
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Thomy Tonia
22Institute of Social and Preventive Medicine, University of Bern, Bern, Switzerland
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David Rigau
23Cochrane Iberoamerica, Barcelona, Spain
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Daniel R. Ouellette
24Henry Ford Hospital, Detroit, MI, USA
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  • Article
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  • FIGURE 1
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    FIGURE 1

    Approach for pulmonary sarcoidosis. Use of rituximab, JAK inhibitor and repository corticotropin injection (RCI) should be on a case-by-case basis. This figure is a combination of the recommendations made in this guideline and a description of Task Force members’ current practice in situations where there was not enough evidence to warrant a recommendation or for questions for which a systematic review of the literature was not undertaken. Note that the information depicted as current practice (in white boxes) is not intended as a recommendation for clinical practice. #: assess need for treatment based on low risk, intermediate risk but impaired quality of life or high risk as discussed in text. GC: glucocorticoid.

  • FIGURE 2
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    FIGURE 2

    Stepwise approach to the management of cosmetically important cutaneous sarcoidosis. Use of apremilast and tofacitinib should be on a case-by-case basis. This figure is a combination of the recommendations made in this guideline and a description of Task Force members’ current practice in situations where there was not enough evidence to warrant a recommendation or for questions for which a systematic review of the literature was not undertaken. Note that the information depicted as current practice (in white boxes) is not intended as a recommendation for clinical practice. #: assess need for treatment as discussed in text. GC: glucocorticoid.

  • FIGURE 3
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    FIGURE 3

    Approach to cardiac sarcoidosis. This figure is a combination of the recommendations made in this guideline and a description of Task Force members’ current practice in situations where there was not enough evidence to warrant a recommendation or for questions for which a systematic review of the literature was not undertaken. Note that the information depicted as current practice (in white boxes) is not intended as a recommendation for clinical practice. #: use of implanted cardioverter defibrillator recommendation adapted from the Heart Rhythm Society [160, 162]; ¶: clinically relevant cardiac sarcoidosis is defined as rhythm disturbances, heart failure or high risk for sudden cardiac death; +: infliximab and adalimumab are usually used in combination with second-line agents. GC: glucocorticoids.

  • FIGURE 4
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    FIGURE 4

    Approach to neurologic sarcoidosis. This figure is a combination of the recommendations made in this guideline, and a description of Task Force members’ current practice in situations where there was not enough evidence to warrant a recommendation or for questions for which a systematic review of the literature was not undertaken. Note that the information depicted as current practice (in white boxes) is not intended as a recommendation for clinical practice. #: infliximab and adalimumab are usually used in combination with second-line agents. GC: glucocorticoids.

  • FIGURE 5
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    FIGURE 5

    Approach to the evaluation and management of sarcoidosis-associated fatigue. The use of low-dose corticosteroids with or without methotrexate should be considered on a case-by-case basis. This figure is a combination of the recommendations made in this guideline, and a description of Task Force members’ current practice in situations where there was not enough evidence to warrant a recommendation or for questions for which a systematic review of the literature was not undertaken. Note that the information depicted as current practice (in white boxes) is not intended as a recommendation for clinical practice. #: other causes of fatigue include diabetes mellitus, thyroid dysfunction, neuroendocrine disorders, sleep apnoea, small-fibre neuropathy, vitamin D deficiency with low 1,25-dihydroxycholecalciferol, congestive heart failure and neurologic disease.

  • FIGURE 6
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    FIGURE 6

    An approach to small-fibre neuropathy symptoms used by Task Force members. The use of intravenous immunoglobulin (IVIg) or anti-tumour necrosis factor (TNF) antagonists should be considered on a case-by-case basis. This figure is a combination of the recommendations made in this guideline and a description of Task Force members’ current practice in situations where there was not enough evidence to warrant a recommendation or for questions for which a systematic review of the literature was not undertaken. Note that the information depicted as current practice (in white boxes) is not intended as a recommendation for clinical practice. GABA: γ-aminobutyric acid.

