Long-term efficacy of immunoglobulins in small fiber neuropathy related to Sjögren’s syndrome

Abstract

The most common peripheral nervous system manifestations in Sjogren’s syndrome are small fiber sensory neuropathies (SFPN) and axonal sensorimotor polyneuropathies. Currently, treatment in small fiber neuropathy is mainly symptomatic and based on anti-depressors and anti-epileptics. The benefit of treatment with polyvalent immunoglobulins for SFPN has been reported in small series of patients, although transient in several cases. The medium-to-long-term effects of polyvalent immunoglobulins (Ig) in SFPN in patients with Sjogren’s syndrome who are refractory to conventional treatments remain an unmet medical need. We present our experience related to the persistent improvement of Ig in a case series of SFPN in Sjogren’s syndrome and relevant data in the literature regarding the benefits of immunoglobulins, for this indication.

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References

  1. 1.

    Binard A, Devauchelle-Pensec V, Fautrel B, Jousse S, Youinou P, Saraux A (2007) Epidemiology of Sjögren's syndrome: where are we now? Clin Exp Rheumatol 25:1–4

    CAS  PubMed  Google Scholar 

  2. 2.

    Segal B, Thomas W, Rogers T et al (2008) Prevalence, severity, and predictors of fatigue in subjects with primary Sjögren's syndrome. Arthritis Rheum 59:1780–1787

    PubMed  PubMed Central  Google Scholar 

  3. 3.

    Ramos-Casals M, Solans R, Rosas J, GEMESS Study Group et al (2008) Primary Sjögren syndrome in Spain: clinical and immunologic expression in 1010 patients. Medicine 87:210–219

    CAS  PubMed  Google Scholar 

  4. 4.

    Pavlakis PP, Alexopoulos H, Kosmidis ML et al (2011) Peripheral neuropathies in Sjogren syndrome: a new reappraisal. J Neurol Neurosurg Psychiatry 82:798–802

    PubMed  Google Scholar 

  5. 5.

    Mori K, Iijima M, Koike H et al (2005) The wide spectrum of clinical manifestations in Sjögren's syndrome-associated neuropathy. Brain 128:2518–2534

    PubMed  Google Scholar 

  6. 6.

    Delalande S, de Seze J, Fauchais AL et al (2004) Neurologic manifestations in primary Sjögren syndrome: a study of 82 patients. Medicine 83:280–291

    PubMed  Google Scholar 

  7. 7.

    Devigili G, Tugnoli V, Penza P et al (2008) The diagnostic criteria for small fibre neuropathy: from symptoms to neuropathology. Brain 131:1912–1925

    PubMed  PubMed Central  Google Scholar 

  8. 8.

    Gorson KC, Ropper AH (1995) Idiopathic distal small fiber neuropathy. Acta Neurol Scand 92:376–382

    CAS  PubMed  Google Scholar 

  9. 9.

    De Sousa EA, Hays AP, Chin RL, Sander HW, Brannagan TH (2006) Characteristics of patients with sensory neuropathy diagnosed with abnormal small nerve fibres on skin biopsy. J Neurol Neurosurg Psychiatry 77:983–985

    PubMed  PubMed Central  Google Scholar 

  10. 10.

    Chai J, Herrmann DN, Stanton M, Barbano RL, Logigian EL (2005) Painful small-fiber neuropathy in Sjogren syndrome. Neurology 65:925–927

    CAS  PubMed  Google Scholar 

  11. 11.

    Hoeijmakers JG, Faber CG, Lauria G, Merkies IS, Waxman SG (2012) Small-fibre neuropathies—advances in diagnosis, pathophysiology and management. Nat Rev Neurol 8:369–379

    CAS  PubMed  Google Scholar 

  12. 12.

    Oaklander AL, Klein MM (2013) Evidence of small-fiber polyneuropathy in unexplained, juvenile-onset, widespread pain syndromes. Pediatrics 131:e1091–e1100

    PubMed  PubMed Central  Google Scholar 

  13. 13.

    Lang M, Treister R, Oaklander AL (2016) Diagnostic value of blood tests for occult causes of initially idiopathic small-fiber polyneuropathy. J Neurol 263:2515–2527

    CAS  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Moulin D, Boulanger A, Clark AJ, Canadian Pain Society et al (2014) Pharmacological management of chronic neuropathic pain: revised consensus statement from the Canadian Pain Society. Pain Res Manag 19:328–335

    PubMed  PubMed Central  Google Scholar 

  15. 15.

    Gorson KC, Herrmann DN, Thiagarajan R et al (2008) Non-length dependent small fibre neuropathy/ganglionopathy. J Neurol Neurosurg Psychiatry 79:163–169

    CAS  PubMed  Google Scholar 

  16. 16.

