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July 2018; 5 (4) Clinical/Scientific NotesOpen Access

Mortality in neuromyelitis optica is strongly associated with African ancestry

Maureen A. Mealy, Remi A. Kessler, Zoe Rimler, Allyson Reid, Lauren Totonis, Gary Cutter, Ilya Kister, Michael Levy
First published June 7, 2018, DOI: https://doi.org/10.1212/NXI.0000000000000468
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  1. Maureen A. Mealy, PhD(c), RN*,
  2. Remi A. Kessler, BA*,
  3. Zoe Rimler, BS,
  4. Allyson Reid, BA,
  5. Lauren Totonis, BS,
  6. Gary Cutter, PhD,
  7. Ilya Kister, MD and
  8. Michael Levy, MD, PhD
  1. From the Department of Neurology (M.A.M., R.A.K., L.T., M.L.), Johns Hopkins University, Baltimore, MD; the Department of Neurology (Z.R., A.R., I.K.), New York University; and the University of Alabama (G.C.), Birmingham, AL.
  1. Correspondence
    Dr. Levy mlevy{at}jhmi.edu
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  1. (1) Consortium of MS Centers, speaker honoraria; (2) Teva, Speaker honoraria

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  1. (1) Multiple Sclerosis, Editorial Board, 2010-present (2) JASN, 2013- present, statistical consulting reviewer (3) Alzheimers & Dementia: Translational Research & Clinical Interventions

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Employment, Commercial Entity:

  1. (1) Employed by the University of Alabama at Birmingham; (2) President of Pythagoras, Inc. a private consulting company located in Birmingham AL.

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  1. Argenx BVBA, Atara Biotherapeutics, Consortium of MS Centers (grant), Genzyme, Genentech, Innate Therapeutics, Jannsen Pharmaceuticals, Klein-Buendel Incorporated, Medimmune, Medday, Nivalis, Novartis, Opexa Therapeutics, Roche, Savara Inc., Somahlution, Teva pharmaceuticals, Transparency Life Sciences, TG Therapeutics

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Research Support, Government Entities:

