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March 2023; 10 (2) Research ArticleOpen Access

Comparison of Structural Changes in Nodding Syndrome and Other Epilepsies Associated With Onchocerca volvulus

Rajarshi Mazumder, Samson Kamya Lubowa, Noriko Salamon, View ORCID ProfileNicholas J. Jackson, Michael Kawooya, Pamela Rosemary Akun, Ronald Anguzu, Rodney J. Ogwang, Joseph Kubofcik, View ORCID ProfileThomas Nutman, Kevin Marsh, Charles Newton, Angela Vincent, View ORCID ProfileRichard Idro
First published December 21, 2022, DOI: https://doi.org/10.1212/NXI.0000000000200074
Rajarshi Mazumder
From the Department of Neurology (R.M.), David Geffen School of Medicine at University of California Los Angeles; Kampala MRI Centre (S.K.L., M.K.), Uganda; Department of Radiological Sciences (N.S.), David Geffen School of Medicine, University of California Los Angeles, CA; Division of General Internal Medicine and Health Services Research (N.J.J.), David Geffen School of Medicine at UCLA; Centre of Tropical Neuroscience (P.R.A., R.A., R.I.), Kitgum Site, Uganda; Makerere University (R.A., R.J.O., R.I.), College of Health Sciences, Kampala, Uganda; Laboratory of Parasitic Diseases (J.K., T.N.), National Institutes of Health, Bethesda, MD; Centre for Tropical Medicine and Global Health (K.M., R.I.), Nuffield Department of Medicine, University of Oxford, United Kingdom; Department of Psychiatry (C.N.), University of Oxford, United Kingdom; and Nuffield Department of Clinical Neurosciences (A.V.), University of Oxford, United Kingdom.
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Samson Kamya Lubowa
From the Department of Neurology (R.M.), David Geffen School of Medicine at University of California Los Angeles; Kampala MRI Centre (S.K.L., M.K.), Uganda; Department of Radiological Sciences (N.S.), David Geffen School of Medicine, University of California Los Angeles, CA; Division of General Internal Medicine and Health Services Research (N.J.J.), David Geffen School of Medicine at UCLA; Centre of Tropical Neuroscience (P.R.A., R.A., R.I.), Kitgum Site, Uganda; Makerere University (R.A., R.J.O., R.I.), College of Health Sciences, Kampala, Uganda; Laboratory of Parasitic Diseases (J.K., T.N.), National Institutes of Health, Bethesda, MD; Centre for Tropical Medicine and Global Health (K.M., R.I.), Nuffield Department of Medicine, University of Oxford, United Kingdom; Department of Psychiatry (C.N.), University of Oxford, United Kingdom; and Nuffield Department of Clinical Neurosciences (A.V.), University of Oxford, United Kingdom.
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Noriko Salamon
From the Department of Neurology (R.M.), David Geffen School of Medicine at University of California Los Angeles; Kampala MRI Centre (S.K.L., M.K.), Uganda; Department of Radiological Sciences (N.S.), David Geffen School of Medicine, University of California Los Angeles, CA; Division of General Internal Medicine and Health Services Research (N.J.J.), David Geffen School of Medicine at UCLA; Centre of Tropical Neuroscience (P.R.A., R.A., R.I.), Kitgum Site, Uganda; Makerere University (R.A., R.J.O., R.I.), College of Health Sciences, Kampala, Uganda; Laboratory of Parasitic Diseases (J.K., T.N.), National Institutes of Health, Bethesda, MD; Centre for Tropical Medicine and Global Health (K.M., R.I.), Nuffield Department of Medicine, University of Oxford, United Kingdom; Department of Psychiatry (C.N.), University of Oxford, United Kingdom; and Nuffield Department of Clinical Neurosciences (A.V.), University of Oxford, United Kingdom.
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Nicholas J. Jackson
From the Department of Neurology (R.M.), David Geffen School of Medicine at University of California Los Angeles; Kampala MRI Centre (S.K.L., M.K.), Uganda; Department of Radiological Sciences (N.S.), David Geffen School of Medicine, University of California Los Angeles, CA; Division of General Internal Medicine and Health Services Research (N.J.J.), David Geffen School of Medicine at UCLA; Centre of Tropical Neuroscience (P.R.A., R.A., R.I.), Kitgum Site, Uganda; Makerere University (R.A., R.J.O., R.I.), College of Health Sciences, Kampala, Uganda; Laboratory of Parasitic Diseases (J.K., T.N.), National Institutes of Health, Bethesda, MD; Centre for Tropical Medicine and Global Health (K.M., R.I.), Nuffield Department of Medicine, University of Oxford, United Kingdom; Department of Psychiatry (C.N.), University of Oxford, United Kingdom; and Nuffield Department of Clinical Neurosciences (A.V.), University of Oxford, United Kingdom.
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Michael Kawooya
