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Articles
April 18, 2012
Letter to the Editor

Simultaneous PML-IRIS after discontinuation of natalizumab in a patient with MS

May 1, 2012 issue
78 (18) 1390-1393

Abstract

Objective:

Progressive multifocal leukoencephalopathy (PML) is a severe complication of natalizumab therapy in patients with multiple sclerosis (MS), which is often accompanied by an immune reconstitution inflammatory syndrome (IRIS) after removal of the drug. We describe a patient with MS who presented with simultaneous PML-IRIS 2 months after stopping natalizumab for other reasons.

Case Report and Results:

The patient had widespread PML and severe IRIS. He received corticosteroids and displayed a vigorous JC virus–specific cellular immune response. Elevated myoinositol and lipid/creatine peaks measured in PML lesions by proton magnetic resonance spectroscopy (1H-MRS) corresponded to episodes of contrast enhancement on MRI scans and persisted after the enhancement subsided. He demonstrated steady clinical improvement, but developed marked residual atrophy in areas affected by PML and inflammation, as well as seizures.

Conclusions:

New enhancing white matter lesions, occurring after discontinuation of natalizumab, can be the manifestation of PML-IRIS rather than an MS exacerbation. Elevated myoinositol and lipid/creatine peaks appear to be more sensitive markers of inflammation in PML lesions than contrast enhancement. 1H-MRS may become useful as a biomarker for PML-IRIS by helping clinicians determine the need for corticosteroid administration and anticipate continuing clinical recovery.

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REFERENCES

1.
Vermersch P, Kappos L, Gold R, et al. Clinical outcomes of natalizumab-associated progressive multifocal leukoencephalopathy. Neurology 2011; 76: 1697–1704.
2.
Johnson T, Nath A. Neurological complications of immune reconstitution in HIV-infected populations. Ann NY Acad Sci 2010; 1184: 106–120.
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O'Connor PW, Goodman A, Kappos L, et al. Disease activity return during natalizumab treatment interruption in patients with multiple sclerosis. Neurology 2011; 76: 1858–1865.
4.
Miravalle A, Jensen R, Kinkel RP. Immune reconstitution inflammatory syndrome in patients with multiple sclerosis following cessation of natalizumab therapy. Arch Neurol 2011; 68: 186–191.
5.
Bonham S, Meya DB, Bohjanen PR, Boulware DR. Biomarkers of HIV immune reconstitution inflammatory syndrome. Biomark Med 2008; 2: 349–361.
6.
Gheuens S, Bord E, Kesari S, et al. Role of CD4+ and CD8+ T-cell responses against JC virus in the outcome of patients with progressive multifocal leukoencephalopathy (PML) and PML with immune reconstitution inflammatory syndrome. J Virol 2011; 85: 7256–7263.
7.
Katz-Brull R, Lenkinski RE, Du Pasquier RA, Koralnik IJ. Elevation of myoinositol is associated with disease containment in progressive multifocal leukoencephalopathy. Neurology 2004; 63: 897–900.
8.
Cuvinciuc V, Martin-Blondel G, Marchou B, Bonneville F. Proton MR spectroscopy of progressive multifocal leukoencephalopathy-immune reconstitution inflammatory syndrome. AJNR Am J Neuroradiol 2010; 31: E69–E70; author reply E71.
Letters to the Editor
18 June 2012
Re:Withdrawal of natalizumab in MS patients: a tale of two tails
Sarah Gheuens, MD
Igor J. Koralnik, Boston, MA

We thank Marousi et al. for their comments on our paper. We agree that PML may also occur in the setting of occult of minimal immunosuppression, as seen in 5 cases at our center and in 33 previously reported patients. [1] As they mention, clinicians should be aware that either PML-IRIS or a relapse of MS may occur after discontinuation of natalizumab.

1. Gheuens S, Pierone G, Peeters P, Koralnik IJ. Progressive multifocal leukoencephalopathy in individuals with minimal or occult immunosuppression. J Neurol Neurosurg Psychiatry 2010;81:247-254.

For disclosures, contact the editorial office at [email protected].

