Sjögren syndrome-associated small fiber neuropathy: Characterization from a prospective series of 40 cases

Medicine (United States)

Volumn 92, Issue 5, 2013, Pages

  Sène, Damien ^a   Cacoub, Patrice ^b   Authier, François Jérôme ^c,d   Haroche, Julien ^b   Créange, Alain ^d   Saadoun, David ^b   Amoura, Zahir ^b   Guillausseau, Pierre Jean ^d   Lefaucheur, Jean Pascal ^a  

^a HÔPITAL LARIBOISIÈRE   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c HENRI MONDOR HOSPITAL   (France)

^d UNIVERSITÉ PARIS EST CRÉTEIL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINUCLEAR ANTIBODY; AZATHIOPRINE; CLONAZEPAM; DULOXETINE; GABAPENTIN; HYDROXYCHLOROQUINE; METHOTREXATE; MORPHINE SULFATE; PARACETAMOL; PREGABALIN; RHEUMATOID FACTOR; STEROID; TRAMADOL;

ADULT; ALLODYNIA; ARTHRALGIA; ARTICLE; B LYMPHOCYTE ACTIVATION; CLINICAL ARTICLE; CLINICAL FEATURE; CONSTIPATION; CONTROLLED STUDY; DYSAUTONOMIA; ENZYME LINKED IMMUNOSORBENT ASSAY; ERYTHROMELALGIA; EVOKED RESPONSE; FEMALE; HOT FLUSH; HUMAN; HUMAN TISSUE; HYPERGAMMAGLOBULINEMIA; HYPERHIDROSIS; IMMUNOFLUORESCENCE; MALE; NERVE CONDUCTION; NERVE FIBER; PAIN; PARESTHESIA; PRIORITY JOURNAL; SJOEGREN SYNDROME; SKIN BIOPSY; SMALL FIBER NEUROPATHY; XEROSTOMIA;

EID: 84888005489     PISSN: 00257974     EISSN: 15365964     Source Type: Journal    
DOI: 10.1097/MD.0000000000000005     Document Type: Article

References (61)

