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June 2015; 2 (3) ArticleOpen Access

Clinical course and treatment of anti-HMGCR antibody–associated necrotizing autoimmune myopathy

Sudarshini Ramanathan, Daman Langguth, Todd A. Hardy, Nidhi Garg, Chris Bundell, Arada Rojana-Udomsart, Russell C. Dale, Thomas Robertson, Andrew L. Mammen, Stephen W. Reddel
First published April 2, 2015, DOI: https://doi.org/10.1212/NXI.0000000000000096
Sudarshini Ramanathan
From the Department of Neurology (S.R., T.A.H., N.G., S.W.R.), Concord Repatriation General Hospital, Sydney, New South Wales, Australia; Neuroimmunology Group (S.R., R.C.D.), Institute for Neuroscience and Muscle Research, The Kids Research Institute at the Children's Hospital at Westmead, Sydney Medical School, University of Sydney, New South Wales, Australia; Department of Neurology (S.R.), Westmead Hospital, Sydney, New South Wales, Australia; Sullivan Nicolaides Pathology (D.L.), Brisbane, Queensland, Australia; Concord Clinical School (T.A.H., S.W.R.), University of Sydney, New South Wales, Australia; Clinical Immunology (C.B.), PathWest, QEII Medical Center, Nedlands, Western Australia, Australia; School of Pathology and Laboratory Medicine (C.B.), University of Western Australia, Nedlands, Western Australia, Australia; Australian Neuro-Muscular Research Institute (ANRI) and Centre for Neuromuscular and Neurological Disorders (CNND) (A.R.-U.), University of Western Australia, QEII Medical Centre, Nedlands, Western Australia, Australia; Pathology Queensland (T.R.), Royal Brisbane & Women's Hospital, Brisbane, Queensland, Australia; and National Institute of Arthritis and Musculoskeletal and Skin Diseases (A.L.M.), National Institutes of Health, Bethesda, MD.
FRACP
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Daman Langguth
From the Department of Neurology (S.R., T.A.H., N.G., S.W.R.), Concord Repatriation General Hospital, Sydney, New South Wales, Australia; Neuroimmunology Group (S.R., R.C.D.), Institute for Neuroscience and Muscle Research, The Kids Research Institute at the Children's Hospital at Westmead, Sydney Medical School, University of Sydney, New South Wales, Australia; Department of Neurology (S.R.), Westmead Hospital, Sydney, New South Wales, Australia; Sullivan Nicolaides Pathology (D.L.), Brisbane, Queensland, Australia; Concord Clinical School (T.A.H., S.W.R.), University of Sydney, New South Wales, Australia; Clinical Immunology (C.B.), PathWest, QEII Medical Center, Nedlands, Western Australia, Australia; School of Pathology and Laboratory Medicine (C.B.), University of Western Australia, Nedlands, Western Australia, Australia; Australian Neuro-Muscular Research Institute (ANRI) and Centre for Neuromuscular and Neurological Disorders (CNND) (A.R.-U.), University of Western Australia, QEII Medical Centre, Nedlands, Western Australia, Australia; Pathology Queensland (T.R.), Royal Brisbane & Women's Hospital, Brisbane, Queensland, Australia; and National Institute of Arthritis and Musculoskeletal and Skin Diseases (A.L.M.), National Institutes of Health, Bethesda, MD.
