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January 14, 2020; 94 (2) Article

Hashimoto encephalopathy in the 21st century

View ORCID ProfileSimone Mattozzi, Lidia Sabater, Domingo Escudero, Helena Ariño, Thais Armangue, Mateus Simabukuro, Takahiro Iizuka, Makoto Hara, Albert Saiz, Stefano Sotgiu, Josep Dalmau, Francesc Graus
First published December 27, 2019, DOI: https://doi.org/10.1212/WNL.0000000000008785
Simone Mattozzi
From the Neuroimmunology Program (S.M., L.S., H.A., T.A., A.S., J.D., F.G.), Institut d'Investigació Biomèdica August Pi i Sunyer, Barcelona, Spain; Department of Medical, Surgical and Experimental Medicine (S.M., S.S.), University of Sassari, Italy; Service of Neurology (D.E., A.S.), Hospital Clinic, and Pediatric Neuroimmunology Unit (T.A.), Neurology Department, Sant Joan de Déu Children's Hospital, University of Barcelona, Spain; Neurology Division (M.S.), Hospital das Clínicas, São Paulo University, Brazil; Department of Neurology (T.I.), Kitasato University School of Medicine, Sagamihara; Division of Neurology (M.H.), Department of Medicine, Nihon University School of Medicine, Tokyo, Japan; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia; and Institució Catalana de Recerca i Estudis Avançats (J.D.), Barcelona, Spain.
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Lidia Sabater
From the Neuroimmunology Program (S.M., L.S., H.A., T.A., A.S., J.D., F.G.), Institut d'Investigació Biomèdica August Pi i Sunyer, Barcelona, Spain; Department of Medical, Surgical and Experimental Medicine (S.M., S.S.), University of Sassari, Italy; Service of Neurology (D.E., A.S.), Hospital Clinic, and Pediatric Neuroimmunology Unit (T.A.), Neurology Department, Sant Joan de Déu Children's Hospital, University of Barcelona, Spain; Neurology Division (M.S.), Hospital das Clínicas, São Paulo University, Brazil; Department of Neurology (T.I.), Kitasato University School of Medicine, Sagamihara; Division of Neurology (M.H.), Department of Medicine, Nihon University School of Medicine, Tokyo, Japan; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia; and Institució Catalana de Recerca i Estudis Avançats (J.D.), Barcelona, Spain.
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Domingo Escudero
From the Neuroimmunology Program (S.M., L.S., H.A., T.A., A.S., J.D., F.G.), Institut d'Investigació Biomèdica August Pi i Sunyer, Barcelona, Spain; Department of Medical, Surgical and Experimental Medicine (S.M., S.S.), University of Sassari, Italy; Service of Neurology (D.E., A.S.), Hospital Clinic, and Pediatric Neuroimmunology Unit (T.A.), Neurology Department, Sant Joan de Déu Children's Hospital, University of Barcelona, Spain; Neurology Division (M.S.), Hospital das Clínicas, São Paulo University, Brazil; Department of Neurology (T.I.), Kitasato University School of Medicine, Sagamihara; Division of Neurology (M.H.), Department of Medicine, Nihon University School of Medicine, Tokyo, Japan; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia; and Institució Catalana de Recerca i Estudis Avançats (J.D.), Barcelona, Spain.
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Helena Ariño
From the Neuroimmunology Program (S.M., L.S., H.A., T.A., A.S., J.D., F.G.), Institut d'Investigació Biomèdica August Pi i Sunyer, Barcelona, Spain; Department of Medical, Surgical and Experimental Medicine (S.M., S.S.), University of Sassari, Italy; Service of Neurology (D.E., A.S.), Hospital Clinic, and Pediatric Neuroimmunology Unit (T.A.), Neurology Department, Sant Joan de Déu Children's Hospital, University of Barcelona, Spain; Neurology Division (M.S.), Hospital das Clínicas, São Paulo University, Brazil; Department of Neurology (T.I.), Kitasato University School of Medicine, Sagamihara; Division of Neurology (M.H.), Department of Medicine, Nihon University School of Medicine, Tokyo, Japan; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia; and Institució Catalana de Recerca i Estudis Avançats (J.D.), Barcelona, Spain.