Tables

  • Figures
  • Supplementary Materials
  • TABLE 1

    Task Force recommendations

    PICO questionRecommendations
    1) In patients with pulmonary sarcoidosis, should glucocorticoid treatment be used versus no immunosuppressive treatment?
    • For untreated patients with major involvement from pulmonary sarcoidosis believed to be at higher risk of future mortality or permanent disability from sarcoidosis, we recommend the introduction of glucocorticoid treatment to improve and/or preserve FVC and QoL. (Strong recommendation, low quality of evidence.)

    2) In patients with pulmonary sarcoidosis, should one add immunosuppressive treatment or remain on glucocorticoid treatment alone?
    • For patients with symptomatic pulmonary sarcoidosis believed to be at higher risk of future mortality or permanent disability from sarcoidosis who have been treated with glucocorticoids and have continued disease or unacceptable side-effects from glucocorticoids, we suggest the addition of methotrexate to improve and/or preserve FVC and QoL. (Conditional recommendation, very low quality of evidence.)

    • For patients with symptomatic pulmonary sarcoidosis believed to be at higher risk of future mortality or permanent disability from sarcoidosis who have been treated with glucocorticoids or other immunosuppressive agents and have continued disease, we suggest the addition of infliximab to improve and/or preserve FVC and QoL. (Conditional recommendation, low quality of evidence.)

    3) In patients with cutaneous sarcoidosis, should glucocorticoid treatment be used versus no immunosuppressive treatment?
    • For patients with cutaneous sarcoidosis and cosmetically important active skin lesions which cannot be controlled by local treatment, we suggest oral glucocorticoids be considered to reduce skin lesions. (Conditional recommendation, very low quality of evidence.)

    4) In patients with cutaneous sarcoidosis, should one add other immunosuppressive treatment when treatment with glucocorticoids has not been effective?
    • For patients with cutaneous sarcoidosis who have been treated with glucocorticoids and/or other immunosuppressive agents and have continued cosmetically important active skin disease, we suggest the addition of infliximab compared to no additional treatment to reduce skin lesions. (Conditional recommendation, low quality of evidence.)

    5) In patients with clinically relevant cardiac sarcoidosis, should glucocorticoids with or without other immunosuppressives versus no immunosuppression be used?
    • For patients with evidence of functional cardiac abnormalities, including heart block, dysrhythmias or cardiomyopathy, we recommend the use of glucocorticoids (with or without other immunosuppressives). (Strong recommendation, very low quality of evidence.)

    6) In patients with neurosarcoidosis, should immunosuppressive treatment be used versus no immunosuppressive treatment?
    • For patients with clinically significant neurosarcoidosis, we recommend treatment with glucocorticoids. (Strong recommendation, very low quality of evidence.)

    • For patients with neurosarcoidosis that have been treated with glucocorticoids and have continued disease, we suggest the addition of methotrexate. (Conditional recommendation, very low quality of evidence.)

    • For patients with neurosarcoidosis that have been treated with glucocorticoids and a second-line agent (methotrexate, azathioprine, mycophenolate mofetil) and have continued disease, we suggest the addition of infliximab. (Conditional recommendation, very low quality of evidence.)

    7) In patients with sarcoidosis-associated fatigue, should immunosuppressants, neurostimulants, exercise or other treatments be used versus no treatment for fatigue?
    • In patients with sarcoidosis who have troublesome fatigue, we suggest a pulmonary rehabilitation programme and/or inspiratory muscle strength training for 6–12 weeks to improve fatigue. (Conditional recommendation, low quality of evidence.)

    • In patients with sarcoidosis who have troublesome fatigue that is not related to disease activity, and after consideration of a pulmonary exercise or rehabilitation programme, we suggest the use of d-methylphenidate or armodafinil for 8 weeks to test its effect on fatigue and tolerability. (Conditional recommendation, low quality of evidence.)

    8) In sarcoidosis patients with small-fibre neuropathy, should immunosuppressants or intravenous immunoglobulin be prescribed versus no treatment?
    • No recommendations were made for this PICO question due to a lack of sufficient evidence.

    PICO: Patients, Intervention, Comparison, Outcomes; FVC: forced vital capacity; QoL: quality of life.