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Todd A. Hardy
From the Department of Neurology (S.R., T.A.H., N.G., S.W.R.), Concord Repatriation General Hospital, Sydney, New South Wales, Australia; Neuroimmunology Group (S.R., R.C.D.), Institute for Neuroscience and Muscle Research, The Kids Research Institute at the Children's Hospital at Westmead, Sydney Medical School, University of Sydney, New South Wales, Australia; Department of Neurology (S.R.), Westmead Hospital, Sydney, New South Wales, Australia; Sullivan Nicolaides Pathology (D.L.), Brisbane, Queensland, Australia; Concord Clinical School (T.A.H., S.W.R.), University of Sydney, New South Wales, Australia; Clinical Immunology (C.B.), PathWest, QEII Medical Center, Nedlands, Western Australia, Australia; School of Pathology and Laboratory Medicine (C.B.), University of Western Australia, Nedlands, Western Australia, Australia; Australian Neuro-Muscular Research Institute (ANRI) and Centre for Neuromuscular and Neurological Disorders (CNND) (A.R.-U.), University of Western Australia, QEII Medical Centre, Nedlands, Western Australia, Australia; Pathology Queensland (T.R.), Royal Brisbane & Women's Hospital, Brisbane, Queensland, Australia; and National Institute of Arthritis and Musculoskeletal and Skin Diseases (A.L.M.), National Institutes of Health, Bethesda, MD.
FRACP, PhD
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Nidhi Garg
From the Department of Neurology (S.R., T.A.H., N.G., S.W.R.), Concord Repatriation General Hospital, Sydney, New South Wales, Australia; Neuroimmunology Group (S.R., R.C.D.), Institute for Neuroscience and Muscle Research, The Kids Research Institute at the Children's Hospital at Westmead, Sydney Medical School, University of Sydney, New South Wales, Australia; Department of Neurology (S.R.), Westmead Hospital, Sydney, New South Wales, Australia; Sullivan Nicolaides Pathology (D.L.), Brisbane, Queensland, Australia; Concord Clinical School (T.A.H., S.W.R.), University of Sydney, New South Wales, Australia; Clinical Immunology (C.B.), PathWest, QEII Medical Center, Nedlands, Western Australia, Australia; School of Pathology and Laboratory Medicine (C.B.), University of Western Australia, Nedlands, Western Australia, Australia; Australian Neuro-Muscular Research Institute (ANRI) and Centre for Neuromuscular and Neurological Disorders (CNND) (A.R.-U.), University of Western Australia, QEII Medical Centre, Nedlands, Western Australia, Australia; Pathology Queensland (T.R.), Royal Brisbane & Women's Hospital, Brisbane, Queensland, Australia; and National Institute of Arthritis and Musculoskeletal and Skin Diseases (A.L.M.), National Institutes of Health, Bethesda, MD.
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Chris Bundell
From the Department of Neurology (S.R., T.A.H., N.G., S.W.R.), Concord Repatriation General Hospital, Sydney, New South Wales, Australia; Neuroimmunology Group (S.R., R.C.D.), Institute for Neuroscience and Muscle Research, The Kids Research Institute at the Children's Hospital at Westmead, Sydney Medical School, University of Sydney, New South Wales, Australia; Department of Neurology (S.R.), Westmead Hospital, Sydney, New South Wales, Australia; Sullivan Nicolaides Pathology (D.L.), Brisbane, Queensland, Australia; Concord Clinical School (T.A.H., S.W.R.), University of Sydney, New South Wales, Australia; Clinical Immunology (C.B.), PathWest, QEII Medical Center, Nedlands, Western Australia, Australia; School of Pathology and Laboratory Medicine (C.B.), University of Western Australia, Nedlands, Western Australia, Australia; Australian Neuro-Muscular Research Institute (ANRI) and Centre for Neuromuscular and Neurological Disorders (CNND) (A.R.-U.), University of Western Australia, QEII Medical Centre, Nedlands, Western Australia, Australia; Pathology Queensland (T.R.), Royal Brisbane & Women's Hospital, Brisbane, Queensland, Australia; and National Institute of Arthritis and Musculoskeletal and Skin Diseases (A.L.M.), National Institutes of Health, Bethesda, MD.
