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New Algorithms Improving PML Risk Stratification in MS Patients Treated With Natalizumab

Publicated to:Frontiers In Neurology. 11 579438- - 2020-12-17 11(), DOI: 10.3389/fneur.2020.579438

Authors: Toboso, Inmaculada; Tejeda-Velarde, Amalia; Alvarez-Lafuente, Roberto; Arroyo, Rafael; Hegen, Harald; Deisenhammer, Florian; Sainz de la Maza, Susana; Alvarez-Cermeno, Jose C; Izquierdo, Guillermo; Paramo, Dolores; Oliva, Pedro; Casanova, Bonaventura; Aguera-Morales, Eduardo; Franciotta, Diego; Gastaldi, Matteo; Fernandez, Oscar; Urbaneja, Patricia; Garcia-Dominguez, Jose M; Romero, Fernando; Laroni, Alicia; Uccelli, Antonio; Perez-Sempere, Angel; Saiz, Albert; Blanco, Yolanda; Galimberti, Daniela; Scarpini, Elio; Espejo, Carmen; Montalban, Xavier; Rasche, Ludwig; Paul, Friedemann; Gonzalez, Ines; Alvarez, Elena; Ramo, Cristina; Caminero, Ana B; Aladro, Yolanda; Calles, Carmen; Eguia, Pablo; Belenguer-Benavides, Antonio; Ramio-Torrenta, Lluis; Quintana, Ester; Martinez-Rodriguez, Jose E; Oterino, Agustin; Lopez de Silanes, Carlos; Casanova, Luis I; Landete, Lamberto; Frederiksen, Jette; Bsteh, Gabriel; Mulero, Patricia; Comabella, Manuel; Hernandez, Miguel A; Espino, Mercedes; Prieto, Jose M; Perez, Domingo; Otano, Maria; Padilla, Francisco; Garcia-Merino, Juan A; Navarro, Laura; Muriel, Alfonso; Frossard, Lucienne Costa; Villar, Luisa M

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Abstract

© Copyright © 2020 Toboso, Tejeda-Velarde, Alvarez-Lafuente, Arroyo, Hegen, Deisenhammer, Sainz de la Maza, Alvarez-Cermeño, Izquierdo, Paramo, Oliva, Casanova, Agüera-Morales, Franciotta, Gastaldi, Fernández, Urbaneja, Garcia-Dominguez, Romero, Laroni, Uccelli, Perez-Sempere, Saiz, Blanco, Galimberti, Scarpini, Espejo, Montalban, Rasche, Paul, González, Álvarez, Ramo, Caminero, Aladro, Calles, Eguía, Belenguer-Benavides, Ramió-Torrentà, Quintana, Martínez-Rodríguez, Oterino, López de Silanes, Casanova, Landete, Frederiksen, Bsteh, Mulero, Comabella, Hernández, Espiño, Prieto, Pérez, Otano, Padilla, García-Merino, Navarro, Muriel, Frossard and Villar. Overview: We assessed the role of age and disease activity as new factors contributing to establish the risk of progressive multifocal leucoencephalopathy in multiple sclerosis patients treated with natalizumab in 36 University Hospitals in Europe. We performed the study in 1,307 multiple sclerosis patients (70.8% anti-John Cunninghan virus positive antibodies) treated with natalizumab for a median time of 3.28 years. Epidemiological, clinical, and laboratory variables were collected. Lipid-specific IgM oligoclonal band status was available in 277 patients. Factors associated with progressive multifocal leucoencephalopathy onset were explored by uni- and multivariate logistic regression. Results: Thirty-five patients developed progressive multifocal leucoencephalopathy. The multivariate analysis identified anti-John Cunninghan virus antibody indices and relapse rate as the best predictors for the onset of this serious opportunistic infection in the whole cohort. They allowed to stratify progressive multifocal leucoencephalopathy risk before natalizumab initiation in individual patients [area under the curve (AUC) = 0.85]. The risk ranged from <1/3,300 in patients with anti-John Cunninghan virus antibody indices <0.9 and relapse rate >0.5, to 1/50 in the opposite case. In patients with lipid-specific IgM oligoclonal bands assessment, age at natalizumab onset, anti-John Cunninghan virus antibody indices, and lipid-specific IgM oligoclonal band status predicted progressive multifocal leucoencephalopathy risk (AUC = 0.92). The absence of lipid-specific IgM oligoclonal bands was the best individual predictor (OR = 40.94). The individual risk ranged from <1/10,000 in patients younger than 45 years at natalizumab initiation, who showed anti John Cunningham virus antibody indices <0.9 and lipid-specific IgM oligoclonal bands to 1/33 in the opposite case. Conclusions: In a perspective of personalized medicine, disease activity, anti-lipid specific IgM oligoclonal bands, anti Jonh Cunninghan virus antibody levels, and age can help tailor natalizumab therapy in multiple sclerosis patients, as predictors of progressive multifocal leucoencephalopathy.

Keywords

biomarkersdemyelinating diseasesdisease modifying treatmentsmultiple sclerosisnatalizumabAlemtuzumabBiomarkerBiomarkersDemyelinating diseasesDiseaseDisease modifying treatmentsMultiple sclerosisMultiple-sclerosisNatalizumabProgressive multifocal leucoencephalopathyProgressive multifocal leukoencephalopathyTrial

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal Frontiers In Neurology due to its progression and the good impact it has achieved in recent years, according to the agency WoS (JCR), it has become a reference in its field. In the year of publication of the work, 2020, it was in position 72/208, thus managing to position itself as a Q2 (Segundo Cuartil), in the category Clinical Neurology. Notably, the journal is positioned en el Cuartil Q2 para la agencia Scopus (SJR) en la categoría Neurology (Clinical).

From a relative perspective, and based on the normalized impact indicator calculated from the Field Citation Ratio (FCR) of the Dimensions source, it yields a value of: 4.08, which indicates that, compared to works in the same discipline and in the same year of publication, it ranks as a work cited above average. (source consulted: Dimensions Jun 2025)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2025-06-06, the following number of citations:

  • WoS: 10
  • Scopus: 12
  • Europe PMC: 6
  • OpenCitations: 10

Impact and social visibility

From the perspective of influence or social adoption, and based on metrics associated with mentions and interactions provided by agencies specializing in calculating the so-called "Alternative or Social Metrics," we can highlight as of 2025-06-06:

  • The use, from an academic perspective evidenced by the Altmetric agency indicator referring to aggregations made by the personal bibliographic manager Mendeley, gives us a total of: 33.
  • The use of this contribution in bookmarks, code forks, additions to favorite lists for recurrent reading, as well as general views, indicates that someone is using the publication as a basis for their current work. This may be a notable indicator of future more formal and academic citations. This claim is supported by the result of the "Capture" indicator, which yields a total of: 30 (PlumX).

With a more dissemination-oriented intent and targeting more general audiences, we can observe other more global scores such as:

  • The Total Score from Altmetric: 9.25.
  • The number of mentions on the social network X (formerly Twitter): 1 (Altmetric).

It is essential to present evidence supporting full alignment with institutional principles and guidelines on Open Science and the Conservation and Dissemination of Intellectual Heritage. A clear example of this is:

  • The work has been submitted to a journal whose editorial policy allows open Open Access publication.

Leadership analysis of institutional authors

This work has been carried out with international collaboration, specifically with researchers from: Austria; Denmark; Germany; Italy.