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Real world experience with teriflunomide in multiple sclerosis: the TER-Italy study

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Abstract

Objective

To identify baseline factors associated with disease activity in patients with relapsing–remitting multiple sclerosis (RRMS) under teriflunomide treatment.

Methods

This was an independent, multi-centre, retrospective post-marketing study. We analysed data of 1,507 patients who started teriflunomide since October 2014 and were regularly followed in 28 Centres in Italy. We reported the proportions of patients who discontinued treatment (after excluding 32 lost to follow-up) and who experienced clinical disease activity, i.e., relapse(s) and/or confirmed disability worsening, as assessed by the Expanded Disability Status Scale (EDSS). Decision tree-based analysis was performed to identify baseline factors associated with clinical disease activity during teriflunomide treatment.

Results

At database lock (September 2020), approximately 29% of patients (430 out of 1,475) discontinued teriflunomide because of disease activity (~ 46%), adverse events (~ 37%), poor tolerability (~ 15%), pregnancy planning (~ 2%). Approximately 28% of patients experienced disease activity over a median follow-up of 2.75 years: ~ 9% had relapses but not disability worsening; ~ 13% had isolated disability worsening; ~ 6% had both relapses and disability worsening. The most important baseline factor associated with disease activity (especially disability worsening) was an EDSS > 4.0 (p < 0.001). In patients with moderate disability level (EDSS 2.0–4.0), disease activity occurred more frequently in case of ≥ 1 pre-treatment relapses (p = 0.025). In patients with milder disability level (EDSS < 2.0), disease activity occurred more frequently after previous exposure to ≥ 2 disease-modifying treatments (p = 0.007).

Conclusions

Our study suggests a place-in-therapy for teriflunomide in naïve patients with mild disability level or in those who switched their initial treatment for poor tolerability. Adverse events related with teriflunomide were consistent with literature data, without any new safety concern.

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Data availability

The data that support the findings of this study are available from the corresponding author (luca.prosperini@gmail.com) upon reasonable request.

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Acknowledgements

Collaborator List (TER-Italy Study Group), see Supplementary Material.

Funding

None.

Author information

Authors and Affiliations

  1. Multiple Sclerosis Centre, “E. Muscatello” Hospital - ASP8, Augusta, SR, Italy

    Sebastiano Bucello

  2. UOC Centro Sclerosi Multipla, Neurologia II ASST Valle Olona, PO di Gallarate (VA), Varese, Italy

    Pietro Annovazzi & Mauro Zaffaroni

  3. Department of Biomedicine, Neurosciences and Advanced Diagnostics (BiND), University of Palermo, Palermo, Italy

    Paolo Ragonese & Alessia Bianchi

  4. Multiple Sclerosis Centre, Department of Human Neurosciences, Sapienza University, Rome, Italy

    Marta Altieri & Antonio Cortese

  5. Multiple Sclerosis Centre, Department of Neurology, Papa Giovanni XXIII Hospital, Bergamo, Italy

    Valeria Barcella

  6. Multiple Sclerosis Research Centre, IRCCS Mondino Foundation, Pavia, Italy

    Roberto Bergamaschi & Giulia Mallucci

  7. Multiple Sclerosis Centre, S. Andrea Hospital, Sapienza University, Rome, Italy

    Giovanna Borriello

  8. Centre for Experimental Neurological Therapies, S. Andrea Hospital, Department of Mental Health and Sensory Organs, Sapienza University, Rome, Italy

    Maria Chiara Buscarinu

  9. Institute Foundation “G. Giglio”, Multiple Sclerosis Centre, Cefalù-Palermo, Italy

    Graziella Callari & Luigi Maria Edoardo Grimaldi

  10. Centro di Riferimento Regionale Sclerosi Multipla (CReSM), SCDO Neurologia, AOU S. Luigi Gonzaga, Orbassano, TO, Italy

    Marco Capobianco & Marianna Lo Re

  11. Neurology, Neurophysiology and Neurobiology Unit, Department of Medicine, Università Campus Bio-Medico, Rome, Italy

    Fioravante Capone

  12. Multiple Sclerosis Centre, Department of Neurosciences, City of Health and Science University Hospital, Torino, Italy

    Paola Cavalla

  13. Multiple Sclerosis Centre, Scientific Institute S. Maria Nascente, Don Carlo Gnocchi Foundation, Milan, Italy

    Rosella Cavarretta

  14. Multiple Sclerosis Centre, S. Filippo Neri Hospital, Rome, Italy

    Antonio Cortese & Elisabetta Ferraro

  15. Multiple Sclerosis Centre, Clinical Neurology Unit, SS. Annunziata University Hospital, Chieti, Italy

    Giovanna De Luca & Valentina Tomassini

  16. Multiple Sclerosis Centre, Department of Medicine and Surgery, University Hospital, Perugia, Italy

    Massimiliano Di Filippo

  17. UOC Neurologia, G.O.M. “Bianchi Melacrino Morelli”, Reggio Calabria, Italy

    Vincenzo Dattola

  18. IRCCS Istituto Neurologico Mediterraneo (INM) Neuromed, Pozzilli, IS, Italy

    Roberta Fantozzi & Girolama Alessandra Marfia

  19. Fatebenefratelli Foundation for Health Research and Education AFaR Division, Rome, Italy

    Maria Maddalena Filippi

  20. Multiple Sclerosis Centre, Department of Neurosciences, S. Camillo-Forlanini Hospital, C.ne Gianicolense 87, 00152, Rome, Italy

