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Comparison of cutaneous silent period parameters in patients with primary Sjögren’s syndrome with the healthy population and determination of ıts relationship with clinical parameters

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Abstract

Small fiber neuropathy (SFN) is one of the main neurological manifestations in primary Sjögren’s Syndrome (pSS). For the detection of SFN, cutaneous silent period (CSP) measurement is gaining popularity recently due to its non-invasiveness and practical application. Evaluating SFN involvement in patients with pSS using CSP and evaluating its relationship with clinical parameters. Patients with a diagnosis of pSS and healthy volunteers demographically homogeneous with the patient group were included in the study. The CSP responses were recorded over the abductor pollicis brevis muscle. The latency and duration values of the responses were obtained. In patient group, EULAR Sjögren’s Syndrome Patient Reported Index (ESSPRI), Hospital Anxiety and Depression Scale (HADS), Short Form-36 (SF-36) questionnaire, Leeds Assessment of Neuropathic Symptoms and Signs (LANSS) and Central Sensitization Inventory (CSI) were applied for the evaluation of symptom severity, mood, quality of life, presence of neuropathic pain and central sensitization, respectively. The mean CSP latency was significantly longer in patient group compared to control group (p < 0.001). Mean CSP duration was also significantly shorter in patient group (p < 0.001). There were no significant differences in CSP parameters according to patients’ neuropathic pain or central sensitization profile. There were significant correlations of CSP parameters (latency and duration, respectively) with ESSPRI dryness (ρ = 0.469, p = 0.004; ρ =  −0.553, p < 0.001), fatigue (ρ = 0.42, p = 0.011; ρ =  −0.505, p = 0.002), pain (ρ = 0.428, p = 0.009; ρ =  −0.57, p < 0.001) subscores and mean ESSPRI score (ρ = 0.631, p < 0.001; ρ = −0.749, p < 0.001). When SF-36 subscores and CSP parameters were investigated, a significant correlation was found only between “bodily pain” subscore and CSP duration (ρ =  −0.395, p = 0.017). In HADS, LANSS and CSI evaluations, a significant correlation was found only between HADS anxiety score and the CSP duration (ρ = 0.364, p = 0.02). As indicated by CSP measurement, SFN is more prominent in patients with pSS than in the healthy population. It is important to investigate the presence of SFN because of its correlation with the leading symptoms in the clinical spectrum of pSS.

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References

  1. Tarn JR, Howard-Tripp N, Lendrem DW, Mariette X, Saraux A, Devauchelle-Pensec V, Seror R, Skelton AJ, James K, McMeekin P et al (2019) Symptom-based stratification of patients with primary Sjögren’s syndrome: multi-dimensional characterisation of international observational cohorts and reanalyses of randomised clinical trials. Lancet Rheumatol 1(2):e85–e94

    Article  Google Scholar 

  2. Birnbaum J (2010) Peripheral nervous system manifestations of Sjögren syndrome: clinical patterns, diagnostic paradigms, etiopathogenesis, and therapeutic strategies. Neurologist 16(5):287–297

    Article  Google Scholar 

  3. Chai J, Logigian EL (2010) Neurological manifestations of primary Sjogren’s syndrome. Curr Opin Neurol 23(5):509–513

    Article  Google Scholar 

  4. Margaretten M (2017) Neurologic manifestations of primary Sjögren syndrome. Rheum Dis Clin 43(4):519–529

    Article  Google Scholar 

  5. 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 (2005) The wide spectrum of clinical manifestations in Sjögren’s syndrome-associated neuropathy. Brain 128(11):2518–2534

    Article  Google Scholar 

  6. Johnson SA, Shouman K, Shelly S, Sandroni P, Berini SE, Dyck PJB, Hoffman EM, Mandrekar J, Niu Z, Lamb CJ, Low PA, Singer W, Mauermann ML, Mills J, Dubey D, Staff NP, Klein CJ (2021) Small fiber neuropathy incidence, prevalence, longitudinal impairments, and disability. Neurology 97(22):e2236–e2247

    Article  CAS  Google Scholar 

  7. Hovaguimian A, Gibbons CH (2011) Diagnosis and treatment of pain in small-fiber neuropathy. Curr Pain Headache Rep 15(3):193–200

    Article  Google Scholar 

  8. Chan AC, Wilder-Smith EP (2016) Small fiber neuropathy: getting bigger! Muscle Nerv 53(5):671–682

    Article  Google Scholar 

  9. Floeter MK (2003) Cutaneous silent periods. Muscle Nerv 28(4):391–401

    Article  Google Scholar 

  10. Kilinc O, Sencan S, Ercalik T, Koytak PK, Alibas H, Gunduz OH, Tanridag T, Uluc K (2018) Cutaneous silent period in myofascial pain syndrome. Muscle Nerv 57(1):E24–E28

    Google Scholar 

  11. Tekatas A, Tekatas DD, Solmaz V, Karaca T, Pamuk ON (2020) Small fiber neuropathy and related factors in patients with systemic lupus erythematosus; the results of cutaneous silent period and skin biopsy. Adv Rheumatol 60:31

