Clinical Rheumatology

, Volume 37, Issue 7, pp 1861–1867 | Cite as

Pain threshold and temporomandibular function in systemic sclerosis: comparison with psoriatic arthritis

  • Antonino Lo Giudice
  • Idona Brewer
  • Rosalia Leonardi
  • Neal Roberts
  • Gianluca Bagnato
Original Article


The aim of the study was to evaluate whether a reduced pain threshold is associated with increased temporomandibular dysfunction in systemic sclerosis (SSc) compared to psoriatic arthritis (PsA) and healthy controls. Ninety subjects participated in the study (30 SSc, 30 PsA, and 30 healthy controls). The Helkimo index was used to evaluate temporomandibular dysfunction. Digital palpation was performed at the temporomandibular joint (TMJ) surface and at the superficial masseter muscle (SMM) and pain intensity was recorded on a visual analog scale (VAS), while pain pressure threshold (PPT) was measured at the same sites through a pressure algometer. PPT scores were lower in SSc patients compared to PsA patients and controls. In addition, the average Helkimo index score, measuring the degree of TMJ dysfunction, was higher in SSc compared to PsA and controls. A significant inverse correlation was observed between every PPT score, and both Helkimo index and VAS palpation in SSc and PsA. Both the range of motion and all the other pain-related subdomains of the Helkimo index score (pain on movement, pain palpation TMJ and pain palpation muscle) were significantly worse in SSc compared to PsA, while no significant differences were observed in the TMJ function subdomain. In SSc patients, the skin score was directly associated with the range of motion subdomain of the Helkimo index. Our results confirm that TMJ function is impaired in SSc; further longitudinal studies are needed to assess the role of pain threshold in the assessment of limitations in TMJ function and to identify an objective marker of therapeutic response.


Pain pressure threshold  Psoriatic arthritis Systemic sclerosis Temporomandibular joint 


Compliance with ethical standards

This observational cross-sectional parallel group study (1:1:1) was approved by the ethics committee of the Faculty of Medicine at the University of Messina (prot. N.15–15). All subjects provided their written informed consent.