11 June 2012
Withdrawal of natalizumab in MS patients: a tale of two tails
Stella Marousi
Stella Marousi, Athens, Greece; Maria Travasarou, Athens, Greece; Clementine E. Karageorgiou, Athens, Greece

Gheuens et al. presented a case of PML-IRIS 2 months after natalizumab discontinuation. [1] Their patient had an active history of ethanol abuse, which can be considered a 'functional' equivalent to immunosuppression. Interestingly, prior use of immunosuppressants has been included to the recently developed risk-stratification algorithm for PML. [2] This case underscores the need for clinicians to adopt a wider concept of immunosuppression, rather than restricting it solely to the use of pharmacologic agents. We and others published 3 cases of definitive severe MS rebound about 2 months following natalizumab discontinuation [3-5], and further implied that younger patients are more prone to such relapses. [5] However, Gheuens et al. concluded that new enhancing MRI lesions after natalizumab withdrawal may also be the manifestation of PML-IRIS. [1]. As experience from patients discontinuing natalizumab and switching to other therapies mounts, a high degree of clinical vigilance for both incidences (i.e. MS rebound and PML) should follow the immediate post- natalizumab period. However, until official guidelines are issued, it is unclear exactly how patients should be treated in the interval between natalizumab and the next therapeutic choice.

1. Gheuens S, Smith DR, Wang X, Alsop DC, Lenkinski RE, Koralnik IJ. Simultaneous PML-IRIS after discontinuation of natalizumab in a patient with MS. Neurology;78:1390-1393.

2. Bloomgren G, Richman S, Hotermans C, et al. Risk of natalizumab- associated progressive multifocal leukoencephalopathy. N Engl J Med;366:1870-1880.

3. Lenhard T, Biller A, Mueller W, Metz I, Schonberger J, Wildemann B. Immune reconstitution inflammatory syndrome after withdrawal of natalizumab? Neurology;75:831-833.

4. Hellwig K, Gold R. Immune reconstitution inflammatory syndrome after withdrawal of natalizumab? Neurology;76:1362-1363; author reply 1363.

5. Marousi S, Giannouli E, Karkanis I, Tagaris GA, Karageorgiou CE. Immune reconstitution inflammatory syndrome after withdrawal of natalizumab? Neurology;76:1362-1363; author reply 1363. For disclosures, contact the editorial office at [email protected].

Information & Authors

Information

Published In

Neurology®
Volume 78Number 18May 1, 2012
Pages: 1390-1393
PubMed: 22517104

Publication History

Received: September 9, 2011
Accepted: November 28, 2011
Published online: April 18, 2012
Published in print: May 1, 2012

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Disclosure

Dr. Gheuens is funded by NIH grant T32 AI07387-21 and is a fellow of the Clinical Investigator Training Program: Beth Israel Deaconess Medical Center–Harvard/MIT Health Sciences and Technology, in collaboration with Pfizer Inc. and Merck & Co. Dr. Smith has received consulting/advisory fees and speaking honoraria but not grant support or standing committee income from all of the manufacturers of FDA-approved products for multiple sclerosis treatment. Dr. Wang is supported in part by NIH grant R01 NS047029. Dr. Alsop is an inventor on several patents related to perfusion MRI (US Patent Nos. 7,545,142, 7,369,888, 6,980,845, 6,717,405), for which he has received royalties from GE Healthcare and Siemens Medical; receives research support from GE Healthcare and is also supported by grants from the NIH, CA115745, EB004582, MH80729, MH077073, DC008796, NS047029, CA101942, AG031720, AG028076, DK084463, and the Congressionally Directed Military Research Program of the Department of Defense, SC090251; and serves as Associate Editor of Magnetic Resonance in Medicine. Dr. Lenkinski is supported in part by NIH grant R01 NS047029 and receives research support from GE Healthcare. Dr. Koralnik is funded by NIH grants R56 NS 041198, R01 NS 047029 and K24 NS 060950; has received a research grant from Biogen Idec and the National Multiple Sclerosis Society; served on scientific advisory boards for Hoffmann La Roche, GlaxoSmithKline and Merck Serono; received consulting fees from Bristol Myers Squibb, Ono Pharmaceuticals, Merck Serono, Hoffmann La Roche, GlaxoSmithKline, Perseid Therapeutics, Vertex Pharmaceutical, Johnson & Johnson; and is an editorial board member for the Journal of NeuroVirology and receives royalties from UpToDate for topics on the management of HIV and CNS mass lesions and on PML. Go to Neurology.org for full disclosures.