1. Barendregt PJ, van den Bent MJ, van Raaij-van den Aarssen VJ, van den Meiracker AH, Vecht CJ, van der Heijde GL, Markusse HM. Involvement of the peripheral nervous system in primary Sjogren's syndrome. Ann Rheum Dis. 2001;60:876-881.
2. Bouhassira D, Attal N, Alchaar H, Boureau F, Brochet B, Bruxelle J, Cunin G, Fermanian J, Ginies P, Grun-Overdyking A, Jafari-Schluep H, Lanteri-Minet M, Laurent B, Mick G, Serrie A, Valade D, Vicaut E. Comparison of pain syndromes associated with nervous or somatic lesions and development of a new neuropathic pain diagnostic questionnaire (DN4). Pain. 2005;114:29-36.
3. Casanova-Molla J, Grau-Junyent JM, Morales M, Valls-Sole J. On the relationship between nociceptive evoked potentials and intraepidermal nerve fiber density in painful sensory polyneuropathies. Pain. 2011;152:410-418.
4. Chai J, Herrmann DN, Stanton M, Barbano RL, Logigian EL. Painful small-fiber neuropathy in Sjogren syndrome. Neurology. 2005;65:925-927.
5. Chao CC, Tseng MT, Lin YJ, Yang WS, Hsieh SC, Lin YH, Chiu MJ, Chang YC, Hsieh ST. Pathophysiology of neuropathic pain in type 2 diabetes: skin denervation and contact heat-evoked potentials. Diabetes Care. 2010;33:2654-2659.
6. Cruccu G, Anand P, Attal N, Garcia-Larrea L, Haanpaa M, Jorum E, Serra J, Jensen TS. EFNS guidelines on neuropathic pain assessment. Eur J Neurol. 2004;11:153-162.
7. Davidson BK, Kelly CA, Griffiths ID. Primary Sjogren's syndrome in the North East of England: a long-term follow-up study. Rheumatology (Oxford). 1999;38:245-253.
8. Denislic M, Meh D. Neurophysiological assessment of peripheral neuropathy in primary Sjogren's syndrome. Clin Investig. 1994;72:822-829.
9. Devigili G, Tugnoli V, Penza P, Camozzi F, Lombardi R, Melli G, Broglio L, Granieri E, Lauria G. The diagnostic criteria for small fibre neuropathy: from symptoms to neuropathology. Brain. 2008;131:1912-1925.
10. England JD, Gronseth GS, Franklin G, Carter GT, Kinsella LJ, Cohen JA, Asbury AK, Szigeti K, Lupski JR, Latov N, Lewis RA, Low PA, Fisher MA, Herrmann DN, Howard JF Jr, Lauria G, Miller RG, Polydefkis M, Sumner AJ. Practice parameter: evaluation of distal symmetric polyneuropathy: role of autonomic testing, nerve biopsy, and skin biopsy (an evidence-based review). Report of the American Academy of Neurology, American Association of Neuromuscular and Electrodiagnostic Medicine, and American Academy of Physical Medicine and Rehabilitation. Neurology. 2009;72:177-184.
11. Faber CG, Hoeijmakers JG, Ahn HS, Cheng X, Han C, Choi JS, Estacion M, Lauria G, Vanhoutte EK, Gerrits MM, Dib-Hajj S, Drenth JP, Waxman SG, Merkies IS. Gain of function Nanu1.7 mutations in idiopathic small fiber neuropathy. Ann Neurol. 2012;71:26-39.
12. Fauchais AL, Martel C, Gondran G, Lambert M, Launay D, Jauberteau MO, Hachulla E, Vidal E, Hatron PY. Immunological profile in primary Sjogren syndrome: clinical significance, prognosis and long-term evolution to other auto-immune disease. Autoimmun Rev. 2010;9:595-599.
13. Fauchais AL, Richard L, Gondran G, Ghorab K, Palat S, Bezanahary H, Loustaud-Ratti V, Ly K, Jauberteau MO, Vallat JM, Vidal E, Magy L. Small fibre neuropathy in primary Sjogren syndrome. Rev Med Interne. 2011;32:142-148.
14. Fox RI. Sjogren's syndrome. Lancet. 2005;366:321-331.
15. Garcia-Carrasco M, Ramos-Casals M, Rosas J, Pallares L, Calvo-Alen J, Cervera R, Font J, Ingelmo M. Primary Sjogren syndrome: clinical and immunologic disease patterns in a cohort of 400 patients. Medicine (Baltimore). 2002;81:270-280.
16. Gemignani F, Giovanelli M, Vitetta F, Santilli D, Bellanova MF, Brindani F, Marbini A. Non-length dependent small fiber neuropathy. a prospective case series. J Peripher Nerv Syst. 2010;15:57-62.
17. Gemignani F, Marbini A, Pavesi G, Di Vittorio S, Manganelli P, Cenacchi G, Mancia D. Peripheral neuropathy associated with primary Sjogren's syndrome. J Neurol Neurosurg Psychiatry. 1994;57:983-986.
18. Gono T, Kawaguchi Y, Katsumata Y, Takagi K, Tochimoto A, Baba S, Okamoto Y, Ota Y, Yamanaka H. Clinical manifestations of neurological involvement in primary Sjogren's syndrome. Clin Rheumatol. 2011;30:485-490.
19. Goransson LG, Brun JG, Harboe E, Mellgren SI, Omdal R. Intraepidermal nerve fiber densities in chronic inflammatory autoimmune diseases. Arch Neurol. 2006;63:1410-1413.
20. Goransson LG, Herigstad A, Tjensvoll AB, Harboe E, Mellgren SI, Omdal R. Peripheral neuropathy in primary sjogren syndrome: a population-based study. Arch Neurol. 2006;63:1612-1615.