  1. ACTIVE U01 NS 042685 (Cutter) 09/23/2005 ? 08/31/2015 NIH/NINDS Thymectomy Plus Prednisone vs. Prednisone Alone in NonThymomatous Myasthenia Gravis This multinational clinical trial aims to assess the utility of thymectomy in treating nonthymomatous Myasthenia Gravis patients comparing surgery plus medications versus medications alone. P30-AI 027767 (Saag, M.) 06/01/2014 ? 05/31/2019 NIH/NIAID UAB Center for Aids Research This CFAR is organized as a partnership between the University of Alabama at Birmingham and the Southern Research Institute. The primary purpose of this partnership is to generate interdisciplinary AIDS research efforts. This Center is responsible for planning, evaluating, managing and documenting a broad array of research activities within two institutions. Particular emphasis is placed upon linking clinical and basic science studies through the use of shared facilities and to translate as quickly as possible fundamental knowledge about AIDS and its related disorders into clinical treatment and prevention programs. U01-HL 119242 (Cutter) 09/01/2014 ? 05/31/2020 NIH/NHLBI Chronic Hypertension and Pregnancy (CHAP): Data Coordinating Center We propose a large pragmatic multi-center randomized trial of pregnant women with mild chronic hypertension to evaluate the benefits and harms of antihypertensive therapy to a goal <140/90 mmHg (as recommended for the general population in the US) compared with ACOG's current policy of expectant management of mild chronic hypertension in pregnancy. The trial will be conducted in 12 experienced research-oriented Ob/Gyn departments (including 25 clinical sites) in the United States. The monitoring plan will include a pre-specified option to increase the planned sample size of 4700 women after interim evaluation by an independent Data Safety and Monitoring Board. R01 HD 064729 (Tita) 04/01/2010 ? 07/31/2015 NIH/NICHD Caesarean Section Optimal Antibiotic Prophylaxis (C/SOAP) Trial A multicenter randomized trial to determine the efficacy and safety of a modified (extended-spectrum) antibiotic prophylaxis strategy at cesarean delivery to reduce surgical site infections. R01 AG 021927 (Marson) 07/01/2010 ? 06/30/2015 NIH/NIA Functional Change in Mild Cognitive Impairment (COINS) This R01 project investigates longitudinal change in higher order functional abilities in patients with MCI, and develops predictor models for clinical progression and conversion from MCI to dementia. No number assigned (Cutter) 01/01/2004 ? 12/31/2015 Consortium of MS Centers (CMSC) North American Research Consortium on Multiple Sclerosis (NARCOMS) The goals of this project are to facilitate a confidential way for patients to supply valuable information to researchers about their course of disease that may lead to more effective treatments and care. W81XWH-12-1-0155 (Korf) 05/15/2012 ? 05/14/2017 U.S. Department of Defense NEUTOFIBOMATOSIS CLINICAL CONSORTIUM AWARD This is a cooperative study group that is focusing on multiple trials in NF. The role of the operations center is both as the data center and the overall coordinating of the study group. U01NS45719 (Lublin) 06/01/2004 ? 11/30/2015 NIH/NINDS CombiRx Statistical and Data Management Center A Phase III, multi-center, double-blind, randomized study comparing the combined use of Interferon Beta-1a and Glatiramer Acetate to either agent alone in patients with relapsing remitting multiple sclerosis. 140305 (Greenberg) 09/01/2013 ? 08/31/2016 Patient Centered Outcomes Research Institute Collaborative Assessment of Pediatric Transverse Myelitis: Understand, Reveal, Educate (CAPTURE) U34 AR062891 (K. Saag) 04/15/2013 ? 03/31/2015 NIH/NIAMS Effectiveness of DiscontinuinG BisphosphonatEs Study (EDGE) Planning grant for a Pragmatic Clinical Trial (PCT), ?Effectiveness of DiscontinuinG bisphosphonatEs (EDGE) Study?, a ?real world? effectiveness trial of an initially estimated 4,100 patients randomized to continuation or discontinuation of prior alendronate therapy. P30DK079337 (Agarwal) 09/20/13 ? 07/31/18 NIH/NIDDK UAB/UCSD O?Brien Core Center for Acute Kidney Injury Research In summary, these cores and the outstanding cohort of investigators assembled for this center will provide unique expertise that is critical for innovative and productive research in AKI. With its Extended Research Base that includes both clinical and basic investigators, this O'Brien center will accelerate the translation of new investigative insights towards novel therapies for patients with AKI. RSTFD0000541263 (Cutter) 09/01/13 ? 08/31/17 Children?s Hospital (Boston) Early Biomarkers of Autism Spectrum Disorders in Infants with Tuberous Sclerosis MG Registry (Cutter) 01/01/14-present (annually) MGFA This is new registry (1.5 years old) that is a patient registry of Myasthenia Gravis Patients based solely on patient reported outcomes tracking their disease over time. CBD Trial (Cutter) 04/01/2014 ? 9/30/2015 State of Alabama The data management center for the effectiveness of cannabidiol (CBD) oil for the treatment of seizures and epilepsy.

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  1. (1) Consortium of MS Centers (2) Myasthenia Gravis Foundation of America, grant for MG Registry

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  1. Pythagoras, Inc. Sub S Corporation - President.

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Legal Proceedings:

  1. Galderma Litigation (acne case) reviewed statistical data

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  1. Biogen Idec MS Franchise Data Generation Advisory Board Genentech Advisory Board

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  1. Received research support from Biogen-Idec, Serono, Novartis, Genzyme

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  1. NONE

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  1. (1) Guthy-Jackson Charitable Foundation (2) National Multiple Sclerosis Society

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  1. Asterias, Chugai, Alexion

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  1. Editorial Board member of Multiple Sclerosis and Related Disorders

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  1. 1. Aquaporin-4 sequence that elicits pathogenic T cell response in animal model of neuromyelitis optica. 2. Description: patent covers use of peptide for diagnostic and therapeutic developments.

