Journal of
Oral Rehabilitation
Journal of Oral Rehabilitation 2015 42; 723–732
Transcranial direct current stimulation and exercises for treatment of chronic temporomandibular disorders: a blind randomised-controlled trial L. B. OLIVEIRA*†, T. S. LOPES†, C. SOARES†, R. MALUF†, B. T. GOES*, ‡ & A . F . B A P T I S T A * ‡ *Bahian School of Medicine and Human Health, Salvador, †Adventist K . N . S A*
College of
‡
Bahia, Cachoeira, and Functional Electrostimulation Laboratory, Health Sciences Institute, Federal University of Bahia, Salvador, Brazil
SUMMARY To evaluate the effect of adding transcranial direct current stimulation (tDCS) to exercises for chronic pain, dysfunction and quality of life in subjects with temporomandibular disorders (TMD). Participants were selected based on the RDC/TMD criteria and assessed for pain intensity, pressure pain threshold over temporomandibular joint and cervical muscles and quality of life. After initial assessment, all individuals underwent a 4week protocol of exercises and manual therapy, together with active or sham primary motor cortex tDCS. Stimulation was delivered through sponge electrodes, with 2 mA amplitude, for 20 min daily, over the first 5 days of the trial. A total of 32 subjects (mean age 247 68 years) participated in the evaluations and treatment protocol. Mean pain intensity pre-treatment was 55 14 for active tDCS group, and 63 12 for sham tDCS. Both groups showed a decrease in pain intensity scores during the trial period (time factor – F45,1375 = 287,
Background Temporomandibular disorders (TMD) are considered a group of articular and muscular conditions in the orofacial area involving not only the temporomandibular joint (TMJ), but also other associated structures. Currently, TMD is identified as the main cause of oro-facial pain, with a prevalence of around 10% in the general population, with tendency to become chronic (1). It is known that the chronification of pain is associated with the phenomenon of pain memory in the © 2015 John Wiley & Sons Ltd
P < 0001; group factor – F10,300 = 77, P < 005). However, there were no differences between the groups regarding change in pain intensity (time*group interaction – F45,1375 = 15, P = 0137). This result remained the same after 5 months (t-test t = 029, P > 005). Pressure pain thresholds decrease and improvement in quality of life were also noticeable in both groups, but again without significant differences between them. Absolute benefit increase was 375% (CI 95%: 159% to 909%), and number needed to treat was 266. This study suggests that there is no additional benefit in adding tDCS to exercises for the treatment of chronic TMD in young adults. KEYWORDS: temporomandibular disorders, electrotherapy, quality of life, oro-facial pain, rehabilitation Accepted for publication 26 March 2015
central nervous system (CNS). Peripheral sensitisation associated with chronic tissue irritation leads to functional and structural changes in the CNS and contributes to the maintenance of the painful condition. These plastic modifications are known as maladaptive plasticity and have been implicated as key factors in chronic pain generation (2). As neuroplastic changes might play an important role in the maintenance of pain in TMD, the modulation of cortical neuron activity may contribute to reversing maladaptive plasticity and a consequent decrease in pain. doi: 10.1111/joor.12300
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L . B . O L I V E I R A et al. There is also evidence that exercises and postural training are better than placebo or no treatment for TMD (3). For other chronic conditions, exercises have been extensively studied; (4) however, it is not yet clear whether a brain with a low plastic capacity may prevent the benefits commonly generated by exercises, and even if there is some relationship between brain plastic capacity and the dose of exercises being administered. However, it is possible that conditioning the brain to exercise can have a positive effect (5). Over the past 10 years, several studies have been developed to assess the effects of transcranial direct current stimulation (tDCS) over the primary motor cortex area (M1), a region implicated in pain modulation. tDCS has demonstrated a beneficial clinical effect in controlling a number of painful syndromes of nociceptive or neuropathic origins and may also optimise the process of motor learning (6–8). However, its analgesic effect could not be confirmed in a recent systematic review (9). Although the use of tDCS alone may not be sufficient to promote a consistent analgesic effect, its use with exercises may have an additive effect or improve motor function and have an indirect effect on pain. So, this study was designed to test whether tDCS could influence the effects of exercises on participants with TMD and chronic pain. We hypothesised that active tDCS would enhance the effect of exercises in reducing pain and improving functional outcomes and quality of life.
10 the worst pain ever felt) during the last 6 months. The exclusion criteria were as follows: individuals who had received any type of physiotherapy treatment in the last month, the presence of rheumatic or cardiovascular diseases or convulsion and the presence of metal implant in the brain or skull. After the first comprehensive evaluation, the secretary of the clinical facility, who was not involved with any other procedures of the study, randomised participants who fulfilled the inclusion criteria for treatment and accepted to participate in the study. Randomisation occurred by the simple random method, in which each subject was invited to remove a small sealed envelope from a larger opaque envelope indicating two treatment groups: (a) active group, submitted to exercises + tDCS; (b) control group, who underwent exercises + sham tDCS, with 16 subjects being allocated to each group. The principal researcher performed all evaluations and the exercise protocol. A second researcher applied tDCS to all the patients and was blind to assessment and exercise protocols. Two other researchers analysed the data. All the procedures were conducted according to the World Medical Association Declaration of Helsinki. Ethical approval for this study was granted by the Bahia’s Adventist College Ethics Committee, approval number 0142/11. All participants signed a term of voluntary and informed consent approved by the research ethics committee, before randomisation.