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Thais Armangue
From the Neuroimmunology Program (S.M., L.S., H.A., T.A., A.S., J.D., F.G.), Institut d'Investigació Biomèdica August Pi i Sunyer, Barcelona, Spain; Department of Medical, Surgical and Experimental Medicine (S.M., S.S.), University of Sassari, Italy; Service of Neurology (D.E., A.S.), Hospital Clinic, and Pediatric Neuroimmunology Unit (T.A.), Neurology Department, Sant Joan de Déu Children's Hospital, University of Barcelona, Spain; Neurology Division (M.S.), Hospital das Clínicas, São Paulo University, Brazil; Department of Neurology (T.I.), Kitasato University School of Medicine, Sagamihara; Division of Neurology (M.H.), Department of Medicine, Nihon University School of Medicine, Tokyo, Japan; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia; and Institució Catalana de Recerca i Estudis Avançats (J.D.), Barcelona, Spain.
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Mateus Simabukuro
From the Neuroimmunology Program (S.M., L.S., H.A., T.A., A.S., J.D., F.G.), Institut d'Investigació Biomèdica August Pi i Sunyer, Barcelona, Spain; Department of Medical, Surgical and Experimental Medicine (S.M., S.S.), University of Sassari, Italy; Service of Neurology (D.E., A.S.), Hospital Clinic, and Pediatric Neuroimmunology Unit (T.A.), Neurology Department, Sant Joan de Déu Children's Hospital, University of Barcelona, Spain; Neurology Division (M.S.), Hospital das Clínicas, São Paulo University, Brazil; Department of Neurology (T.I.), Kitasato University School of Medicine, Sagamihara; Division of Neurology (M.H.), Department of Medicine, Nihon University School of Medicine, Tokyo, Japan; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia; and Institució Catalana de Recerca i Estudis Avançats (J.D.), Barcelona, Spain.
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Takahiro Iizuka
From the Neuroimmunology Program (S.M., L.S., H.A., T.A., A.S., J.D., F.G.), Institut d'Investigació Biomèdica August Pi i Sunyer, Barcelona, Spain; Department of Medical, Surgical and Experimental Medicine (S.M., S.S.), University of Sassari, Italy; Service of Neurology (D.E., A.S.), Hospital Clinic, and Pediatric Neuroimmunology Unit (T.A.), Neurology Department, Sant Joan de Déu Children's Hospital, University of Barcelona, Spain; Neurology Division (M.S.), Hospital das Clínicas, São Paulo University, Brazil; Department of Neurology (T.I.), Kitasato University School of Medicine, Sagamihara; Division of Neurology (M.H.), Department of Medicine, Nihon University School of Medicine, Tokyo, Japan; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia; and Institució Catalana de Recerca i Estudis Avançats (J.D.), Barcelona, Spain.
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Makoto Hara
From the Neuroimmunology Program (S.M., L.S., H.A., T.A., A.S., J.D., F.G.), Institut d'Investigació Biomèdica August Pi i Sunyer, Barcelona, Spain; Department of Medical, Surgical and Experimental Medicine (S.M., S.S.), University of Sassari, Italy; Service of Neurology (D.E., A.S.), Hospital Clinic, and Pediatric Neuroimmunology Unit (T.A.), Neurology Department, Sant Joan de Déu Children's Hospital, University of Barcelona, Spain; Neurology Division (M.S.), Hospital das Clínicas, São Paulo University, Brazil; Department of Neurology (T.I.), Kitasato University School of Medicine, Sagamihara; Division of Neurology (M.H.), Department of Medicine, Nihon University School of Medicine, Tokyo, Japan; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia; and Institució Catalana de Recerca i Estudis Avançats (J.D.), Barcelona, Spain.
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Albert Saiz