From the Department of Neurology (R.M.), David Geffen School of Medicine at University of California Los Angeles; Kampala MRI Centre (S.K.L., M.K.), Uganda; Department of Radiological Sciences (N.S.), David Geffen School of Medicine, University of California Los Angeles, CA; Division of General Internal Medicine and Health Services Research (N.J.J.), David Geffen School of Medicine at UCLA; Centre of Tropical Neuroscience (P.R.A., R.A., R.I.), Kitgum Site, Uganda; Makerere University (R.A., R.J.O., R.I.), College of Health Sciences, Kampala, Uganda; Laboratory of Parasitic Diseases (J.K., T.N.), National Institutes of Health, Bethesda, MD; Centre for Tropical Medicine and Global Health (K.M., R.I.), Nuffield Department of Medicine, University of Oxford, United Kingdom; Department of Psychiatry (C.N.), University of Oxford, United Kingdom; and Nuffield Department of Clinical Neurosciences (A.V.), University of Oxford, United Kingdom.
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Pamela Rosemary Akun
From the Department of Neurology (R.M.), David Geffen School of Medicine at University of California Los Angeles; Kampala MRI Centre (S.K.L., M.K.), Uganda; Department of Radiological Sciences (N.S.), David Geffen School of Medicine, University of California Los Angeles, CA; Division of General Internal Medicine and Health Services Research (N.J.J.), David Geffen School of Medicine at UCLA; Centre of Tropical Neuroscience (P.R.A., R.A., R.I.), Kitgum Site, Uganda; Makerere University (R.A., R.J.O., R.I.), College of Health Sciences, Kampala, Uganda; Laboratory of Parasitic Diseases (J.K., T.N.), National Institutes of Health, Bethesda, MD; Centre for Tropical Medicine and Global Health (K.M., R.I.), Nuffield Department of Medicine, University of Oxford, United Kingdom; Department of Psychiatry (C.N.), University of Oxford, United Kingdom; and Nuffield Department of Clinical Neurosciences (A.V.), University of Oxford, United Kingdom.
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Ronald Anguzu
From the Department of Neurology (R.M.), David Geffen School of Medicine at University of California Los Angeles; Kampala MRI Centre (S.K.L., M.K.), Uganda; Department of Radiological Sciences (N.S.), David Geffen School of Medicine, University of California Los Angeles, CA; Division of General Internal Medicine and Health Services Research (N.J.J.), David Geffen School of Medicine at UCLA; Centre of Tropical Neuroscience (P.R.A., R.A., R.I.), Kitgum Site, Uganda; Makerere University (R.A., R.J.O., R.I.), College of Health Sciences, Kampala, Uganda; Laboratory of Parasitic Diseases (J.K., T.N.), National Institutes of Health, Bethesda, MD; Centre for Tropical Medicine and Global Health (K.M., R.I.), Nuffield Department of Medicine, University of Oxford, United Kingdom; Department of Psychiatry (C.N.), University of Oxford, United Kingdom; and Nuffield Department of Clinical Neurosciences (A.V.), University of Oxford, United Kingdom.
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Rodney J. Ogwang
From the Department of Neurology (R.M.), David Geffen School of Medicine at University of California Los Angeles; Kampala MRI Centre (S.K.L., M.K.), Uganda; Department of Radiological Sciences (N.S.), David Geffen School of Medicine, University of California Los Angeles, CA; Division of General Internal Medicine and Health Services Research (N.J.J.), David Geffen School of Medicine at UCLA; Centre of Tropical Neuroscience (P.R.A., R.A., R.I.), Kitgum Site, Uganda; Makerere University (R.A., R.J.O., R.I.), College of Health Sciences, Kampala, Uganda; Laboratory of Parasitic Diseases (J.K., T.N.), National Institutes of Health, Bethesda, MD; Centre for Tropical Medicine and Global Health (K.M., R.I.), Nuffield Department of Medicine, University of Oxford, United Kingdom; Department of Psychiatry (C.N.), University of Oxford, United Kingdom; and Nuffield Department of Clinical Neurosciences (A.V.), University of Oxford, United Kingdom.
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Joseph Kubofcik
From the Department of Neurology (R.M.), David Geffen School of Medicine at University of California Los Angeles; Kampala MRI Centre (S.K.L., M.K.), Uganda; Department of Radiological Sciences (N.S.), David Geffen School of Medicine, University of California Los Angeles, CA; Division of General Internal Medicine and Health Services Research (N.J.J.), David Geffen School of Medicine at UCLA; Centre of Tropical Neuroscience (P.R.A., R.A., R.I.), Kitgum Site, Uganda; Makerere University (R.A., R.J.O., R.I.), College of Health Sciences, Kampala, Uganda; Laboratory of Parasitic Diseases (J.K., T.N.), National Institutes of Health, Bethesda, MD; Centre for Tropical Medicine and Global Health (K.M., R.I.), Nuffield Department of Medicine, University of Oxford, United Kingdom; Department of Psychiatry (C.N.), University of Oxford, United Kingdom; and Nuffield Department of Clinical Neurosciences (A.V.), University of Oxford, United Kingdom.
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Thomas Nutman