    • TABLE 2

      Immunosuppressive therapies for sarcoidosis

      DrugUsual dosageMajor toxicitiesRecommended monitoringComments
      Prednisone/prednisoloneInitial 20 mg once a day; follow-up 5–10 mg once a day to once every other dayDiabetes; hypertension; weight gain; osteoporosis; cataracts; glaucoma; moodinessBone density; blood pressure and serum glucoseCumulative toxicity
      Methotrexate10–15 mg once a weekNausea; leukopenia; hepatotoxicity; pulmonaryCBC, hepatic, renal serum testingCleared by kidney, avoid in significant renal failure
      Leflunomide10–20 mg once a dayNausea; leukopenia; hepatotoxicity; pulmonaryCBC, hepatic, renal serum testingCleared by kidney, avoid in significant renal failure
      Azathioprine50–250 mg once a dayNausea; leukopenia; infections; malignancyCBC
      Mycophenolate mofetil500–1500 mg twice a dayDiarrhoea; leukopenia; infections; malignancyCBCLess experience in sarcoidosis than other agents
      Infliximab or biosimilars#3–5 mg·kg−1 initially, 2 weeks later, then once every 4–6 weeksInfections; allergic reactionScreen for prior TB; monitor for allergic reactions; contraindicated in severe CHF, prior malignancy, demyelinating neurologic disease, active TB, deep fungal infectionsAllergic reactions can be life threatening
      Adalimumab#40 mg every 1–2 weeksInfectionsScreen for prior TB; monitor for allergic reactions; contraindicated in severe CHF, prior malignancy, demyelinating neurologic disease, active TB, deep fungal infectionsLess toxic than infliximab
      Rituximab#500–1000 mg every 1–6 monthsInfectionsScreen for viral hepatitis; check IgG level with chronic therapyHigh risk for viral reactivation; can lead to IgG deficiency
      RCI#40–80 units twice a weekDiabetes; hypertension; oedema; anxietyMonitor glucose and blood pressureMost of toxicity is on day of injection
      Hydroxychloroquine200–400 mg once a dayLoss of visionOcular exams periodically depending on age and renal functionMinimal impact on cardiac and neurologic disease

      More details regarding dosages, major toxicities and monitoring are given in supplement S1 in the supplementary material and adapted from prior reports [4, 39–48]. CBC: complete blood count; TB: tuberculosis; CHF: congestive heart failure; RCI: repository corticotropin injection. #: use reserved for patients who have failed prior treatments with steroids and/or antimetabolites.

      • TABLE 3

        Outcomes for patient care and clinical research

        MeasureCategoryLevel
        Pulmonary sarcoidosisPatient wellbeingPhysician judgementImportant
        Clinical judgement of improvement, worsening/progressionPhysician judgementCritical
        Clinical judgement alone
        Treatment chest imaging: Scadding score [20], changes inTreatment imagingImportant
        Treatment chest imaging: Muers score [49], changes in
        PET/CT chest imaging, changes inScanImportant
        Pulmonary function tests: FVC, FEV1, FEV1/FVC, DLCO, SaO2Lung function testsCritical
        6-min walk distance [50]Exercise capacityImportant
        Quality of lifeQuality of lifeImportant
        SGRQ [51]
        Short Form-36 [52]
        Fatigue Assessment Scale [53]
        SAT Lung [54]
        KSQ General health [55]
        KSQ Lung health [55]
        Serious AEs; life-threatening AEsAEsCritical
        AEs leading to discontinuation
        Other AEs
        Extrapulmonary sarcoidosisPhysician global assessmentCutaneous sarcoidosis disease activityImportant
        SASI [56]
        CSAMI [57]
        Photographs
        Clinical judgement of improvement, worsening/progressionPhysician judgementCritical
        Skin measure of diseaseImportant
        Eye measure of diseaseCritical
        Kidney measure of diseaseImportant
        Löfgren syndrome measure of disease
        HypercalcaemiaCritical
        Quality of lifeQuality of lifeCritical
        Fatigue Assessment Scale
        SAT Skin [54]
        SAT Fatigue [54]
        KSQ Dermatology questionnaire
        Serious AEs; life-threatening AEsAEsCritical
        AEs leading to discontinuation
        Other AEs
        Cardiac sarcoidosisClinical judgement of improvement, worsening/progressionPhysician judgementCritical
        PET/CT chest imaging, changes inTreatment imagingCritical
        MRI chest imaging, changes in
        ArrythmiasArrythmiasCritical
        Quality of lifeQuality of lifeImportant
        Serious AEs; life-threatening AEsAEsCritical
        AEs leading to discontinuation
        Other AEs
        NeurosarcoidosisMeasures of neurologic diseasePhysician judgementCritical
        Clinical judgement of improvement, worsening/progression
        Quality of lifeQuality of lifeCritical
        Serious AE; life-threatening AEsAEsCritical
        AEs leading to discontinuation
        Other AEs
        All categoriesSteroid sparingSteroid sparingCritical