  1. 1.
    Gabrielli A, Avvedimento EV, Krieg T (2009) Scleroderma. N Engl J Med 360(19):1989–2003. CrossRefPubMedGoogle Scholar
  2. 2.
    Gyger G, Baron M (2012) Gastrointestinal manifestations of scleroderma: recent progress in evaluation, pathogenesis, and management. Curr Rheumatol Rep 14(1):22–29. CrossRefPubMedGoogle Scholar
  3. 3.
    Wollheim FA (2005) Classification of systemic sclerosis. Visions and reality. Rheumatology (Oxford) 44(10):1212–1216. CrossRefGoogle Scholar
  4. 4.
    Emmanuel A (2016) Current management of the gastrointestinal complications of systemic sclerosis. Nat Rev Gastroenterol Hepatol 13(8):461–472. CrossRefPubMedGoogle Scholar
  5. 5.
    Dagenais M, MacDonald D, Baron M, Hudson M, Tatibouet S, Steele R, Gravel S, Mohit S, El Sayegh T, Pope J, Fontaine A, Masseto A, Matthews D, Sutton E, Thie N, Jones N, Copete M, Kolbinson D, Markland J, Nogueira-Filho G, Robinson D, Gornitsky M (2015) The Canadian Systemic Sclerosis Oral Health Study IV: oral radiographic manifestations in systemic sclerosis compared with the general population. Oral Surg Oral Med Oral Pathol Oral Radiol 120(2):104–111. CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Baron M, Hudson M, Tatibouet S, Steele R, Lo E, Gravel S, Gyger G, El Sayegh T, Pope J, Fontaine A, Masetto A, Matthews D, Sutton E, Thie N, Jones N, Copete M, Kolbinson D, Markland J, Nogueira G, Robinson D, Fritzler M, Gornitsky M (2015) Relationship between disease characteristics and orofacial manifestations in systemic sclerosis: Canadian Systemic Sclerosis Oral Health Study III. Arthritis Care Res (Hoboken) 67(5):681–690. CrossRefGoogle Scholar
  7. 7.
    Silvestre-Rangil J, Martinez-Herrera M, Silvestre F-J (2015) Dental management of patients with microstomia. A review of the literature and update on the treatment. J Oral Res 4(5):340–350. CrossRefGoogle Scholar
  8. 8.
    Matarese G, Isola G, Alibrandi A, Lo Gullo A, Bagnato G, Cordasco G, Perillo L (2016) Occlusal and MRI characterizations in systemic sclerosis patients: a prospective study from Southern Italian cohort. Joint Bone Spine 83(1):57–62. CrossRefPubMedGoogle Scholar
  9. 9.
    Aliko A, Ciancaglini R, Alushi A, Tafaj A, Ruci D (2011) Temporomandibular joint involvement in rheumatoid arthritis, systemic lupus erythematosus and systemic sclerosis. Int J Oral Maxillofac Surg 40(7):704–709. CrossRefPubMedGoogle Scholar
  10. 10.
    Lo Gullo A, Mandraffino G, Bagnato G, Aragona CO, Imbalzano E, D'Ascola A, Rotondo F, Cinquegrani A, Mormina E, Saitta C, Versace AG, Sardo MA, Lo Gullo R, Loddo S, Saitta A (2015) Vitamin D status in rheumatoid arthritis: inflammation, arterial stiffness and circulating progenitor cell number. PLoS One 10(8):e0134602. CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Crincoli V, Di Comite M, Di Bisceglie MB, Fatone L, Favia G (2015) Temporomandibular disorders in psoriasis patients with and without psoriatic arthritis: an observational study. Int J Med Sci 12(4):341–348. CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Hu WL, Chang CH, Hung YC, Tseng YJ, Hung IL, Hsu SF (2014) Laser acupuncture therapy in patients with treatment-resistant temporomandibular disorders. PLoS One 9(10):e110528. CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Kothari SF, Baad-Hansen L, Hansen LB, Bang N, Sorensen LH, Eskildsen HW, Svensson P (2016) Pain profiling of patients with temporomandibular joint arthralgia and osteoarthritis diagnosed with different imaging techniques. J Headache Pain 17(1):61. CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Kothari SF, Baad-Hansen L, Oono Y, Svensson P (2015) Somatosensory assessment and conditioned pain modulation in temporomandibular disorders pain patients. Pain 156(12):2545–2555. CrossRefPubMedGoogle Scholar
  15. 15.