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Arada Rojana-Udomsart
From the Department of Neurology (S.R., T.A.H., N.G., S.W.R.), Concord Repatriation General Hospital, Sydney, New South Wales, Australia; Neuroimmunology Group (S.R., R.C.D.), Institute for Neuroscience and Muscle Research, The Kids Research Institute at the Children's Hospital at Westmead, Sydney Medical School, University of Sydney, New South Wales, Australia; Department of Neurology (S.R.), Westmead Hospital, Sydney, New South Wales, Australia; Sullivan Nicolaides Pathology (D.L.), Brisbane, Queensland, Australia; Concord Clinical School (T.A.H., S.W.R.), University of Sydney, New South Wales, Australia; Clinical Immunology (C.B.), PathWest, QEII Medical Center, Nedlands, Western Australia, Australia; School of Pathology and Laboratory Medicine (C.B.), University of Western Australia, Nedlands, Western Australia, Australia; Australian Neuro-Muscular Research Institute (ANRI) and Centre for Neuromuscular and Neurological Disorders (CNND) (A.R.-U.), University of Western Australia, QEII Medical Centre, Nedlands, Western Australia, Australia; Pathology Queensland (T.R.), Royal Brisbane & Women's Hospital, Brisbane, Queensland, Australia; and National Institute of Arthritis and Musculoskeletal and Skin Diseases (A.L.M.), National Institutes of Health, Bethesda, MD.
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Russell C. Dale
From the Department of Neurology (S.R., T.A.H., N.G., S.W.R.), Concord Repatriation General Hospital, Sydney, New South Wales, Australia; Neuroimmunology Group (S.R., R.C.D.), Institute for Neuroscience and Muscle Research, The Kids Research Institute at the Children's Hospital at Westmead, Sydney Medical School, University of Sydney, New South Wales, Australia; Department of Neurology (S.R.), Westmead Hospital, Sydney, New South Wales, Australia; Sullivan Nicolaides Pathology (D.L.), Brisbane, Queensland, Australia; Concord Clinical School (T.A.H., S.W.R.), University of Sydney, New South Wales, Australia; Clinical Immunology (C.B.), PathWest, QEII Medical Center, Nedlands, Western Australia, Australia; School of Pathology and Laboratory Medicine (C.B.), University of Western Australia, Nedlands, Western Australia, Australia; Australian Neuro-Muscular Research Institute (ANRI) and Centre for Neuromuscular and Neurological Disorders (CNND) (A.R.-U.), University of Western Australia, QEII Medical Centre, Nedlands, Western Australia, Australia; Pathology Queensland (T.R.), Royal Brisbane & Women's Hospital, Brisbane, Queensland, Australia; and National Institute of Arthritis and Musculoskeletal and Skin Diseases (A.L.M.), National Institutes of Health, Bethesda, MD.
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Thomas Robertson
From the Department of Neurology (S.R., T.A.H., N.G., S.W.R.), Concord Repatriation General Hospital, Sydney, New South Wales, Australia; Neuroimmunology Group (S.R., R.C.D.), Institute for Neuroscience and Muscle Research, The Kids Research Institute at the Children's Hospital at Westmead, Sydney Medical School, University of Sydney, New South Wales, Australia; Department of Neurology (S.R.), Westmead Hospital, Sydney, New South Wales, Australia; Sullivan Nicolaides Pathology (D.L.), Brisbane, Queensland, Australia; Concord Clinical School (T.A.H., S.W.R.), University of Sydney, New South Wales, Australia; Clinical Immunology (C.B.), PathWest, QEII Medical Center, Nedlands, Western Australia, Australia; School of Pathology and Laboratory Medicine (C.B.), University of Western Australia, Nedlands, Western Australia, Australia; Australian Neuro-Muscular Research Institute (ANRI) and Centre for Neuromuscular and Neurological Disorders (CNND) (A.R.-U.), University of Western Australia, QEII Medical Centre, Nedlands, Western Australia, Australia; Pathology Queensland (T.R.), Royal Brisbane & Women's Hospital, Brisbane, Queensland, Australia; and National Institute of Arthritis and Musculoskeletal and Skin Diseases (A.L.M.), National Institutes of Health, Bethesda, MD.