    Dabby R, Gilad R, Sadeh M, Lampl Y, Watemberg N (2006) Acute steroid responsive small-fiber sensory neuropathy: a new entity? J Peripher Nerv Syst 11:47–52

    PubMed  Google Scholar 

  17. 17.

    Sève P, Gachon E, Petiot P, Stankovic K, Charhon A, Broussolle C (2007) Successful treatment with rituximab in a patient with mental nerve neuropathy in primary Sjögren's syndrome. Rheumatol Int 28:175–177

    PubMed  Google Scholar 

  18. 18.

    Mekinian A, Ravaud P, Hatron PY et al (2012) Efficacy of rituximab in primary Sjogren's syndrome with peripheral nervous system involvement: results from the AIR registry. Ann Rheum Dis 71:84–87

    CAS  PubMed  Google Scholar 

  19. 19.

    Wakasugi D, Kato T, Gono T et al (2009) Extreme efficacy of intravenous immunoglobulin therapy for severe burning pain in a patient with small fiber neuropathy associated with primary Sjögren's syndrome. Mod Rheumatol 19:437–440

    PubMed  Google Scholar 

  20. 20.

    Morozumi S, Kawagashira Y, Iijima M et al (2009) Intravenous immunoglobulin treatment for painful sensory neuropathy associated with Sjögren's syndrome. J Neurol Sci 279:57–61

    CAS  PubMed  Google Scholar 

  21. 21.

    Molina JA, Benito-León J, Bermejo F, Jiménez-Jiménez FJ, Oliván J (1996) Intravenous immunoglobulin therapy in sensory neuropathy associated with Sjögren's syndrome. J Neurol Neurosurg Psychiatry 60:699

    CAS  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Kizawa M, Mori K, Iijima M, Koike H, Hattori N, Sobue G (2006) Intravenous immunoglobulin treatment in painful sensory neuropathy without sensory ataxia associated with Sjögren's syndrome. J Neurol Neurosurg Psychiatry 77:967–969

    CAS  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Dalakas MC (2004) Intravenous immunoglobulin in autoimmune neuromuscular diseases. JAMA 291:2367–2375

    CAS  PubMed  Google Scholar 

  24. 24.

    Vitali C, Bombardieri S, Jonsson R, European Study Group on Classification Criteria for Sjögren's Syndrome et al (2002) Classification criteria for Sjögren's syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis 61:554–558

    CAS  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Lauria G, Hsieh ST, Johansson O, Kennedy WR et al (2010) European Federation of Neurological Societies/Peripheral Nerve Society Guideline on the Use of Skin Biopsy in the Diagnosis of Small Fiber Neuropathy. Report of a Joint Task Force of the European Federation of Neurological Societies and the Peripheral Nerve Society. Eur J Neurol. 17(7):903–912

    CAS  PubMed  Google Scholar 

  26. 26.

    Souayah N, Chin RL, Brannagan TH et al (2008) Effect of intravenous immunoglobulin on cerebellar ataxia and neuropathic pain associated with celiac disease. Eur J Neurol 15:1300–1303

    CAS  PubMed  Google Scholar 

  27. 27.

    Parambil JG, Tavee JO, Zhou L, Pearson KS, Culver DA (2011) Efficacy of intravenous immunoglobulin for small fiber neuropathy associated with sarcoidosis. Respir Med 105:101–105

    PubMed  Google Scholar 

  28. 28.

    Hughes RA, Donofrio P, Bril V, ICE Study Group et al (2008) Intravenous immune globulin (10% caprylate-chromatography purified) for the treatment of chronic inflammatory demyelinating polyradiculoneuropathy (ICE study): a randomised placebo-controlled trial. Lancet Neurol 7:136–144

    CAS  PubMed  Google Scholar 

  29. 29.

    Léger JM, De Bleecker JL, Sommer C, PRIMA study investigators et al (2013) Efficacy and safety of Privigen(®) in patients with chronic inflammatory demyelinating polyneuropathy: results of a prospective, single-arm, open-label Phase III study (the PRIMA study). J Peripher Nerv Syst. 18:130–140

    PubMed  PubMed Central  Google Scholar 

  30. 30.

    Kubori T, Mezaki T, Kaji R et al (1999) The clinical usefulness of high-dose intravenous immunoglobulin therapy for chronic inflammatory demyelinating polyneuropathy and multifocal motor neuropathy]. No To Shinkei 51:127–135

    CAS  PubMed  Google Scholar 

  31. 31.

    van Schaik IN, Bril V, van Geloven N, PATH Study Group et al (2018) Subcutaneous immunoglobulin for maintenance treatment in chronic inflammatory demyelinating polyneuropathy (PATH): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Neurol 17:35–46

    PubMed  Google Scholar 

  32. 32.

