Can Experimentally Evoked Pain in the Jaw Muscles or Temporomandibular Joint Affect Anterior Bite Force in Humans?

Aims: To test the hypothesis that experimental pain in the masseter muscle or temporomandibular joint (TMJ) will decrease the anterior maximum voluntary bite force (MVBF) and jaw muscle activity in relation to the perceived effort. Methods: Sixteen volunteers participated in two experimental sessions. Participants were injected with 0.2 mL of monosodium glutamate (1.0 M) into either the masseter muscle or TMJ. The MVBF and corresponding electromyographic (EMG) activity of the masseter, anterior temporalis, and digastric muscles were recorded 10 times at an interval of 2 minutes before and after injection. Pain was measured using a visual analog scale and McGill Pain Questionnaire. In addition, participants were asked how they perceived the interference of pain on their biting performance. The data analysis included a two-way analysis of variance model and t test. Results: There was no significant difference in peak pain intensity (P = .066) and duration of pain (P = .608) between painful muscle and TMJ injections, but TMJ injection produced a significantly larger area under the curve (P = .005) and a significantly higher pain rating index (P = .030). Pain in the muscle (P = .421) and TMJ (P = .057) did not significantly change the MVBF from baseline levels. The EMG activity also did not differ significantly from baseline levels during muscle pain. However, there was a significant increase (P = .028) in the EMG activity of the anterior temporalis and a significant decrease (P = .010) in the EMG activity of the anterior digastric muscle compared to baseline during TMJ pain. Subject-based reports also revealed that in the majority of cases (62.5%), pain did not interfere with the MVBF task. Conclusion: Experimental pain from either masseter muscle or TMJ did not affect the MVBF, in accordance with the subject-based reports. Jaw muscle activity, except for EMG activity of the anterior temporalis and anterior digastric muscles during TMJ pain, also remained unaffected by pain. The findings suggest that it is not pain in itself but rather how pain is perceived that may lead to adaptation of motor function, supporting an integrated pain adaptation model.

electromyography; integrated pain adaptation model; monosodium glutamate

1. Svensson P. What can human experimental pain models teach us about clinical TMD? Arch Oral Biol 2007;52:391–394.

2. Murray GM, Peck CC. Orofacial pain and jaw muscle activity: A new model. J Orofac Pain 2007;21:263–278.

3. LeResche L. Epidemiology of temporomandibular disorders: Implications for the investigation of etiologic factors. Crit Rev Oral Biol Med 1997;8:291–305.

4. Lindroth JE, Schmidt JE, Carlson CR. A comparison between masticatory muscle pain patients and intracapsular pain patients on behavioral and psychosocial domains. J Orofac Pain 2002;16:277–283.

5. Turk DC, Rudy TE, Kubinski JA, Zaki HS, Greco CM. Dysfunctional patients with temporomandibular disorders: Evaluating the efficacy of a tailored treatment protocol. J Consult Clin Psychol 1996;64:139–146.

6. Stohler CS. Craniofacial pain and motor function: Pathogenesis, clinical correlates, and implications. Crit Rev Oral Biol Med 1999;10:504–518.

7. Svensson P, Graven-Nielsen T. Craniofacial muscle pain: Review of mechanisms and clinical manifestations. J Orofac Pain 2001;15:117–145.

8. Ro JY, Svensson P, Capra N. Effects of experimental muscle pain on electromyographic activity of masticatory muscles in the rat. Muscle Nerve 2002;25:576–584.

9. Matre DA, Sinkjaer T, Svensson P, Arendt-Nielsen L. Experimental muscle pain increases the human stretch reflex. Pain 1998;75:331–339.

10. Svensson P, De Laat A, Graven-Nielsen T, Arendt-Nielsen L. Experimental jaw-muscle pain does not change heteronymous H- reflexes in the human temporalis muscle. Exp Brain Res 1998; 121:311–318.

11. Lund JP, Donga R, Widmer CG, Stohler CS. The pain-adaptation model: A discussion of the relationship between chronic musculoskeletal pain and motor activity. Can J Physiol Pharmacol 1991;69:683–694.

12. Svensson P, Arendt-Nielsen L, Houe L. Muscle pain modulates mastication: An experimental study in humans. J Orofac Pain 1998;12:7–16.

13. Svensson P, Houe L, Arendt-Nielsen L. Bilateral experimental muscle pain changes electromyographic activity of human jaw-closing muscles during mastication. Exp Brain Res 1997; 116:182–185.