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Background

Neuromyelitis optica spectrum disorder (NMOSD) is a severe autoimmune disease of the optic nerve, spinal cord, and, less frequently, brain.1 Severity and degree of recovery from relapses are the factors that determine long-term visual and motor disability and mortality.1 Mortality rates in NMOSD worldwide range from 9% to 32%, depending on age, relapse rate, and recovery from attacks.2,3 In examining mortality data from 2 large, ethnically diverse NMOSD Centers in the Mid-Atlantic United States, we observed a striking race distribution: most deceased patients were of African ancestry. In this analysis, we focus on race as a risk factor for mortality in NMOSD.

Methods

This is a retrospective study of all patients with NMOSD seen at 2 large US-based clinics: Johns Hopkins Hospital (Baltimore, MD) and New York University (New York, NY). NMOSD was defined by the 2015 International Panel of NMO Diagnosis.4 Race was patient reported, whereas all other clinical and demographic factors, including the cause of death, were confirmed by site investigators. Patients not seen in the previous 12 months were called to verify living status. Time to diagnosis, frequency of clinic/hospital visits, and treatment regimen for relapses acted as surrogates of health care access. Institutional review boards from both institutions approved this study.

Results

A total of 427 NMOSD patients were included in this analysis, 328 from Johns Hopkins Hospital and 99 from New York University. In total, 30 patients died during follow-up (table), with an annual mortality rate of 0.68 deaths per 100 patient-years. The mean disease duration at time of death was 6.9 years. Patients of African ancestry constituted 41% of our clinic population, but they comprised 90% of the deceased NMOSD patients, with average age at death of 52.3 years. The other 3 deceased patients included an Asian woman aged 85 years, a Caucasian man aged 69 years, and a Caucasian woman aged 65 years. The overall mortality rate in our total cohort was 7.0%, and among those of African ancestry was 15.4% (p < 0.0001).

View this table:
Table

Demographic and clinical characteristics of cohorts

Patients in each race group were similar regarding age, sex, aquaporin-4 serostatus, time to diagnosis, acute treatment care, and access to our clinics (table). Although more deceased patients were untreated at final follow-up (22% vs. 4%), there was no difference in treatment rates among the races.

In 22 of 30 deceased patients (73%), cause of death was related to NMOSD (table). Most deaths, 70%, were preceded by a relapse in the brainstem and/or upper cervical spinal cord within the previous 12 months despite preventive medications in 80% of patients at the time of the fatal relapse.

Discussion

Our study involved a very large patient sample—427 patients from 2 large specialized NMO centers. The overall mortality rate was 7.0% (30 of 427 patients). This rate is slightly lower than in contemporary studies (9%–13%)3,5 and considerably improved from older landmark studies (22%–32%).2,6,7 The decrease in mortality over time is likely due to earlier diagnosis, use of plasmapheresis for acute relapses, and preventive immunotherapies, which have been shown to decrease relapse rates in observational studies.8 It is important that the definition of NMOSD has changed over the past 2 decades, allowing for milder cases to be diagnosed. Thus, the decrease in mortality could also be in part a technical artifact (“Will Rogers effect”).

The most striking finding of this study is the observation that nearly all the deceased patients in our combined cohort were of African ancestry. Patients of African ancestry make up 41% of the total cohort, but account for 90% of the mortality. This is unlikely due to chance (p < 0.0001, Fisher test) or to differences in delay in diagnosis, clinic access, or treatment (table). This is also unlikely to be due to differences in death rates among races: according the CDC, mortality rate among those of African race was 0.8% and 0.7% among Caucasians (2009–2014). One other study has identified African ancestry as a strong predictor of mortality in NMOSD. In Brazil, where the estimated mortality rate among all patients with NMOSD is 23%, the mortality rate among Afro-Brazilians is a staggering 58%.9 Two European studies did not implicate African race as a risk factor for mortality, but the proportion of African patients in their cohorts was much lower than in the Eastern US and Brazilian NMOSD cohorts.2,10,11 Our results have important implications for management of patients of African ancestry with NMOSD. Further studies, especially prospective studies assessing factors that affect the severity of relapses, may shed light on the high risk of death among patients of African ancestry with NMOSD.