    Article  Google Scholar 

  12. Chai J, Herrmann DN, Stanton M, Barbano RL, Logigian EL (2005) Painful small-fiber neuropathy in Sjögren syndrome. Neurology 65(6):925–927

    Article  CAS  Google Scholar 

  13. Descamps E, Henry J, Labeyrie C, Adams D, Ghaidaa AN, Vandendries C, Adam C, Aiello D, Mariette X, Seror R (2020) Small fiber neuropathy in Sjögren syndrome: comparison with other small fiber neuropathies. Muscle Nerv 61(4):515–520

    Article  CAS  Google Scholar 

  14. Birnbaum J, Lalji A, Saed A, Baer AN (2019) Biopsy-proven small-fiber neuropathy in primary Sjögren’s syndrome: neuropathic pain characteristics, autoantibody findings, and histopathologic features. Arthr Care Res 71(7):936–948

    Article  CAS  Google Scholar 

  15. Zouari HG, Wahab A, Ng Wing Tin S, Sène D, Lefaucheur J-P (2019) The clinical features of painful small-fiber neuropathy suggesting an origin linked to primary Sjögren’s syndrome. Pain Pract 19(4):426–434

    Article  Google Scholar 

  16. Sène D, Cacoub P, Authier F-J, Haroche J, Créange A, Saadoun D, Amoura Z, Guillausseau P-J, Lefaucheur J-P (2013) Sjögren syndrome-associated small fiber neuropathy: characterization from a prospective series of 40 cases. Medicine (Baltimore) 92(5):e10

    Article  Google Scholar 

  17. Segal BM, Pogatchnik B, Henn L, Rudser K, Sivils KM (2013) Pain severity and neuropathic pain symptoms in primary Sjögren’s syndrome: a comparison study of seropositive and seronegative Sjögren’s syndrome patients. Arthr Care Res 65(8):1291–1298

    Article  Google Scholar 

  18. Shiboski CH, Shiboski SC, Seror R, Criswell LA, Labetoulle M, Lietman TM, Rasmussen A, Scofield H, Vitali C, Bowman SJ, Mariette X, International Sjögren’s Syndrome Criteria Working Group (2017) 2016 American college of rheumatology/European league against rheumatism classification criteria for primary Sjögren’s syndrome: a consensus and data-driven methodology involving three international patient cohorts. Ann Rheum Dis 76(1):9–16

    Article  Google Scholar 

  19. Wolfe F, Clauw DJ, Fitzcharles M-A, Goldenberg DL, Häuser W, Katz RL, Mease PJ, Russell AS, Russell IJ, Walitt B (2016) 2016 Revisions to the 2010/2011 fibromyalgia diagnostic criteria. Seminars in arthritis and rheumatism. Elsevier, Amsterdam, pp 319–329

    Google Scholar 

  20. Aydemir Ö, Guvenir T, Kuey L, Kultur S (1997) Validity and reliability of Turkish version of hospital anxiety and depression scale. Turk Psikiyatri Derg 8(4):280–287

    Google Scholar 

  21. Kocyigit H, Aydemir Ö, Fisek G, Ö lmez N, Memis A, (1999) Validity and reliability of Turkish version of short form 36: a study of a patients with romatoid disorder. J Drug Ther 12(2):102–106

    Google Scholar 

  22. Yucel A, Senocak M, Orhan EK, Cimen A, Ertas M (2004) Results of the Leeds assessment of neuropathic symptoms and signs pain scale in Turkey: a validation study. J Pain 5(8):427–432

    Article  Google Scholar 

  23. Keleş ED, Birtane M, Ekuklu G, Kılınçer C, Çalıyurt O, Taştekin N, Is EE, Ketenci A, Neblett R (2021) Validity and reliability of the Turkish version of the central sensitization inventory. Arch Rheumatol 36(4):518–526

    Google Scholar 

  24. Sène D (2018) Small fiber neuropathy: diagnosis, causes, and treatment. Jt Bone Spine 85(5):553–559

    Article  Google Scholar 

  25. Pindi Sala T, Villedieu M, Damian L, Crave J-C, Pautot V, Stojanovich L, Tervaert JWC, Cherin P, Belizna C (2020) Long-term efficacy of immunoglobulins in small fiber neuropathy related to Sjögren’s syndrome. J Neurol 267(12):3499–3507

    Article  Google Scholar 

  26. Gorson KC, Herrmann DN, Thiagarajan R, Brannagan TH, Chin RL, Kinsella LJ, Ropper AH (2008) Non-length dependent small fibre neuropathy/ganglionopathy. J Neurol Neurosurg Psychiatry 79(2):163–169

    Article  CAS  Google Scholar 

  27. Dubost J-J, Couderc M, Pereira B, Mariette X, Seror R, Gottenberg J-E, Hachulla E, Le Guern V, Saraux A, Morel J, Salliot C, Tournadre A, Soubrier M (2021) Concomitant fibromyalgia in primary Sjögren’s syndrome in the French ASSESS cohort: comparison of the ACR 1990 and ACR 2016 criteria, FiRST questionnaire and physician’s opinion. Clin Exp Rheumatol 39(6):140–145