From the Neuroimmunology Program (S.M., L.S., H.A., T.A., A.S., J.D., F.G.), Institut d'Investigació Biomèdica August Pi i Sunyer, Barcelona, Spain; Department of Medical, Surgical and Experimental Medicine (S.M., S.S.), University of Sassari, Italy; Service of Neurology (D.E., A.S.), Hospital Clinic, and Pediatric Neuroimmunology Unit (T.A.), Neurology Department, Sant Joan de Déu Children's Hospital, University of Barcelona, Spain; Neurology Division (M.S.), Hospital das Clínicas, São Paulo University, Brazil; Department of Neurology (T.I.), Kitasato University School of Medicine, Sagamihara; Division of Neurology (M.H.), Department of Medicine, Nihon University School of Medicine, Tokyo, Japan; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia; and Institució Catalana de Recerca i Estudis Avançats (J.D.), Barcelona, Spain.
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Stefano Sotgiu
From the Neuroimmunology Program (S.M., L.S., H.A., T.A., A.S., J.D., F.G.), Institut d'Investigació Biomèdica August Pi i Sunyer, Barcelona, Spain; Department of Medical, Surgical and Experimental Medicine (S.M., S.S.), University of Sassari, Italy; Service of Neurology (D.E., A.S.), Hospital Clinic, and Pediatric Neuroimmunology Unit (T.A.), Neurology Department, Sant Joan de Déu Children's Hospital, University of Barcelona, Spain; Neurology Division (M.S.), Hospital das Clínicas, São Paulo University, Brazil; Department of Neurology (T.I.), Kitasato University School of Medicine, Sagamihara; Division of Neurology (M.H.), Department of Medicine, Nihon University School of Medicine, Tokyo, Japan; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia; and Institució Catalana de Recerca i Estudis Avançats (J.D.), Barcelona, Spain.
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Josep Dalmau
From the Neuroimmunology Program (S.M., L.S., H.A., T.A., A.S., J.D., F.G.), Institut d'Investigació Biomèdica August Pi i Sunyer, Barcelona, Spain; Department of Medical, Surgical and Experimental Medicine (S.M., S.S.), University of Sassari, Italy; Service of Neurology (D.E., A.S.), Hospital Clinic, and Pediatric Neuroimmunology Unit (T.A.), Neurology Department, Sant Joan de Déu Children's Hospital, University of Barcelona, Spain; Neurology Division (M.S.), Hospital das Clínicas, São Paulo University, Brazil; Department of Neurology (T.I.), Kitasato University School of Medicine, Sagamihara; Division of Neurology (M.H.), Department of Medicine, Nihon University School of Medicine, Tokyo, Japan; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia; and Institució Catalana de Recerca i Estudis Avançats (J.D.), Barcelona, Spain.
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Francesc Graus
From the Neuroimmunology Program (S.M., L.S., H.A., T.A., A.S., J.D., F.G.), Institut d'Investigació Biomèdica August Pi i Sunyer, Barcelona, Spain; Department of Medical, Surgical and Experimental Medicine (S.M., S.S.), University of Sassari, Italy; Service of Neurology (D.E., A.S.), Hospital Clinic, and Pediatric Neuroimmunology Unit (T.A.), Neurology Department, Sant Joan de Déu Children's Hospital, University of Barcelona, Spain; Neurology Division (M.S.), Hospital das Clínicas, São Paulo University, Brazil; Department of Neurology (T.I.), Kitasato University School of Medicine, Sagamihara; Division of Neurology (M.H.), Department of Medicine, Nihon University School of Medicine, Tokyo, Japan; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia; and Institució Catalana de Recerca i Estudis Avançats (J.D.), Barcelona, Spain.
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Citation
Hashimoto encephalopathy in the 21st century
Simone Mattozzi, Lidia Sabater, Domingo Escudero, Helena Ariño, Thais Armangue, Mateus Simabukuro, Takahiro Iizuka, Makoto Hara, Albert Saiz, Stefano Sotgiu, Josep Dalmau, Francesc Graus
Neurology Jan 2020, 94 (2) e217-e224; DOI: 10.1212/WNL.0000000000008785