    Claudio Gasperini & Luca Prosperini

  21. Multiple Sclerosis Clinical and Research Unit, Department of Systems Medicine, Tor Vergata University, Rome, Italy

    Doriana Landi & Girolama Alessandra Marfia

  22. Clinica Neurologica, Azienda Ospedaliero-Universitaria di Cattinara, Trieste, Italy

    Paolo Manganotti

  23. Centro Sclerosi Multipla, Fondazione Policlinico Universitario “A. Gemelli” IRCCS Università Cattolica del Sacro Cuore, Rome, Italy

    Massimiliano Mirabella

  24. Clinica Neurologica, Centro Sclerosi Multipla, Azienda Ospedaliera di Padova, Padova, Italy

    Paola Perini & Sofia Zywicki

  25. Unit of Neurology, Unit of Neurorehabilitation and Neurophysiology Service, IRCCS San Raffaele Institute, Milan, Italy

    Marco Pisa & Massimo Filippi

  26. Multiple Sclerosis Centre, Neurology Unit and Stroke Unit, AOOR “Villa Sofia-Cervello”, Palermo, Italy

    Sabrina Realmuto

  27. Centro Sclerosi Multipla, IRCCS Neurolesi “Bonino-Pulejo”, Messina, Italy

    Margherita Russo

  28. Institute for Advanced Biomedical Technologies (ITAB), Department of Neurosciences, Imaging and Clinical Sciences, University G. d’Annunzio of Chieti-Pescara, Chieti, Italy

    Valentina Tomassini

  29. Centro Sclerosi Multipla, UO Neuroimmunologia e Malattie Neuromuscolari, Fondazione IRCCS Ist. Neurologico C. Besta, Milan, Italy

    Valentina Liliana Adriana Torri-Clerici

  30. UOC di Neurologia, Ospedale di Mirano (VE), Mirano, Italy

    Cristina Zuliani

  31. Neuroimaging Research Unit, Division of Neuroscience, IRCCS San Raffaele Institute, Milan, Italy

    Massimo Filippi

  32. Vita-Salute San Raffaele University, Milan, Italy

    Massimo Filippi

Authors
  1. Sebastiano Bucello
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  2. Pietro Annovazzi
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  3. Paolo Ragonese
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  4. Marta Altieri
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  5. Valeria Barcella
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  6. Roberto Bergamaschi
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  7. Alessia Bianchi
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  8. Giovanna Borriello
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  9. Maria Chiara Buscarinu
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  10. Graziella Callari
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  11. Marco Capobianco
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  12. Fioravante Capone
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  13. Paola Cavalla
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  14. Rosella Cavarretta
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  15. Antonio Cortese
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  16. Giovanna De Luca
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  17. Massimiliano Di Filippo
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  18. Vincenzo Dattola
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  19. Roberta Fantozzi
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  20. Elisabetta Ferraro
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  21. Maria Maddalena Filippi
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  22. Claudio Gasperini
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  23. Luigi Maria Edoardo Grimaldi
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  24. Doriana Landi
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  25. Marianna Lo Re
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  26. Giulia Mallucci
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  27. Paolo Manganotti
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  28. Girolama Alessandra Marfia
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  29. Massimiliano Mirabella
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  30. Paola Perini
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  31. Marco Pisa
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  32. Sabrina Realmuto
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  33. Margherita Russo
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  34. Valentina Tomassini
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  35. Valentina Liliana Adriana Torri-Clerici
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  36. Mauro Zaffaroni
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  37. Cristina Zuliani
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  38. Sofia Zywicki
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  39. Massimo Filippi
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  40. Luca Prosperini
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Corresponding author

Correspondence to Luca Prosperini.