    Kothari SF, Baad-Hansen L, Andersen K, Svensson P (2014) Neurosensory assessment in patients with total reconstruction of the temporomandibular joint. Int J Oral Maxillofac Surg 43(9):1096–1103. CrossRefPubMedGoogle Scholar
  16. 16.
    Linsen SS, Reich RH, Teschke M (2012) Pressure pain threshold and oral health-related quality of life implications of patients with alloplastic temporomandibular joint replacement—a prospective study. J Oral Maxillofac Surg 70(11):2531–2542. CrossRefPubMedGoogle Scholar
  17. 17.
    van den Hoogen F, Khanna D, Fransen J, Johnson SR, Baron M, Tyndall A, Matucci-Cerinic M, Naden RP, Medsger TA Jr, Carreira PE, Riemekasten G, Clements PJ, Denton CP, Distler O, Allanore Y, Furst DE, Gabrielli A, Mayes MD, van Laar JM, Seibold JR, Czirjak L, Steen VD, Inanc M, Kowal-Bielecka O, Muller-Ladner U, Valentini G, Veale DJ, Vonk MC, Walker UA, Chung L, Collier DH, Ellen Csuka M, Fessler BJ, Guiducci S, Herrick A, Hsu VM, Jimenez S, Kahaleh B, Merkel PA, Sierakowski S, Silver RM, Simms RW, Varga J, Pope JE (2013) 2013 classification criteria for systemic sclerosis: an American college of rheumatology/European league against rheumatism collaborative initiative. Ann Rheum Dis 72(11):1747–1755. CrossRefPubMedGoogle Scholar
  18. 18.
    Taylor W, Gladman D, Helliwell P, Marchesoni A, Mease P, Mielants H, Group CS (2006) Classification criteria for psoriatic arthritis: development of new criteria from a large international study. Arthritis Rheum 54(8):2665–2673. CrossRefPubMedGoogle Scholar
  19. 19.
    Rolke R, Baron R, Maier C, Tolle TR, Treede RD, Beyer A, Binder A, Birbaumer N, Birklein F, Botefur IC, Braune S, Flor H, Huge V, Klug R, Landwehrmeyer GB, Magerl W, Maihofner C, Rolko C, Schaub C, Scherens A, Sprenger T, Valet M, Wasserka B (2006) Quantitative sensory testing in the German Research Network on Neuropathic Pain (DFNS): standardized protocol and reference values. Pain 123(3):231–243. CrossRefPubMedGoogle Scholar
  20. 20.
    Pigg M, Baad-Hansen L, Svensson P, Drangsholt M, List T (2010) Reliability of intraoral quantitative sensory testing (QST). Pain 148(2):220–226. CrossRefPubMedGoogle Scholar
  21. 21.
    Wajed J, Ejindu V, Heron C, Hermansson M, Kiely P, Sofat N (2012) Quantitative sensory testing in painful hand osteoarthritis demonstrates features of peripheral sensitisation. Int J Rheumatol 2012:703138. CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Lee YC, Lu B, Edwards RR, Wasan AD, Nassikas NJ, Clauw DJ, Solomon DH, Karlson EW (2013) The role of sleep problems in central pain processing in rheumatoid arthritis. Arthritis Rheum 65(1):59–68. CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Walton D, MacDermid J, Nielson W, Teasell R, Chiasson M, Brown L (2011) Reliability, standard error, and minimum detectable change of clinical pressure pain threshold testing in people with and without acute neck pain. J Orthop Sport Phys 41(9):644–650. CrossRefGoogle Scholar
  24. 24.
    Isselee H, De Laat A, De Mot B, Lysens R (2002) Pressure-pain threshold variation in temporomandibular disorder myalgia over the course of the menstrual cycle. J Orofac Pain 16(2):105–117PubMedGoogle Scholar
  25. 25.
    Helkimo M (1974) Studies on function and dysfunction of the masticatory system. II. Index for anamnestic and clinical dysfunction and occlusal state. Sven Tandlak Tidskr 67(2):101–121PubMedGoogle Scholar
  26. 26.
    Clements P, Lachenbruch P, Siebold J, White B, Weiner S, Martin R, Weinstein A, Weisman M, Mayes M, Collier D et al (1995) Inter and intraobserver variability of total skin thickness score (modified Rodnan TSS) in systemic sclerosis. J Rheumatol 22(7):1281–1285PubMedGoogle Scholar
  27. 27.
    Crincoli V, Fatone L, Fanelli M, Rotolo RP, Chiala A, Favia G, Lapadula G (2016) Orofacial manifestations and temporomandibular disorders of systemic scleroderma: an observational study. Int J Mol Sci 17(7).