Authors

Affiliations & Disclosures

S. Gheuens, MD
From the Division of NeuroVirology (S.G., I.J.K.), Division of Viral Pathogenesis (S.G., I.J.K.), and Department of Radiology (X.W., D.C.A., R.E.L.), Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA; and Thames Neurologic Institute Neurology Associates (D.R.S.), Norwich, CT.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers’ Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NIH T32 CA09031-32 May 2009-April 2010 NIH T32 AI07387-21 December 2010-July 2012
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
Belgian American Educational Foundation, postdoctoral position, May 2010-December 2010
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
D.R. Smith, MD
From the Division of NeuroVirology (S.G., I.J.K.), Division of Viral Pathogenesis (S.G., I.J.K.), and Department of Radiology (X.W., D.C.A., R.E.L.), Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA; and Thames Neurologic Institute Neurology Associates (D.R.S.), Norwich, CT.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
Received honoraria/fees from all MS therapeutics manufacturers totalling approx $50K/yr
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
Neurology practice, approx $250K/yr Speakers’ Bureaus: Received honoraria/fees from all MS therapeutics manufacturers totalling approx $50K/yr
Consultancies:
1.
NONE
Speakers’ Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
X. Wang, MD
From the Division of NeuroVirology (S.G., I.J.K.), Division of Viral Pathogenesis (S.G., I.J.K.), and Department of Radiology (X.W., D.C.A., R.E.L.), Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA; and Thames Neurologic Institute Neurology Associates (D.R.S.), Norwich, CT.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers’ Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
D.C. Alsop, PhD
From the Division of NeuroVirology (S.G., I.J.K.), Division of Viral Pathogenesis (S.G., I.J.K.), and Department of Radiology (X.W., D.C.A., R.E.L.), Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA; and Thames Neurologic Institute Neurology Associates (D.R.S.), Norwich, CT.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
Magnetic Resonance in Medicine, Associate Editor 2010-present
Patents:
1.
Methods for perfusion imaging with arterial spin labeling MRI, patent #’s 7,545,142 7,369,888 6,980,845 6,717,405
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers’ Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
GE Healthcare Technologies, Research Support, 2002-present
Research Support, Government Entities:
1.
NIH, 1 R01 CA115745-01A1, PI, 2006-present NIH, R01-EB004582, Co-investigator, 2006-present NIH, R01 MH80729-01A2, Co-investigator, 2007-present NIH, R01 MH077073-01A2, Co-investigator, 2008-present NIH, R01DC008796-01A1, Co-investigator, 2008-present NIH, R01 NS047029-04A2, Co-investigator, 2009-present NIH, 1P50 CA101942-01, Co-investigator, 2009-present DOD, SC090251, Co-investigator, 2010-present NIH, 1P01AG031720, Project Leader, 2010-present NIH,5R01AG028076, Co-investigator, 2009-present NIH, R21DK084463, Co-investigator, 2010-present
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
multi-slice perfusion imaging patents 7,369,888 and 6,980,845, Siemens Medical, 2009
Royalty Payments, Technology or Inventions:
1.
GE Healthcare, patent 7,545,142 (Arterial spin labeling with pulsed radio frequency sequences), 2009
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
R.E. Lenkinski, PhD
From the Division of NeuroVirology (S.G., I.J.K.), Division of Viral Pathogenesis (S.G., I.J.K.), and Department of Radiology (X.W., D.C.A., R.E.L.), Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA; and Thames Neurologic Institute Neurology Associates (D.R.S.), Norwich, CT.
Disclosure
Scientific Advisory Boards:
1.
Aspect MRI Rcadia Medical Aposense
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
Academic Radiology,2003-present
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers’ Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NIH,R01 EB004582,PI 4/1/10-3/31/15
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
I.J. Koralnik, MD
From the Division of NeuroVirology (S.G., I.J.K.), Division of Viral Pathogenesis (S.G., I.J.K.), and Department of Radiology (X.W., D.C.A., R.E.L.), Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA; and Thames Neurologic Institute Neurology Associates (D.R.S.), Norwich, CT.
Disclosure
Scientific Advisory Boards:
1.
Hoffman La Roche;, Glaxo Smith Klyne;, Merck Serono;
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
Journal Of NeuroVirology, Editorial Board Member (2008- present)
Patents:
1.
NONE
Publishing Royalties:
1.
UpToDate, Topics on the management of HIV and CNS mass lesions and on PML (2002-present)
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
Received consulting fees from Bristol Myers Sqibb;, Ono pharmaceuticals;, Merck Serono;,Hoffman La Roche;,Glaxo Smith Klyne;,Perseid Therapeutics;, Vertex Pharamaceutical;, Johnson & Johnson;
Speakers’ Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
Biogen Idec Research grant
Research Support, Government Entities:
1.
NIH R01 and R56 NS 041198, PI, 2000-present, R01 NS 047029, PI, 2004-present, K24 NS 060950, PI, 2008-present
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
National Multiple Sclerosis society;
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE

Notes

Correspondence & reprint requests to Dr. Koralnik: [email protected]

Author Contributions

Dr. Gheuens was involved in patient care, imaging and immunologic studies, writing the first draft of the manuscript, and preparing the figures. Dr. Smith was involved in patient care and revising the manuscript. Dr. Wang was involved in performing the imaging and collecting the MRS data and revising the manuscript. Dr. Alsop was involved in performing the imaging and collecting the MRS data and revising the manuscript. Dr. Lenkinski was involved in performing the imaging and collecting the MRS data and revising the manuscript. Dr. Koralnik was involved in patient care, imaging and immunologic studies, and supervising, editing and revising the manuscript, and preparing the figures.

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Cited By
  1. PML - opportunistische Infektion des Gehirns, InFo Neurologie + Psychiatrie, 25, 1, (24-35), (2023).https://doi.org/10.1007/s15005-022-3121-7
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  2. The Effect of Intravenous Methylprednisolone on Recurrent Exacerbation in Hematologic Malignancy-associated Progressive Multifocal Leukoencephalopathy, Internal Medicine, 60, 8, (1287-1291), (2021).https://doi.org/10.2169/internalmedicine.5917-20
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  3. Epilepsia partialis continua revealing idelalisib-associated PML-IRIS: clinical and pathological features, Journal of NeuroVirology, 26, 3, (437-441), (2019).https://doi.org/10.1007/s13365-019-00821-3
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  4. Host-Immune Interactions in JC Virus Reactivation and Development of Progressive Multifocal Leukoencephalopathy (PML), Journal of Neuroimmune Pharmacology, 14, 4, (649-660), (2019).https://doi.org/10.1007/s11481-019-09877-8
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  5. Treatment of natalizumab‐associated PML with filgrastim , Annals of Clinical and Translational Neurology, 6, 5, (923-931), (2019).https://doi.org/10.1002/acn3.776
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  6. Progressive multifocal leukoencephalopathy immune reconstitution inflammatory syndrome, Radiopaedia.org, (2017).https://doi.org/10.53347/rID-53234
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  7. Current and Emerging Therapies in Multiple Sclerosis: Implications for the Radiologist, Part 2—Surveillance for Treatment Complications and Disease Progression, American Journal of Neuroradiology, 38, 9, (1672-1680), (2017).https://doi.org/10.3174/ajnr.A5148
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  8. Metabolic profiles by 1H-magnetic resonance spectroscopy in natalizumab-associated post-PML lesions of multiple sclerosis patients who survived progressive multifocal leukoencephalopathy (PML), PLOS ONE, 12, 4, (e0176415), (2017).https://doi.org/10.1371/journal.pone.0176415
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  9. Multiple sclerosis update: use of MRI for early diagnosis, disease monitoring and assessment of treatment related complications, The British Journal of Radiology, 90, 1074, (20160721), (2017).https://doi.org/10.1259/bjr.20160721
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  10. Inflammatory natalizumab-associated PML: baseline characteristics, lesion evolution and relation with PML-IRIS, Journal of Neurology, Neurosurgery & Psychiatry, 89, 5, (535-541), (2017).https://doi.org/10.1136/jnnp-2017-316886
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