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Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Pietro Annovazzi: consulting and/or lecture fees from Mylan, Roche, Almirall e Merck, Biogen, Genzyme, Novartis and Teva. Valeria Barcella: personal compensation for advisory boards and/or speaker’s honoraria from Almirall, Biogen, Merck, Novartis, Roche and Sanofi-Genzyme. Roberto Bergamaschi: personal compensation for scientific advisory boards from Biogen and Almirall; funding for travel and speaker honoraria from Sanofi-Aventis, Genzyme, Biogen, Bayer Schering, Teva, Merck Serono, Almirall, Roche and Novartis; research support from Merck Serono, Biogen Idec, Teva, Bayer Schering, Novartis, Sanofi-Aventis. Giovanna Borriello: travel grants and lecture fees from Almirall, Biogen, Genzyme, Merck, Novartis, Roche, Teva. Maria Chiara Buscarinu: advisory board membership and honoraria for speaking from Teva, Novartis, Sanofi, Merck Serono, and Biogen. Graziella Callari: personal fees from Biogen and Sanofi; travel funding from Bayer, Biogen, and Merck. Marco Capobianco: personal compensation for advisory boards or speaker’s honoraria from Almirall, Biogen, Merck, Novartis, Roche, Sanofi-Genzyme and Teva. Fioravanti Capone: travel grants from Biogen, Merck and Sanofi-Genzyme. Paola Cavalla: personal compensation for advisory boards from Biogen Idec, Teva, Almirall, Sanofi-Genzyme and Merck-Serono; honoraria as a speaker from Biogen, Merck-Serono, Teva, Roche, Novartis and Sanofi-Genzyme; travel grants from Biogen, Merck-Serono, Teva, Roche, Novartis and Sanofi-Genzyme. Antonio Cortese: honoraria for speaking and travel grants from Biogen, Sanofi-Genzyme, and Teva. Giovanna De Luca: travel grants and/or speaker honoraria from Merck-Serono, Roche, Sanofi Genzyme and Biogen. Massimiliano Di Filippo: personal compensation for advisory boards, speaker or writing honoraria, and funding for travelling from Bayer, Biogen, Genzyme, Merck, Mylan, Novartis, Roche and Teva. Roberta Fantozzi: travel grants and/or speaker honoraria from Biogen, Merck and Roche. Massimo Filippi: Editor-in-Chief of the Journal of Neurology; compensation for consulting services and/or speaking activities from Bayer, Biogen, Merck-Serono, Novartis, Roche, Sanofi Genzyme, Takeda, and Teva Pharmaceutical Industries; research support from Biogen, Merck-Serono, Novartis, Roche, Teva Pharmaceutical Industries, Italian Ministry of Health, Fondazione Italiana Sclerosi Multipla, and ARiSLA (Fondazione Italiana di Ricerca per la SLA). Claudio Gasperini: personal compensation for advisory boards from Biogen, Teva, Bayer, Genzyme and Merck; honoraria as speaker from Biogen, Merck, Almirall, Bayer, Teva, Roche, Novartis and Sanofi-Genzyme. Luigi Maria Edoardo Grimaldi: scientific advisory board for Merck Serono; funding for travel or speaker honoraria from Merck Serono, Biogen, Sanofi-Aventis, Bayer Schering and Solvay Pharmaceuticals, Inc.; institutional research support form Teva Pharmaceuticals Industries Ltd, Biogen, Genzyme Corporation, Sanofi-Aventis, Merck Serono, Novartis and Eisai Inc.; research support from Merck Serono, Biogen and Ministero della Salute of Italy. Doriana Landi: travel funding from Biogen, Merck, Sanofi, Teva; speaking or consultations fees from Sanofi, Merck, Teva, Biogen, Roche. Girolama Alessandra Marfia: advisory board membership for Biogen, Genzyme, Merck-Serono, Novartis, and Teva; honoraria for speaking or consultation fees from Almirall, Bayer Schering, Biogen Idec, Genzyme, Merck Serono, Novartis, and Teva. Massimiliano Mirabella: membership of scientific advisory boards for Bayer Schering, Biogen, Sanofi-Genzyme, Merck, Novartis, Teva; consulting and/or speaking fees, research support or travel grants from Almirall, Bayer Schering, Biogen, CSL Behring Sanofi-Genzyme, Merck, Novartis, Teva, Roche, Ultragenix. Paola Perini: speaking honoraria and/or consultant fees from Biogen, Merck Serono, Teva, Novartis and Genzyme. Luca Prosperini: consulting fees from Biogen, Celgene, Novartis and Roche; speaker honoraria from Biogen, Genzyme, Merck Serono, Mylan, Novartis and Teva; travel grants from Biogen, Genzyme, Novartis and Teva; research grants from the Italian MS Society (Associazione Italiana Sclerosi Multipla) and Genzyme. Mauro Zaffaroni: grants for participating in advisory boards or attending scientific meetings from Biogen, Merck, Novartis and Sanofi-Genzyme. Cristina Zuliani: speaker’s honoraria and consulting fees, honoraria for advisory boards, support for attendance of scientific meetings from Almirall, Bayer Shering, Biogen, Merck Serono, Novartis, Roche, Sanofi Genzyme, and Teva. MA, AB, RC, VD, EF, MMF, MLR, GM, PM, MP, PR, MR, VT, VLAT-C, SZ, report no conflict of interest.

Ethical statement

The present study was conducted in accordance with specific national laws and the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. Given its retrospective design, in no way this study did interfere with the care received by patients.

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Bucello, S., Annovazzi, P., Ragonese, P. et al. Real world experience with teriflunomide in multiple sclerosis: the TER-Italy study. J Neurol 268, 2922–2932 (2021). https://doi.org/10.1007/s00415-021-10455-3

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