    Mahdi-Rogers M, Brassington R, Gunn AA, van Doorn PA, Hughes RA (2017) Immunomodulatory treatment other than corticosteroids, immunoglobulin and plasma exchange for chronic inflammatory demyelinating polyradiculoneuropathy. Cochrane Database Syst Rev 5:CD003280

    PubMed  Google Scholar 

  33. 33.

    van der Meche FG, Schmitz PI (1992) A randomized trial comparing intravenous immune globulin and plasma exchange in Guillain-Barre syndrome. Dutch Guillain-Barre Study Group. N Engl J Med 326:1123–1129

    PubMed  Google Scholar 

  34. 34.

    Hughes RA (1996) Intravenous IgG in Guillain-Barré syndrome. BMJ 313:376–377

    CAS  PubMed  PubMed Central  Google Scholar 

  35. 35.

    Pereira PR, Viala K, Maisonobe T et al (2016) Sjögren sensory neuronopathy (Sjögren Ganglionopathy): long-term outcome and treatment response in a series of 13 cases. Medicine 95:e3632

    PubMed  PubMed Central  Google Scholar 

  36. 36.

    Takahashi Y, Takata T, Hoshino M, Sakurai M, Kanazawa I (2003) Benefit of IVIG for long-standing ataxic sensory neuronopathy with Sjogren’s syndrome. IV immunoglobulin. Neurology 60:503–505

    CAS  PubMed  Google Scholar 

  37. 37.

    Rist S, Sellam J, Hachulla E et al (2011) Club Rhumatismes et inflammation. Experience of intravenous immunoglobulin therapy in neuropathy associated with primary Sjögren's syndrome: a national multicentric retrospective study. Arthritis Care Res (Hoboken) 63:1339–1344

    Google Scholar 

  38. 38.

    Birnbaum J (2010) Peripheral nervous system manifestations of Sjogren syndrome: clinical patterns, diagnostic paradigms, etiopathogenesis, and therapeutic strategies. Neurologist 16:287–297

    PubMed  Google Scholar 

  39. 39.

    Liu X, Treister T, Lang M, Oaklander AL (2018) IVIg for apparently autoimmune small-fiber polyneuropathy: first analysis of efficacy and safety. Ther Adv Neurol Disord 11:1756285617744484

    PubMed  PubMed Central  Google Scholar 

  40. 40.

    de Greef BT, Geerts M, Hoeijmakers JG, Faber CG, Merkies IS (2016) Intravenous immunoglobulin therapy for small fiber neuropathy: study protocol for a randomized controlled trial. Trials 17:330

    PubMed  PubMed Central  Google Scholar 

  41. 41.

    Kuitwaard K, van den Berg LH, Vermeulen M et al (2010) Randomised controlled trial comparing two different intravenous immunoglobulins in chronic inflammatory demyelinating polyradiculoneuropathy. J Neurol Neurosurg Psychiatry 81:1374–1379

    CAS  PubMed  Google Scholar 

  42. 42.

    Rajabally YA, Kearney DA (2011) Thromboembolic complications of intravenous immunoglobulin therapy in patients with neuropathy: a two-year study. J Neurol Sci 308:124–127

    CAS  PubMed  Google Scholar 

  43. 43.

    Mohamed M (2016) Intravenous immunoglobulin-associated hemolysis: risk factors, challenges, and solutions. Int J Clin Transfus Med 4:121–131

    Google Scholar 

  44. 44.

    van Schaik IN, van den Berg LH, de Haan R, Vermeulen M (2005) Intravenous immunoglobulin for multifocal motor neuropathy. Cochrane Database Syst Rev 18:CD004429

    Google Scholar 

  45. 45.

    Rajabally YA, Seow H, Wilson P (2006) Dose of intravenous immunoglobulins in chronic inflammatory demyelinating polyneuropathy. J Peripher Nerv Syst 11:325–329

    CAS  PubMed  Google Scholar 

  46. 46.

    Lunn MP, Ellis L, Hadden RD, Rajabally YA, Winer JB, Reilly MM (2016) A proposed dosing algorithm for the individualized dosing of human immunoglobulin in chronic inflammatory neuropathies. J Peripher Nerv Syst 21:33–37

    CAS  PubMed  Google Scholar 

  47. 47.