        PET: positron emission tomography; CT: computed tomography; FVC: forced vital capacity; FEV1: forced expiratory volume in 1 s; DLCO: diffusing capacity of the lung for carbon monoxide; SaO2: arterial oxygen saturation; SGRQ: St George's Respiratory Questionnaire; SAT: Sarcoidosis Assessment Tool; KSQ: King's Sarcoidosis Questionnaire; AE: adverse event; SASI: Sarcoidosis Activity and Severity Instrument; CSAMI: Cutaneous Sarcoidosis Activity and Morphology Instrument; MRI: magnetic resonance imaging.

        • TABLE 4

          Prognostic variables that may influence treatment decisions for cardiac sarcoidosis

          • Age >50 years
          • Left ventricular ejection fraction <40%
          • New York Heart Association Functional Class III or IV
          • Increased left ventricular end-diastolic diameter
          • Late gadolinium enhancement on cardiac magnetic resonance imaging
          • Ventricular tachycardia
          • Cardiac inflammation identified by fluorodeoxyglucose positron emission tomography scan
          • Echocardiographic evidence of abnormal global longitudinal strain
          • Interventricular septal thinning
          • Elevated troponin or brain natriuretic peptide

          Features found to be associated with increased risk for morbidity or mortality from cardiac sarcoidosis [150–159].

          Supplementary Materials

          • Figures
          • Tables
          • Supplementary Material

            Please note: supplementary material is not edited by the Editorial Office, and is uploaded as it has been supplied by the author.

            Supplement 1: Individual therapies ERJ-04079-2020.Supplement_1

            Supplement 2: Evidence summaries and evidence to decision tables for all PICOs ERJ-04079-2020.Supplement_2

          • Supplementary Material

            This one-page PDF can be shared freely online.

            Shareable PDF ERJ-04079-2020.Shareable

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          ERS clinical practice guidelines on treatment of sarcoidosis
          Robert P. Baughman, Dominique Valeyre, Peter Korsten, Alexander G. Mathioudakis, Wim A. Wuyts, Athol Wells, Paola Rottoli, Hiliaro Nunes, Elyse E. Lower, Marc A. Judson, Dominique Israel-Biet, Jan C. Grutters, Marjolein Drent, Daniel A. Culver, Francesco Bonella, Katerina Antoniou, Filippo Martone, Bernd Quadder, Ginger Spitzer, Blin Nagavci, Thomy Tonia, David Rigau, Daniel R. Ouellette
          European Respiratory Journal Dec 2021, 58 (6) 2004079; DOI: 10.1183/13993003.04079-2020

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          ERS clinical practice guidelines on treatment of sarcoidosis
          Robert P. Baughman, Dominique Valeyre, Peter Korsten, Alexander G. Mathioudakis, Wim A. Wuyts, Athol Wells, Paola Rottoli, Hiliaro Nunes, Elyse E. Lower, Marc A. Judson, Dominique Israel-Biet, Jan C. Grutters, Marjolein Drent, Daniel A. Culver, Francesco Bonella, Katerina Antoniou, Filippo Martone, Bernd Quadder, Ginger Spitzer, Blin Nagavci, Thomy Tonia, David Rigau, Daniel R. Ouellette
          European Respiratory Journal Dec 2021, 58 (6) 2004079; DOI: 10.1183/13993003.04079-2020
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          • Article
            • Abstract
            • Abstract
            • Introduction
            • Methodology
            • Pulmonary sarcoidosis
            • Cutaneous sarcoidosis
            • Cardiac sarcoidosis
            • Neurologic disease
            • Fatigue
            • Small-fibre neuropathy
            • Discussion
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