From the Department of Neurology (R.M.), David Geffen School of Medicine at University of California Los Angeles; Kampala MRI Centre (S.K.L., M.K.), Uganda; Department of Radiological Sciences (N.S.), David Geffen School of Medicine, University of California Los Angeles, CA; Division of General Internal Medicine and Health Services Research (N.J.J.), David Geffen School of Medicine at UCLA; Centre of Tropical Neuroscience (P.R.A., R.A., R.I.), Kitgum Site, Uganda; Makerere University (R.A., R.J.O., R.I.), College of Health Sciences, Kampala, Uganda; Laboratory of Parasitic Diseases (J.K., T.N.), National Institutes of Health, Bethesda, MD; Centre for Tropical Medicine and Global Health (K.M., R.I.), Nuffield Department of Medicine, University of Oxford, United Kingdom; Department of Psychiatry (C.N.), University of Oxford, United Kingdom; and Nuffield Department of Clinical Neurosciences (A.V.), University of Oxford, United Kingdom.
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Kevin Marsh
From the Department of Neurology (R.M.), David Geffen School of Medicine at University of California Los Angeles; Kampala MRI Centre (S.K.L., M.K.), Uganda; Department of Radiological Sciences (N.S.), David Geffen School of Medicine, University of California Los Angeles, CA; Division of General Internal Medicine and Health Services Research (N.J.J.), David Geffen School of Medicine at UCLA; Centre of Tropical Neuroscience (P.R.A., R.A., R.I.), Kitgum Site, Uganda; Makerere University (R.A., R.J.O., R.I.), College of Health Sciences, Kampala, Uganda; Laboratory of Parasitic Diseases (J.K., T.N.), National Institutes of Health, Bethesda, MD; Centre for Tropical Medicine and Global Health (K.M., R.I.), Nuffield Department of Medicine, University of Oxford, United Kingdom; Department of Psychiatry (C.N.), University of Oxford, United Kingdom; and Nuffield Department of Clinical Neurosciences (A.V.), University of Oxford, United Kingdom.
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Charles Newton
From the Department of Neurology (R.M.), David Geffen School of Medicine at University of California Los Angeles; Kampala MRI Centre (S.K.L., M.K.), Uganda; Department of Radiological Sciences (N.S.), David Geffen School of Medicine, University of California Los Angeles, CA; Division of General Internal Medicine and Health Services Research (N.J.J.), David Geffen School of Medicine at UCLA; Centre of Tropical Neuroscience (P.R.A., R.A., R.I.), Kitgum Site, Uganda; Makerere University (R.A., R.J.O., R.I.), College of Health Sciences, Kampala, Uganda; Laboratory of Parasitic Diseases (J.K., T.N.), National Institutes of Health, Bethesda, MD; Centre for Tropical Medicine and Global Health (K.M., R.I.), Nuffield Department of Medicine, University of Oxford, United Kingdom; Department of Psychiatry (C.N.), University of Oxford, United Kingdom; and Nuffield Department of Clinical Neurosciences (A.V.), University of Oxford, United Kingdom.
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Angela Vincent
From the Department of Neurology (R.M.), David Geffen School of Medicine at University of California Los Angeles; Kampala MRI Centre (S.K.L., M.K.), Uganda; Department of Radiological Sciences (N.S.), David Geffen School of Medicine, University of California Los Angeles, CA; Division of General Internal Medicine and Health Services Research (N.J.J.), David Geffen School of Medicine at UCLA; Centre of Tropical Neuroscience (P.R.A., R.A., R.I.), Kitgum Site, Uganda; Makerere University (R.A., R.J.O., R.I.), College of Health Sciences, Kampala, Uganda; Laboratory of Parasitic Diseases (J.K., T.N.), National Institutes of Health, Bethesda, MD; Centre for Tropical Medicine and Global Health (K.M., R.I.), Nuffield Department of Medicine, University of Oxford, United Kingdom; Department of Psychiatry (C.N.), University of Oxford, United Kingdom; and Nuffield Department of Clinical Neurosciences (A.V.), University of Oxford, United Kingdom.
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Richard Idro
From the Department of Neurology (R.M.), David Geffen School of Medicine at University of California Los Angeles; Kampala MRI Centre (S.K.L., M.K.), Uganda; Department of Radiological Sciences (N.S.), David Geffen School of Medicine, University of California Los Angeles, CA; Division of General Internal Medicine and Health Services Research (N.J.J.), David Geffen School of Medicine at UCLA; Centre of Tropical Neuroscience (P.R.A., R.A., R.I.), Kitgum Site, Uganda; Makerere University (R.A., R.J.O., R.I.), College of Health Sciences, Kampala, Uganda; Laboratory of Parasitic Diseases (J.K., T.N.), National Institutes of Health, Bethesda, MD; Centre for Tropical Medicine and Global Health (K.M., R.I.), Nuffield Department of Medicine, University of Oxford, United Kingdom; Department of Psychiatry (C.N.), University of Oxford, United Kingdom; and Nuffield Department of Clinical Neurosciences (A.V.), University of Oxford, United Kingdom.
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Citation
Comparison of Structural Changes in Nodding Syndrome and Other Epilepsies Associated With Onchocerca volvulus
Rajarshi Mazumder, Samson Kamya Lubowa, Noriko Salamon, Nicholas J. Jackson, Michael Kawooya, Pamela Rosemary Akun, Ronald Anguzu, Rodney J. Ogwang, Joseph Kubofcik, Thomas Nutman, Kevin Marsh, Charles Newton, Angela Vincent, Richard Idro
Neurol Neuroimmunol Neuroinflamm Mar 2023, 10 (2) e200074; DOI: 10.1212/NXI.0000000000200074