14. Svensson P, Arendt-Nielsen L, Houe L. Sensory-motor interactions of human experimental unilateral jaw muscle pain: A quantitative analysis. Pain 1996;64:241–249.

15. Stohler CS, Ashton-Miller JA, Carlson DS. The effects of pain from the mandibular joint and muscles on masticatory motor behaviour in man. Arch Oral Biol 1988;33:175–182.

16. Hodges PW, Tucker K. Moving differently in pain: A new theory to explain the adaptation to pain. Pain 2011;152:90–98.

17. Peck CC, Murray GM, Gerzina TM. How does pain affect jaw muscle activity? The Integrated Pain Adaptation Model. Aust Dent J 2008;53:201–207.

18. Mintken PE, Cleland JA, Whitman JM, George SZ. Psychometric properties of the Fear-Avoidance Beliefs Questionnaire and Tampa Scale of Kinesiophobia in patients with shoulder pain. Arch Phys Med Rehabil 2010;91:1128–1136.

19. Turner JA, Brister H, Huggins K, Mancl L, Aaron LA, Truelove EL. Catastrophizing is associated with clinical examination findings, activity interference, and health care use among patients with temporomandibular disorders. J Orofac Pain 2005;19:291–300.

20. Turner JA, Aaron LA. Pain-related catastrophizing: What is it?Clin J Pain 2001;17:65–71.

21. Hasenbring MI, Verbunt JA. Fear-avoidance and endurance-related responses to pain: New models of behavior and their consequences for clinical practice. Clin J Pain 2010;26:747–753.

22. Dworkin SF, LeResche L. Research diagnostic criteria for temporomandibular disorders: Review, criteria, examinations and specifications, critique. J Craniomandib Disord 1992;6: 301–355.

23. Lobbezoo F, Naeije M. A reliability study of clinical tooth wear measurements. J Prosthet Dent 2001;86:597–602.

24. Castrillon EE, Cairns BE, Ernberg M, et al. Glutamate-evoked jaw muscle pain as a model of persistent myofascial TMD pain? Arch Oral Biol 2008;53:666–676.

25. Davidson JA, Metzinger SE, Tufaro AP, Dellon AL. Clinical implications of the innervation of the temporomandibular joint. J Craniofac Surg 2003;14:235–239.

26. List T, Tegelberg A, Haraldson T, Isacsson G. Intra-articular morphine as analgesic in temporomandibular joint arthralgia/osteoarthritis. Pain 2001;94:275–282.

27. Widmalm SE, Lillie JH, Ash MM Jr. Anatomical and electromyo-graphic studies of the digastric muscle. J Oral Rehabil 1988; 15:3–21.

28. Alfredson H, Forsgren S, Thorsen K, Lorentzon R. In vivo microdialysis and immunohistochemical analyses of tendon tissue demonstrated high amounts of free glutamate and glutamate NMDAR1 receptors, but no signs of inflammation, in Jumper’s knee. J Orthop Res 2001;19:881–886.

29. Rosendal L, Larsson B, Kristiansen J, et al. Increase in muscle nociceptive substances and anaerobic metabolism in patients with trapezius myalgia: Microdialysis in rest and during exercise. Pain 2004;112:324–334.

30. Castrillon EE, Ernberg M, Cairns BE, et al. Interstitial glutamate concentration is elevated in the masseter muscle of myofascial temporomandibular disorder patients. J Orofac Pain 2010;24: 350–360.

31. Alstergren P, Ernberg M, Nilsson M, Hajati AK, Sessle BJ, Kopp S. Glutamate-induced temporomandibular joint pain in healthy individuals is partially mediated by peripheral NMDA receptors. J Orofac Pain 2010;24:172–180.

32. McCreary CP, Clark GT, Merril RL, Flack V, Oakley ME. Psychological distress and diagnostic subgroups of temporo-mandibular disorder patients. Pain 1991;44:29–34.

33. Rudy TE, Turk DC, Kubinski JA, Zaki HS. Differential treatment responses of TMD patients as a function of psychological characteristics. Pain 1995;61:103–112.

34. Wright EF. Referred craniofacial pain patterns in patients with temporomandibular disorder. J Am Dent Assoc 2000;131: 1307–1315.

35. Castroflorio T, Falla D, Wang K, Svensson P, Farina D. Effect of experimental jaw-muscle pain on the spatial distribution of surface EMG activity of the human masseter muscle during tooth clenching. J Oral Rehabil 2012;39:81–92.

36. Melis M, Lobo SL, Ceneviz C, et al. Effect of cigarette smoking on pain intensity of TMD patients: A pilot study. Cranio 2010; 28:187–192.