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Abstract

Objective To report the presenting syndromes and to determine whether pretreatment criteria of Hashimoto encephalopathy (HE) predict response to steroids.

Methods We assessed symptoms and steroid responsiveness in 24 patients with pretreatment criteria of HE, including (1) subacute onset of cognitive impairment, psychiatric symptoms, or seizures; (2) euthyroid status or mild hypothyroidism; (3) serum thyroid peroxidase antibodies (TPOAb) >200 IU/mL; (4) absent neuronal antibodies in serum/CSF; and (5) no other etiologies. Additional studies included determination of TPOAb (>200 IU/mL) in 74 patients with criteria of possible autoimmune encephalitis (AE) without neuronal antibodies and 205 patients with different neuroimmunologic diseases, psychosis, or new-onset refractory status epilepticus (NORSE). Serum antibodies to the amino (ΝΗ2)-terminal of α-enolase (NH2-α-enolaseAb) were examined in the indicated 24 patients and 13 controls.

Results The 24 patients (14 women) with suspected HE had a median age of 48 years (range 8–79 years). Four syndromes were identified: psychiatric (7, 29%), encephalopathy (7, 29%), NORSE-like (6, 25%), and limbic encephalitis (4, 17%). Only 6 of 19 (31.6%) patients completely responded to steroids. The frequency of TPOAb in the 74 patients with possible AE (6 of 74, 8.1%) was similar to that of the 205 controls (17 of 205, 8.2%; p = 0.84). NH2-α-enolaseAb were identified in 1 of 24 suspected HE cases and 1 of 13 controls.

Conclusion Current pretreatment criteria of HE do not predict steroid responsiveness. The detection of TPOAb across all control groups reveals their poor disease-specificity. NH2-α-enolaseAb did not help in the diagnosis of HE. These findings imply a redefinition of HE that requires a systematic exclusion of antibody-mediated encephalitis.

Glossary

AE=
autoimmune encephalitis;
HE=
Hashimoto encephalopathy;
IVIG=
IV immunoglobulin;
LE=
limbic encephalitis;
NORSE=
new-onset refractory status epilepticus;
TPOAb=
thyroid peroxidase antibodies

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Editorial, page 55

  • Podcast: NPub.org/w0glpg

  • Received April 29, 2019.
  • Accepted in final form August 2, 2019.
  • © 2019 American Academy of Neurology
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Letters: Rapid online correspondence

  • Author response: Hashimoto encephalopathy in the 21st century
    • Francesc Graus, Emeritus professor, Institut d'Investigació Biomèdica August Pi i Sunyer(IDIBAPS) (Barcelona, Spain)
    • Josep O. Dalmau, Director, Neuroimmunology laboratory, Institut d'Investigació Biomèdica August Pi i Sunyer(IDIBAPS) (Barcelona, Spain)
    Submitted September 18, 2020
  • Reader response: Hashimoto encephalopathy in the 21st century
    • Makoto Yoneda, Dean and Professor, Faculty of Nursing and Social Welfare Sciences, Fukui Prefectural University (Fukui, Japan)
    • Akiko Matsunaga, Staff, Faculty of Nursing and Social Welfare Sciences, Fukui Prefectural University (Fukui, Japan)
    • Masamichi Ikawa, Senior Assistant Professor, Department of Advanced Medicine for Community Healthcare, Faculty of Medical Sciences, University of Fukui (Fukui, Japan)
    Submitted September 10, 2020
  • Author response: Hashimoto encephalopathy in the 21st century
    • Francesc Graus, MD, Neuroimmunology Program, Institut d’Investigació Biomèdica August Pi i Sunyer (IDIBAPS) (Barcelona, Spain)
    • Josep Dalmau, MD, Neuroimmunology Program, Institut d’Investigació Biomèdica August Pi i Sunyer (IDIBAPS) (Barcelona, Spain)
    Submitted January 29, 2020
  • Reader response: Hashimoto encephalopathy in the 21st century
    • Khichar Shubhakaran, Professor and Head Neurology, Dr. S.N. Medical College (Jodhpur, India)
    Submitted January 17, 2020
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