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Abstract

Background and Objective Nodding syndrome (NS) is a unique childhood-onset epileptic disorder that occurs predominantly in several regions of sub-Saharan Africa. The disease has been associated with Onchocerca volvulus (Ov)–induced immune responses and possible cross-reactivity with host proteins. The aim of this study was to compare structural changes in the brain on MRI between NS and other forms of onchocerciasis-associated epilepsies (OAEs) and to relate structural changes to the Ov-induced immune responses and level of disability.

Methods Thirty-nine children with NS and 14 age-matched participants with other forms of OAE from an endemic region in Uganda underwent detailed clinical examination, serologic evaluation (including Ov-associated antibodies to Ov-16 and Hu-leiomodin-1) and quantitative volumetric analysis of brain MRIs (1.5 T scanner) using Neuroreader, a cloud-based software.

Results Cerebral and cerebellar atrophy were the predominant features in both NS and OAE. On quantitative volumetric analysis, participants with NS had larger ventricular volumes compared with participants with OAE, indicative of increased global cortical atrophy (pcorr = 0.036). Among children with NS, severe disability correlated with higher degree of atrophy in the gray matter volume (pcorr = 0.009) and cerebellar volume (pcorr = 0.009). NS cases had lower anti-Ov-16 IgG signal-to-noise ratios than the OAE cases (p < 0.01), but no difference in the levels of the Hu-leiomodin-1 antibodies (p = 0.64). The levels of Ov-associated antibodies did not relate to the degree of cerebral or cerebellar atrophy in either NS or OAE cases.

Discussion This is the first study to show that cerebral and cerebellar atrophy correlated with the severity of NS disability, providing an imaging marker for these endemic epileptic disorders that until now have remained poorly characterized. Both NS and OAE have cerebral and cerebellar atrophy, and the levels of Ov-associated antibodies do not seem to be related to the structural changes on MRI.

Glossary

mRS=
modified Rankin scale;
NS=
nodding syndrome;
OAE=
onchocerciasis-associated epilepsy;
Ov=
Onchocerca volvulus

Footnotes

  • The article processing charge was funded by UCLA and University of Oxford.

  • Go to Neurology.org/NN for full disclosures. Funding information is provided at the end of the article.

  • Submitted and externally peer reviewed. The handling editor was Editor Josep O. Dalmau, MD, PhD, FAAN.

  • Received July 11, 2022.
  • Accepted in final form October 18, 2022.
  • Copyright © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology.

This is an open access article distributed under the terms of the Creative Commons Attribution License 4.0 (CC BY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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