  28. 28.
    Bagnato G, De Andres I, Sorbara S, Verduci E, Corallo G, Ferrera A, Morgante S, Roberts WN Jr, Bagnato G (2015) Pain threshold and intensity in rheumatic patients: correlations with the Hamilton Depression Rating scale. Clin Rheumatol 34(3):555–561. CrossRefPubMedGoogle Scholar
  29. 29.
    Bagnato GL, Miceli G, Marino N, Sciortino D, Bagnato GF (2016) Pulsed electromagnetic fields in knee osteoarthritis: a double blind, placebo-controlled, randomized clinical trial. Rheumatology (Oxford) 55(4):755–762. CrossRefGoogle Scholar
  30. 30.
    Goode AP, Shi XA, Gracely RH, Renner JB, Jordan JM (2014) Associations between pressure-pain threshold, symptoms, and radiographic knee and hip osteoarthritis. Arthritis Care Res (Hoboken) 66(10):1513–1519. CrossRefGoogle Scholar
  31. 31.
    Hodge MC, Nathan D, Bach TM (2009) Plantar pressure pain thresholds and touch sensitivity in rheumatoid arthritis. Foot Ankle Int 30(1):1–9. CrossRefPubMedGoogle Scholar
  32. 32.
    Gerecz-Simon EM, Tunks ER, Heale JA, Kean WF, Buchanan WW (1989) Measurement of pain threshold in patients with rheumatoid arthritis, osteoarthritis, ankylosing spondylitis, and healthy controls. Clin Rheumatol 8(4):467–474CrossRefPubMedGoogle Scholar
  33. 33.
    Wieckiewicz W, Wozniak K, Piatkowska D, Szyszka-Sommerfeld L, Lipski M (2015) The diagnostic value of pressure algometry for temporomandibular disorders. Biomed Res Int 2015:575038. CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Silveira A, Armijo-Olivo S, Gadotti IC, Magee D (2014) Masticatory and cervical muscle tenderness and pain sensitivity in a remote area in subjects with a temporomandibular disorder and neck disability. J Oral Facial Pain Headache 28(2):138–146. CrossRefPubMedGoogle Scholar
  35. 35.
    Svensson P, Arendt-Nielsen L, Nielsen H, Larsen JK (1995) Effect of chronic and experimental jaw muscle pain on pain-pressure thresholds and stimulus-response curves. J Orofac Pain 9(4):347–356PubMedGoogle Scholar
  36. 36.
    Ayesh EE, Jensen TS, Svensson P (2007) Hypersensitivity to mechanical and intra-articular electrical stimuli in persons with painful temporomandibular joints. J Dent Res 86(12):1187–1192. CrossRefPubMedGoogle Scholar
  37. 37.
    Wylde V, Palmer S, Learmonth ID, Dieppe P (2012) Somatosensory abnormalities in knee OA. Rheumatology (Oxford) 51(3):535–543. CrossRefGoogle Scholar
  38. 38.
    Bagnato G, Cordova F, Sciortino D, Miceli G, Bruno A, Ferrera A, Sangari D, Coppolino G, Muscatello MRA, Pandolfo G, Zoccali RA, Roberts WN (2017) Association between cortisol levels and pain threshold in systemic sclerosis and major depression. Rheumatol Int.
  39. 39.
    Nordahl S, Alstergren P, Kopp S (2000) Tumor necrosis factor-alpha in synovial fluid and plasma from patients with chronic connective tissue disease and its relation to temporomandibular joint pain. J Oral Maxillofac Surg 58(5):525–530CrossRefPubMedGoogle Scholar

Copyright information

© International League of Associations for Rheumatology (ILAR) 2018

Authors and Affiliations

  1. 1.Department of Medical-Surgical Specialties, Department of Orthodontics, Policlinico Universitario “Vittorio Emanuele”University of CataniaCataniaItaly
  2. 2.Department of Biomedical and Dental Sciences and Morphofunctional Imaging - Section of Orthodontics, School of Dentistry, Policlinico Universitario “G. Martino”University of MessinaMessinaItaly
  3. 3.Department of Medicine, Division of RheumatologyUniversity of Louisville School of MedicineLouisvilleUSA
  4. 4.Division of Rheumatology, Department of Clinical and Experimental Medicine, Policlinico Universitario “G. Martino”University of MessinaMessinaItaly

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