    Article  Google Scholar 

  28. Bailly F (2021) The challenge of differentiating fibromyalgia from small-fiber neuropathy in clinical practice. Jt Bone Spine 88(6):105232

    Article  Google Scholar 

  29. Üçeyler N, Zeller D, Kahn A-K, Kewenig S, Kittel-Schneider S, Schmid A, Casanova-Molla J, Reiners K, Sommer C (2013) Small fibre pathology in patients with fibromyalgia syndrome. Brain 136(6):1857–1867

    Article  Google Scholar 

  30. Koçer B, Tezcan ME, Batur HZ, Haznedaroğlu Ş, Göker B, İrkeç C, Çetinkaya R (2016) Cognition, depression, fatigue, and quality of life in primary Sjögren’s syndrome: correlations. Brain Behav 6(12):e00586

    Article  Google Scholar 

  31. Ng Wing Tin S, Zouari HG, Wahab A, Sène D, Lefaucheur J-P (2019) Characterization of neuropathic pain in primary Sjögren’s syndrome with respect to neurophysiological evidence of small-fiber neuropathy. Pain Med 20(5):979–987

    Article  Google Scholar 

  32. Birnbaum J, Duncan T, Owoyemi K, Wang KC, Carrino J, Chhabra A (2014) Use of a novel high-resolution magnetic resonance neurography protocol to detect abnormal dorsal root Ganglia in Sjögren patients with neuropathic pain: case series of 10 patients and review of the literature. Medicine (Baltimore) 93(3):121–134

    Article  Google Scholar 

  33. Latremoliere A, Woolf CJ (2009) Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain 10(9):895–926

    Article  Google Scholar 

  34. Devigili G, Rinaldo S, Lombardi R, Cazzato D, Marchi M, Salvi E, Eleopra R, Lauria G (2019) Diagnostic criteria for small fibre neuropathy in clinical practice and research. Brain 142(12):3728–3736

    Article  Google Scholar 

  35. Morkavuk G, Leventoglu A (2014) Small fiber neuropathy associated with hyperlipidemia: utility of cutaneous silent periods and autonomic tests. ISRN Neurol 2014:579242

    Article  CAS  Google Scholar 

  36. Onal M, Ulas U, Oz O, Bek V, Yucel M, Taslipinar A, Odabasi Z (2010) Cutaneous silent period changes in type 2 diabetes mellitus patients with small fiber neuropathy. Clin Neurophysiol 121(5):714–718

    Article  CAS  Google Scholar 

  37. Bakkers M, Faber CG, Hoeijmakers JGJ, Lauria G, Merkies IS (2014) Small fibers, large impact: quality of life in small-fiber neuropathy. Muscle Nerv 49(3):329–336

    Article  Google Scholar 

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Acknowledgements

Abstract of the study has been presented previously in “Scientific Abstracts” of EULAR. Abstract of the study has been submitted for EULAR 2022 European Congress of Rheumatology and accepted for publication in electronic “Abstract Book” with the number “AB0494”. The abstract is available at https://ard.bmj.com/content/81/Suppl_1/1373.2.

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Authors and Affiliations

  1. Department of Physical Medicine and Rehabilitation, Faculty of Medicine, Marmara University Medical School Pendik Research and Training Hospital, Fevzi Çakmak Mahallesi, Tepe Sokak, No: 41, Üst Kaynarca, Pendik, Istanbul, Turkey

    Günay Yolcu, Ozge Kenis-Coskun & Evrim Karadag-Saygi

  2. Division of Rheumatology, Department of Internal Medicine, Faculty of Medicine, Marmara University, Istanbul, Turkey

    Kerem Yigit Abacar & Guzide Nevsun-Inanc

  3. Division of Pain Medicine, Department of Physical Medicine and Rehabilitation, Faculty of Medicine, Marmara University, Istanbul, Turkey

    Osman Hakan Gunduz

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  1. Günay Yolcu
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Contributions

All co-authors take full responsibility for the integrity and accuracy of all aspects of the work. All authors approve the submitted version of the manuscript. Authorship contribution: conception and design of study, or acquisition of data, or analysis and interpretation of data: GY, KYA, OKC, GNI, EKS, OHG; drafting the article or revising it critically for important intellectual content: GY, KYA, OKC, GNI, EKS, OHG; final approval of the version to be submitted: GY, KYA, OKC, GNI, EKS, OHG.

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Correspondence to Günay Yolcu.

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The study protocol was approved by the Ethical Committee of Marmara University Medical Faculty (Number: 09.2021.111).

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Yolcu, G., Abacar, K.Y., Kenis-Coskun, O. et al. Comparison of cutaneous silent period parameters in patients with primary Sjögren’s syndrome with the healthy population and determination of ıts relationship with clinical parameters. Rheumatol Int 43, 355–362 (2023). https://doi.org/10.1007/s00296-022-05198-x

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