21. Gorson KC, Herrmann DN, Thiagarajan R, Brannagan TH, Chin RL, Kinsella LJ, Ropper AH. Non-length dependent small fibre neuropathy/ ganglionopathy. J Neurol Neurosurg Psychiatry. 2008;79:163-169.
22. Gorson KC, Ropper AH. Positive salivary gland biopsy, Sjogren syndrome, and neuropathy: clinical implications. Muscle Nerve. 2003;28:553-560.
23. Grant IA, Hunder GG, Homburger HA, Dyck PJ. Peripheral neuropathy associated with sicca complex. Neurology. 1997;48:855-862.
24. Han C, Hoeijmakers JG, Ahn HS, Zhao P, Shah P, Lauria G, Gerrits MM, te Morsche RH, Dib-Hajj SD, Drenth JP, Faber CG, Merkies IS, Waxman SG. Nav1.7-related small fiber neuropathy: impaired slow-inactivation and DRG neuron hyperexcitability. Neurology. 2012;78:1635-1643.
25. Ioannidis JP, Vassiliou VA, Moutsopoulos HM. Long-term risk of mortality and lymphoproliferative disease and predictive classification of primary Sjogren's syndrome. Arthritis Rheum. 2002;46:741-747.
26. Kawagashira Y, Koike H, Fujioka Y, Hashimoto R, Tomita M, Morozumi S, Iijima M, Katsuno M, Tanaka F, Sobue G. Differential, size-dependent sensory neuron involvement in the painful and ataxic forms of primary Sjogren's syndrome-associated neuropathy. J Neurol Sci. 2012;319:139-146.
27. Khan S, Zhou L. Characterization of non-length-dependent small-fiber sensory neuropathy. Muscle Nerve. 2012;45:86-91.
28. Kizawa M, Mori K, Iijima M, Koike H, Hattori N, Sobue G. Intravenous immunoglobulin treatment in painful sensory neuropathy without sensory ataxia associated with Sjogren's syndrome. J Neurol Neurosurg Psychiatry. 2006;77:967-969.
29. Lafitte C, Amoura Z, Cacoub P, Pradat-Diehl P, Picq C, Salachas F, Leger JM, Piette JC, Delattre JY. Neurological complications of primary Sjogren's syndrome. J Neurol. 2001;248:577-584.
30. Lauria G, Cornblath DR, Johansson O, McArthur JC, Mellgren SI, Nolano M, Rosenberg N, Sommer C. EFNS guidelines on the use of skin biopsy in the diagnosis of peripheral neuropathy. Eur J Neurol. 2005;12:747-758.
31. Lauria G, Hsieh ST, Johansson O, Kennedy WR, Leger JM, Mellgren SI, Nolano M, Merkies IS, Polydefkis M, Smith AG, Sommer C, Valls-Sole J. 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. 2010;17:903-912, e44-9.
32. Lefaucheur JP, Ahdab R, Ayache SS, Lefaucheur-Menard I, Rouie D, Tebbal D, Neves DO, Ciampi de Andrade D. Pain-related evoked potentials: a comparative study between electrical stimulation using a concentric planar electrode and laser stimulation using a CO2 laser. Neurophysiol Clin. 2012;42:199-206.
33. Lefaucheur JP, Brusa A, Creange A, Drouot X, Jarry G. Clinical application of laser evoked potentials using the Nd:YAG laser. Neurophysiol Clin. 2002;32:91-98.
34. Lefaucheur JP, Creange A. Neurophysiological testing correlates with clinical examination according to fibre type involvement and severity in sensory neuropathy. J Neurol Neurosurg Psychiatry. 2004;75:417-422.
35. Lefaucheur JP, NgWing Tin S, Kerschen P, Damy T, Plante-Bordeneuve V. Neurophysiological markers of small fibre neuropathy in TTR-FAP mutation carriers. J Neurol. 2013;260:1497-1503.
36. Lopate G, Pestronk A, Al-Lozi M, Lynch T, Florence J, Miller T, Levine T, Rampy T, Beson B, Ramneantu I. Peripheral neuropathy in an outpatient cohort of patients with Sjogren's syndrome. Muscle Nerve. 2006;33:672-676.
37. Loseth S, Mellgren SI, Jorde R, Lindal S, Stalberg E. Polyneuropathy in type 1 and type 2 diabetes: comparison of nerve conduction studies, thermal perception thresholds and intraepidermal nerve fibre densities. Diabetes Metab Res Rev. 2010;26:100-106.
38. Loseth S, Stalberg E, Jorde R, Mellgren SI. Early diabetic neuropathy: thermal thresholds and intraepidermal nerve fibre density in patients with normal nerve conduction studies. J Neurol. 2008;255:1197-1202.
39. Lund C, Koskinen M, Suneetha S, Lockwood DN, Haanpaa M, Haapasalo H, Hietaharju A. Histopathological and clinical findings in leprosy patients with chronic neuropathic pain: a study from Hyderabad, India. Lepr Rev. 2007;78:369-380.
40. Magy L, Richard L, Vallat JM. Usefulness of skin biopsy in the diagnosis of small fiber neuropathy. Presse Med. 2012;41:575-579.
41. Maisonobe T, Le Forestier N, Bouche P. Electrophysiologic study, diagnosis and cases of acquired sensory polyneuropathy. Neurophysiol Clin. 1996;26:202-215.
42. Mori K, Iijima M, Koike H, Hattori N, Tanaka F, Watanabe H, Katsuno M, Fujita A, Aiba I, Ogata A, Saito T, Asakura K, Yoshida M, Hirayama M, Sobue G. The wide spectrum of clinical manifestations in Sjogren's syndrome-associated neuropathy. Brain. 2005;128:2518-2534.