Author contributions

M. Levy, R.A. Kessler, M.A. Mealy, G. Cutter, and I. Kister contributed to the design and conceptualization of the study, analysis and interpretation of the data, and drafting of the manuscript.

Study funding

This study was funded by the NIH, K08 NS078555 (M. Levy).

Disclosure

M.A. Mealy received speaker honoraria from the Consortium of Multiple Sclerosis Centers and research support from the NIH/NCATS. R.A. Kessler, Z. Rimler, A. Reid, and L. Totonis report no disclosures. G. Cutter served on the scientific advisory board of AMO Pharmaceuticals, Apotek, Gilead Pharmaceuticals, Horizon Pharmaceuticals, Modigenetech/Prolor, Merck, Merck/Pfizer, Opko Biologics, Sanofi-Aventis, Reata Pharmaceuticals, Receptos/Celgene, Teva, NHLBI, and NICHD; received speaker honoraria from the Consortium of Multiple Sclerosis Centers and, Teva; served on the editorial board of Multiple Sclerosis, JASN, and Alzheimer's & Dementia: Translational Research & Clinical Interventions; is president of and holds stock in Pythagoras; consulted for Argenx BVBA, Atara Biotherapeutics, Consortium of Multiple Sclerosis Centers, Genzyme, Genentech, Innate Therapeutics, Janssen Pharmaceuticals, Klein-Buendel Incorporated, MedImmune, Medday, Nivalis, Novartis, Opexa Therapeutics, Roche, Savara Inc, Somahlution, Teva, Transparency Life Sciences, and TG Therapeutics; participates in the NARCOMS MS Patient Registry funded by the CMSC; received research support from the NIH/NINDS, NIH/NIAID, UAB Center for AIDS Research, NIH/NHLBI, NIH/NICHD, NIH/NIA, US Department of Defense, NIH/MIAMS Children's Hospital (Boston), Consortium of MS Centers, and Myasthenia Gravis Foundation of America; and reviewed statistical data for Galderma Litigation. I. Kister received served on the scientific advisory board of Biogen IDEC MS Franchise Data Generation and Genentech; consulted for Biogen Idec; and received research support from Biogen Idec, Serono, Novartis, Genzyme, Guthy-Jackson Charitable Foundation, and National Multiple Sclerosis Society. M. Levy served on the scientific advisory board of Asterias, Chugai, and Alexion; is on the editorial board of Multiple Sclerosis and Related Disorders; holds patents for Aquaporin-4 sequence that elicits pathogenic T cell response in animal model of neuromyelitis optica and Use of peptide for diagnostic and therapeutic developments; consulted for Guidepoint Global, Gerson Lehrman Group, and Cowen Group; and received research support from ViroPharma/Shire, Acorda, AcoPharma, Sanofi, Genzyme, Alnylan, Alexion, Terumo BCT, and NINDS. Full disclosure form information provided by the authors is available with the full text of this article at Neurology.org/NN.

Footnotes

  • ↵* Shared first authorship.

  • Funding information and disclosures are provided at the end of the article. Full disclosure form information provided by the authors is available with the full text of this article at Neurology.org/NN.

  • Received August 24, 2017.
  • Accepted in final form April 9, 2018.

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND), which permits downloading and sharing the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

References

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    1. Abboud H,
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    6. Levy M
    . Treatment of acute relapses in neuromyelitis optica: steroids alone versus steroids plus plasma exchange. Mult Scler 2016;22:185–192.
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