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Andrew L. Mammen
From the Department of Neurology (S.R., T.A.H., N.G., S.W.R.), Concord Repatriation General Hospital, Sydney, New South Wales, Australia; Neuroimmunology Group (S.R., R.C.D.), Institute for Neuroscience and Muscle Research, The Kids Research Institute at the Children's Hospital at Westmead, Sydney Medical School, University of Sydney, New South Wales, Australia; Department of Neurology (S.R.), Westmead Hospital, Sydney, New South Wales, Australia; Sullivan Nicolaides Pathology (D.L.), Brisbane, Queensland, Australia; Concord Clinical School (T.A.H., S.W.R.), University of Sydney, New South Wales, Australia; Clinical Immunology (C.B.), PathWest, QEII Medical Center, Nedlands, Western Australia, Australia; School of Pathology and Laboratory Medicine (C.B.), University of Western Australia, Nedlands, Western Australia, Australia; Australian Neuro-Muscular Research Institute (ANRI) and Centre for Neuromuscular and Neurological Disorders (CNND) (A.R.-U.), University of Western Australia, QEII Medical Centre, Nedlands, Western Australia, Australia; Pathology Queensland (T.R.), Royal Brisbane & Women's Hospital, Brisbane, Queensland, Australia; and National Institute of Arthritis and Musculoskeletal and Skin Diseases (A.L.M.), National Institutes of Health, Bethesda, MD.
MD, PhD
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Stephen W. Reddel
From the Department of Neurology (S.R., T.A.H., N.G., S.W.R.), Concord Repatriation General Hospital, Sydney, New South Wales, Australia; Neuroimmunology Group (S.R., R.C.D.), Institute for Neuroscience and Muscle Research, The Kids Research Institute at the Children's Hospital at Westmead, Sydney Medical School, University of Sydney, New South Wales, Australia; Department of Neurology (S.R.), Westmead Hospital, Sydney, New South Wales, Australia; Sullivan Nicolaides Pathology (D.L.), Brisbane, Queensland, Australia; Concord Clinical School (T.A.H., S.W.R.), University of Sydney, New South Wales, Australia; Clinical Immunology (C.B.), PathWest, QEII Medical Center, Nedlands, Western Australia, Australia; School of Pathology and Laboratory Medicine (C.B.), University of Western Australia, Nedlands, Western Australia, Australia; Australian Neuro-Muscular Research Institute (ANRI) and Centre for Neuromuscular and Neurological Disorders (CNND) (A.R.-U.), University of Western Australia, QEII Medical Centre, Nedlands, Western Australia, Australia; Pathology Queensland (T.R.), Royal Brisbane & Women's Hospital, Brisbane, Queensland, Australia; and National Institute of Arthritis and Musculoskeletal and Skin Diseases (A.L.M.), National Institutes of Health, Bethesda, MD.
FRACP, PhD
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Citation
Clinical course and treatment of anti-HMGCR antibody–associated necrotizing autoimmune myopathy
Sudarshini Ramanathan, Daman Langguth, Todd A. Hardy, Nidhi Garg, Chris Bundell, Arada Rojana-Udomsart, Russell C. Dale, Thomas Robertson, Andrew L. Mammen, Stephen W. Reddel
Neurol Neuroimmunol Neuroinflamm Jun 2015, 2 (3) e96; DOI: 10.1212/NXI.0000000000000096

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    Figure 1 Muscle biopsy images demonstrating a pauci-immune necrotizing autoimmune myopathy in illustrative cases 1 and 2

    (A–D) Case 1 deltoid muscle. (A) Frozen section showing scattered necrotic fibers with associated macrophage infiltration but no discernible lymphocytic infiltration (arrow) (hematoxylin & eosin [H&E] stain, magnification 100×). (B) Immunohistochemistry for major histocompatibility complex class I highlights macrophages associated with muscle fiber necrosis and background capillaries, but there is no generalized upregulation on uninvolved muscle fibers in this biopsy sample (arrow) (magnification 100×). (C) Immunohistochemistry for complement membrane attack complex highlights foci of muscle fiber necrosis, but there is no microvascular deposition (arrow) (magnification 100×). (D) Immunohistochemistry for CD3 reveals a paucity of T cells in areas of fiber degeneration. (E, F) Case 2 deltoid muscle. (E) H&E stain (magnification 40×). (F) H&E stain (magnification 100×). There are necrotic fibers with inflammatory cells (arrow) involved in the process of myophagocytosis and a few regenerating fibers, consistent with a pauci-immune necrotizing myopathy.