43. Morozumi S, Kawagashira Y, Iijima M, Koike H, Hattori N, Katsuno M, Tanaka F, Sobue G. Intravenous immunoglobulin treatment for painful sensory neuropathy associated with Sjogren's syndrome. J Neurol Sci. 2009;279:57-61.
44. Moutsopoulos HM, Zerva LV. Anti-Ro (SSA)/La (SSB) antibodies and Sjogren's syndrome. Clin Rheumatol. 1990;9:123-130.
45. Musset L, Diemert MC, Taibi F, Thi Huong Du L, Cacoub P, Leger JM, Boissy G, Gaillard O, Galli J. Characterization of cryoglobulins by immunoblotting. Clin Chem. 1992;38:798-802.
46. Nebuchennykh M, Loseth S, Lindal S, Mellgren SI. The value of skin biopsy with recording of intraepidermal nerve fiber density and quantitative sensory testing in the assessment of small fiber involvement in patients with different causes of polyneuropathy. J Neurol. 2009;256:1067-1075.
47. Nebuchennykh M, Loseth S, Mellgren SI. Aspects of peripheral nerve involvement in patients with treated hypothyroidism. Eur J Neurol. 2010;17:67-72.
48. Periquet MI, Novak V, Collins MP, Nagaraja HN, Erdem S, Nash SM, Freimer ML, Sahenk Z, Kissel JT, Mendell Jr. Painful sensory neuropathy: prospective evaluation using skin biopsy. Neurology. 1999;53:1641-1647.
49. Rage M, Van Acker N, Facer P, Shenoy R, Knaapen MW, Timmers M, Streffer J, Anand P, Meert T, Plaghki L. The time course of CO2 laser-evoked responses and of skin nerve fibre markers after topical capsaicin in human volunteers. Clin Neurophysiol. 2010;121:1256-1266.
50. Rage M, Van Acker N, Knaapen MW, Timmers M, Streffer J, Hermans MP, Sindic C, Meert T, Plaghki L. Asymptomatic small fiber neuropathy in diabetes mellitus: investigations with intraepidermal nerve fiber density, quantitative sensory testing and laser-evoked potentials. J Neurol. 2011;258:1852-1864.
51. Ramos-Casals M, Solans R, Rosas J, Camps MT, Gil A, Del Pino-Montes J, Calvo-Alen J, Jimenez-Alonso J, Mico ML, Beltran J, Belenguer R, Pallares L. Primary Sjogren syndrome in Spain: clinical and immunologic expression in 1010 patients. Medicine (Baltimore). 2008;87:210-219.
52. Scherens A, Maier C, Haussleiter IS, Schwenkreis P, Vlckova-Moravcova E, Baron R, Sommer C. Painful or painless lower limb dysesthesias are highly predictive of peripheral neuropathy: comparison of different diagnostic modalities. Eur J Pain. 2009;13:711-718.
53. Sene D, Authier FJ, Amoura Z, Cacoub P, Lefaucheur JP. Neuropathie des petites fibres: approche diagnostique et traitement, et place de son association au syndrome de Gougerot-Sjogren primaire. Rev Med Interne. 2010;31:677-684.
54. Sene D, Jallouli M, Lefaucheur J-P, Saadoun D, Costedoat-Chalumeau N, Maisonobe T, Diemert M-C, Musset L, Haroche J, Piette J-C, Amoura Z, Cacoub P. Peripheral neuropathies associated with primary Sjogren syndrome: immunologic profiles of nonataxic sensory neuropathy and sensorimotor neuropathy. Medicine (Baltimore). 2011;90:133-138.
55. Shun CT, Chang YC, Wu HP, Hsieh SC, Lin WM, Lin YH, Tai TY, Hsieh ST. Skin denervation in type 2 diabetes: correlations with diabetic duration and functional impairments. Brain. 2004;127:1593-1605.
56. Tesfaye S, Boulton AJ, Dyck PJ, Freeman R, Horowitz M, Kempler P, Lauria G, Malik RA, Spallone V, Vinik A, Bernardi L, Valensi P. Diabetic neuropathies: update on definitions, diagnostic criteria, estimation of severity, and treatments. Diabetes Care. 2010;33:2285-2293.
57. Uceyler N, Zeller D, Kahn AK, Kewenig S, Kittel-Schneider S, Schmid A, Casanova-Molla J, Reiners K, Sommer C. Small fibre pathology in patients with fibromyalgia syndrome. Brain. 2013;136:1857-1867.
58. Vitali C, Bombardieri S, Jonsson R, Moutsopoulos HM, Alexander EL, Carsons SE, Daniels TE, Fox PC, Fox RI, Kassan SS, Pillemer SR, TalalN, Weisman MH. Classification criteria for Sjogren's syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis. 2002;61:554-558.
59. Vlckova-Moravcova E, Bednarik J, Dusek L, Toyka KV, Sommer C. Diagnostic validity of epidermal nerve fiber densities in painful sensory neuropathies. Muscle Nerve. 2008;37:50-60.
60. Wakasugi D, Kato T, Gono T, Ito E, Nodera H, Kawaguchi Y, Yamanaka H, Hara M. Extreme efficacy of intravenous immunoglobulin therapy for severe burning pain in a patient with small fiber neuropathy associated with primary Sjogren's syndrome. Mod Rheumatol. 2009;19:437-440.
61. Wright RA, Grant IA, Low PA. Autonomic neuropathy associated with sicca complex. J Auton Nerv Syst. 1999;75:70-76.