37. Hara ES, Witzel AL, de Luca CE, Ballester RY, Kuboki T, Bolzan MC. A novel vibratory stimulation-based occlusal splint for alleviation of TMD painful symptoms: A pilot study. J Oral Rehabil 2013;40:179–184.

38. Hansdottir R, Bakke M. Joint tenderness, jaw opening, chewing velocity, and bite force in patients with temoromandibular joint pain and matched healthy control subjects. J Orofac Pain 2004;18:108–113.

39. Kogawa EM, Calderon PS, Lauris JR, Araujo CR, Conti PC. Evaluation of maximal bite force in temporomandibular disorders patients. J Oral Rehabil 2006;33:559–565.

40. Bonjardim LR, Gaviao MB, Pereira LJ, Castelo PM. Bite force determination in adolescents with and without temporoman-dibular dysfunction. J Oral Rehabil 2005;32:577–583.

41. Arima T, Svensson P, Arendt-Nielsen L. Capsaicin-induced muscle hyperalgesia in the exercised and non-exercised human masseter muscle. J Orofac Pain 2000;14:213–223.

42. Sarlani E, Grace EG, Reynolds MA, Greenspan JD. Evidence for up-regulated central nociceptive processing in patients with masticatory myofascial pain. J Orofac Pain 2004;18:41–55.

43. Cairns BE, Svensson P, Wang K, et al. Ketamine attenuates glutamate-induced mechanical sensitization of the masseter muscle in human males. Exp Brain Res 2006;169:467–472.

44. Jerjes W, Madland G, Feinmann C, et al. A psychological comparison of temporomandibular disorder and chronic daily headache: Are there targets for therapeutic interventions? Oral Surg, Oral Med Oral Pathol Oral Radiol Endod 2007;103:367–373.

45. Van Eijden TM, Brugman P, Weijs WA, Oosting J. Coactivation of jaw muscles: Recruitment order and level as a function of bite force direction and magnitude. J Biomech 1990;23:475–485.

46. van Dieen JH, Selen LP, Cholewicki J. Trunk muscle activa-tion in low-back pain patients, an analysis of the literature. J Electromyogr Kinesiol 2003;13:333–351.

47. Hasenbring M. Attentional control of pain and the process of chronification. Progress in brain research. 2000;129:525–534.

48. Lyons MF, Baxendale RH. Masseter muscle relaxation rate in volunteers with a myogenous craniomandibular disorder. J Oral Rehabil 1995;22:355–364.

49. Ikebe K, Nokubi T, Morii K, Kashiwagi J, Furuya M. Association of bite force with ageing and occlusal support in older adults. J Dent 2005;33:131–137.

50. Clark GT, Carter MC. Electromyographic study of human jaw-closing muscle endurance, fatigue and recovery at various isometric force levels. Arch Oral Bio 1985;30:563–569.

51. Wang K, Arima T, Arendt-Nielsen L, Svensson P. EMG-force relationships are influenced by experimental jaw-muscle pain. J Oral Rehabil 2000;27:394–402.

52. Blanksma NG, van Eijden TM. Electromyographic heterogeneity in the human temporalis and masseter muscles during static biting, open/close excursions, and chewing. J Dent Res 1995;74:1318–1327.

53. Sae-Lee D, Whittle T, Forte AR, et al. Effects of experimental pain on jaw muscle activity during goal-directed jaw move-ments in humans. Exp Brain Res 2008;189:451–462.

54. Cairns BE, Sessle BJ, Hu JW. Evidence that excitatory amino acid receptors within the temporomandibular joint region are involved in the reflex activation of the jaw muscles. J Neurosci 1998;18:8056–8064.

55. Yu XM, Sessle BJ, Vernon H, Hu JW. Effects of inflammatory irritant application to the rat temporomandibular joint on jaw and neck muscle activity. Pain 1995;60:143–149.

56. Broton JG, Sessle BJ. Reflex excitation of masticatory muscles induced by algesic chemicals applied to the temporomandibular joint of the cat. Arch Oral Biol 1988;33:741–747.

57. Lam DK, Sessle BJ, Cairns BE, Hu JW. Peripheral NMDA receptor modulation of jaw muscle electromyographic activity induced by capsaicin injection into the temporomandibular joint of rats. Brain Res 2005;1046:68–76.

58. Okamoto K, Tashiro A, Chang Z, Thompson R, Bereiter DA. Temporomandibular joint-evoked responses by spinomedullary neurons and masseter muscle are enhanced after repeated psychophysical stress. Eur J Neurosci 2012;36:2025–2034.