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    Figure 2 Clinical course and response to therapy in 6 Australian patients with HMGCR antibodies

    The clinical course, creatine kinase (CK) levels, Medical Research Council (MRC) scale for power grading of shoulder abduction strength (appendix e-1 at Neurology.org/nn), and therapeutic regimens in the 6 patients in this cohort are graphically represented. Timing of statin commencement and cessation are indicated. Horizontal arrows indicate the duration of use of various immunosuppressive therapies. All patients were asymptomatic with no reported weakness at the time of statin commencement based on assessment by their general practitioner. Most patients experienced relapses with attempts to wean steroids, with a rise in CK often preceding clinical weakness. (A) Illustrative case 1 (case 1, table). The CK levels of this 60-year-old man are graphed from the time of statin commencement through 93 months of follow-up. Acute relapses characterized by worsening proximal weakness and coinciding with a rise in CK accompanied attempts to wean the dose of oral prednisone below 10 mg daily. Reinstitution of steroids and the use of IV immunoglobulin (IVIg) had a good correlation with clinical improvement and a reduction in CK. (B) Illustrative case 2 (case 2, table). The CK levels of this 73-year-old woman are shown for 30 months of follow-up. Early recognition of this diagnosis and initiation of high-dose prednisone and methotrexate (MTX) resulted in a rapid improvement in CK and clinical resolution of weakness. A slow and cautious approach to weaning steroids was associated with clinical remission without any relapses, and maintenance immunosuppression with prednisone 5 mg once daily and MTX 20 mg weekly has resulted in clinical stabilization. (C) Case 3, table. This 66-year-old woman was on a statin for 24 months prior to symptom onset. Early treatment with statin cessation and high-dose steroids resulted in an immediate improvement, but rapid steroid tapering prompted a severe relapse necessitating respiratory support and multiple immunosuppressive agents to allow for clinical stabilization. (D) Case 4, table. This 74-year-old woman responded well to steroid therapy, but attempts to wean steroids prompted relapses associated with both a CK rise and clinical weakness. Maintenance therapy with prednisone and IVIg has allowed for clinical remission. (E) Case 5, table. This 77-year-old man was on a statin for 1 year prior to symptom onset. Initial therapy with steroids, IVIg, and MTX allowed for an early recovery. However, a rechallenge with statin therapy prompted a further relapse. This patient required multiple immunosuppressive agents to maintain remission, with attempts to wean prednisone below 15 mg prompting 2 further relapses and ongoing disease activity almost 11 years after statin cessation. Maintenance therapy with prednisone and IVIg has permitted clinical remission. (F) Case 6, table. This 69-year-old man was on a statin for 2.5 years prior to symptom onset. He responded well to treatment with prednisone, IVIg, and MTX. Steroids were weaned due to his significant vascular comorbidities, and he was maintained on MTX. Recent results herald a possible early relapse, with CK levels trending up and mild clinical weakness, suggesting reinstitution of steroid therapy may be required. HMGCR = 3-hydroxy-3-methylglutaryl-coenzyme A reductase; IV MP = IV methylprednisolone; PE = plasmapheresis.

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