    Cornblath DR, Hartung HP, Katzberg HD, Merkies ISJ, van Doorn PA (2018) A randomised, multi-centre phase III study of 3 different doses of intravenous immunoglobulin 10% in patients with chronic inflammatory demyelinating polyradiculoneuropathy (ProCID trial): Study design and protocol. J Peripher Nerv Syst 23:108–114

    CAS  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Oaklander AL, Lang M, Treister R, Liu X (2015) First evaluation of immunoglobulin treatment of small-fiber axonal polyneuropathy (SFPN). Ann Neurol 78:S109

    Google Scholar 

  49. 49.

    Cherin P, Belizna C, Cartry O et al (2016) Long-term subcutaneous immunoglobulin use in inflammatory myopathies: A retrospective review of 19 cases. Autoimmun Rev 15:281–286

    CAS  PubMed  Google Scholar 

  50. 50.

    Cocito D, Merola A, Peci E et al (2014) SCIg and chronic dysimmune neuropathies Italian Network. Subcutaneous immunoglobulin in CIDP and MMN: a short-term nationwide study. J Neurol. 261:2159–2164

    CAS  PubMed  Google Scholar 

  51. 51.

    Racosta JM, Sposato LA, Kimpinski K (2017) Subcutaneous versus intravenous immunoglobulin for chronic autoimmune neuropathies: a meta-analysis. Muscle Nerve 55:802–809

    CAS  PubMed  Google Scholar 

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Funding

The authors have no financial relationships relevant to this article to disclose.

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Correspondence to Taylor Pindi Sala.

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Conflicts of interest

The study is not industry sponsored. Dr. Pindi Sala reports no disclosures. Mrs Mona Villedieu reports no disclosures. Dr Laura Damian reports no disclosures. Mr Jean-Charles Crave reports no disclosures. Dr Vivien Pautot reports no disclosures. Professor Ljudmila Stojanovich reports no disclosures. Professor Jan Willem Cohen Tervaert reports no disclosures. Professor Patrick Cherin reports no disclosures. Dr. Cristina Belizna reports no disclosures.

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No ethics committee approval was required for this report.

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As per local legislation, patients were informed that data from their treatment may be reported and did not refuse the anonymous dissemination of this information.

Appendix 1-Authors

Appendix 1-Authors

All authors approved the final manuscript as submitted and agree to be accountable for all aspects of the work.

Name Location Contribution
Taylor Pindi Sala University Paris Diderot, EA 7334, Patient Centered Outcomes Research, Paris, France Conceptualized and designed the study, collected data, and reviewed and revised the manuscript for important intellectual content
Mona Villedieu Octapharma, 92,100 Boulogne Billancourt, France Conceptualized and designed the study, collected data, and reviewed and revised the manuscript for important intellectual content
Jean-Charles Crave Octapharma, 92,100 Boulogne Billancourt, France Conceptualized and designed the study, collected data, and reviewed and revised the manuscript for important intellectual content
Laura Damian Department of Rheumatology, County Emergency Hospital Cluj-Napoca, Cluj-Napoca, Romania Conceptualized and designed the study, collected data, and reviewed and revised the manuscript for important intellectual content
Vivien Pautot Department of Neurology University Hospital Angers, Angers, France Conceptualized and designed the study, collected data, and reviewed and revised the manuscript for important intellectual content
Ljudmila Stojanovich Scientific Research Department, Internal Medicine-Rheumatology Bezhanijska Kosa, University Medical Center, Belgrade University, Serbia Conceptualized and designed the study, collected data, and reviewed and revised the manuscript for important intellectual content
Jan Willem Cohen Tervaert Department of Medicine, Division of Rheumatology University of Alberta, Edmonton, AB, Canada Conceptualized and designed the study, collected data, and reviewed and revised the manuscript for important intellectual content
Patrick Cherin Internal Medicine Department Hôpital Pitié-Salpétrière, 75,013 Paris Coordinated and conceptualized and designated the study and critically reviewed the manuscript for important intellectual content
Cristina Belizna Vascular and Coagulation Department, University Hospital Angers, Angers, France
CNRS 6015 INSERMU1083, UMR, Angers, France
Coordinated and conceptualized and designated the study and critically reviewed the manuscript for important intellectual content

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Pindi Sala, T., Villedieu, M., Damian, L. et al. Long-term efficacy of immunoglobulins in small fiber neuropathy related to Sjögren’s syndrome. J Neurol 267, 3499–3507 (2020). https://doi.org/10.1007/s00415-020-10033-z

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Keywords

  • Small fiber sensory neuropathies and sjögren syndrome
  • Small fiber sensory neuropathies and sjögren syndrome and treatment
  • Small fiber sensory neuropathies in sjögren syndrome and immunoglobulins
  • Small fiber sensory neuropathies in sjögren syndrome and intravenous immunoglobulins
  • Small fiber sensory neuropathies in sjögren syndrome and subcutaneous immunoglobulins