Methods
Assessment instruments
Study design and study population This was a double-blinded randomised clinical trial. The participants of this study were selected from an initial epidemiological study conducted at the Adventist College of Bahia, Brazil. The population consisted of 880 young adults aged from 18 to 40 years, composed by students and staff. Of those, 190 presented moderate to severe TMD symptoms and were invited to visit the physiotherapy clinic for a complete evaluation. Fortyeight subjects reported to the clinical facility. Among those we invited to participate in the study, all individuals who were diagnosed with TMD based on the Research Diagnosis Criteria for Temporomandibular Disorders (RDC/TMD) Ia or Ib. They should present with oro-facial mean pain intensity equal to or over 4/ 10 on a visual analogue scale (VAS being 0 no pain and
The da Fonseca questionnaire (10) was used for the initial screening. Patients who were classified as having moderate or severe TMD were invited to visit the clinic for further evaluation with the Research Diagnostic Criteria for Temporomandibular Disorders (RDC/TMD) (11, 12), a visual analogue scale (VAS) to assess pain intensity at rest and the WHOQOL-BREF (13) to assess quality of life. Pressure pain threshold was assessed through a mechanical pressure algometer (Force Dial*). The probe (1 cm2) was positioned over the anterior and posterior regions of the TMJ condyle, suboccipital muscles (over the nuchal line of the occiput), upper portion of the trapezium (over the middle of the supraspinal fossa) and levator scapulae (over the
*Wagner Instruments, Greenwich, CT, USA. © 2015 John Wiley & Sons Ltd
TDCS AND EXERCISES FOR TMD superior angle of the scapulae). Pressure was applied at the rate of 1 kg s 1, until pain was first elicited. The average of three trials was used in the analysis. The RDC/TMD and WHOQOL were administered in the first and last days of treatment, while the pain intensity and pressure pain threshold were assessed daily. At the end of the protocol, participants were asked to identify their tDCS group as active or sham. Treatment protocol The treatment protocol was conducted during a 4-week period. During the first week, participants went to the clinic for five consecutive days; first undergoing the initial assessment and the exercise protocol, which lasted 15 min. After the exercises, participants received the tDCS intervention applied by a blinded researcher, for 20 min in a separate and quiet room. The tDCS protocol consisted of 20 min of direct current stimulation (Striat†), at amplitude of 2 mA, with the anode placed in the C3 or C4 region of the motor cortex (EEG 10–20 system) contralateral to the TMJ that presented the higher pain intensity. The cathode was placed over the opposite supra orbital region (14). For the sham tDCS, the electrodes were positioned and the participants were stimulated for 30 s. Then, the equipment was turned off and removed after 20 min. During the following 3 weeks, participants underwent only assessment and performed the exercise protocol 2 days per week until they completed 10 sessions, when they were completely re-evaluated. The principal investigator was blind to randomisation and tDCS treatment; she conducted the daily assessment and only the exercises intervention. Before starting the active protocol, myofascial release technique was performed in the cervical region. The aim of this technique is to move soft tissue layers one over the other, to improve movement between skin, fascia and muscles (15). Soon after, the exercise protocol proposed by Mariano Rocabado (16) was implemented (see supplementary video). It consisted of six repetitions of each exercise at the clinic, progressing from lying down to the sitting position, with the recommendation to practice exercise number two at home at least six times a day. Briefly, the exercises involved (i) cervical traction and self-stretching of the posterior muscles of the head and neck, maintained
†
Ibramed, S~ao Paulo, Brazil.
© 2015 John Wiley & Sons Ltd
for 20 s – goal: relaxation of the suboccipital muscles and cervical spine; (ii) active mouth opening until the amplitude limit imposed by keeping the tip of the tongue in contact with the hard palate – goal: relearning pure rotational motion of the condyle in the glenoid fossa; (iii) lateral movement of the mandible with hyperboloid: teeth gently holding the hyperboloid and performing rolling motions – goal: increase the range of motion; (iv) protrusion of the mandible with bite action starting at the end of protraction returning to over bite position with hyperboloid – goal: mobilisation of the disc into its correct intraarticular position; (v) contraction of the masseter muscle – goal: muscle strengthening; (vi) joint mobilisation performed by the therapist, by introducing the hand into the oral region, pressing down over the last molar on the limited side. This manoeuvre should be performed only in the presence of limited range of motion (opening 005). However, according to the assessment with the RDC/TMD after treatment, 12 participants (75%) of the active tDCS group and six (375%) of the sham tDCS group were no longer classified as having a diagnosis of TMD (v2 = 1, P < 005). Absolute benefit increase was 375% (CI 95%: 159% to 909%) and number needed to treat was 266. As we examined a probabilistic sample, these results show that 375% of the participants treated with tDCS and exercises are estimated to experience the positive outcome specifically due to the use of tDCS, and that for every three individuals with TMD treated with tDCS and exercise, one would be expected to become TMD symptom free.
Fig. 1. Study flowchart. © 2015 John Wiley & Sons Ltd
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Results Forty-eight individuals went to the clinical setting for complete evaluation. Thirty-eight were eligible because they had the inclusion criteria. Only 32 agreed to participate and were randomised to both groups after signing the free informed consent. The other six participants who did not agree to participate in the study had the same characteristics as the studied group regarding age (compared to active tDCS, P = 068; compared to sham tDCS, P = 028), sex distribution (compared to active tDCS, P = 050; compared to sham tDCS, P = 054), skin colour (compared to active tDCS, P = 024; compared to sham tDCS, P = 024), educational level (compared to active tDCS, P = 053; compared to sham tDCS, P = 053), baseline VAS (compared to active tDCS, P = 078); compared to sham tDCS, P = 010) and pain duration (compared to active tDCS, P = 099; compared to sham tDCS, P = 075). The study began in September 2011 and finished in June 2012. The final sample consisted of 16 participants per group (Fig. 1). All subjects were classified as having myofascial temporomandibular dysfunction. There were no differences between pre-treatment groups based on age, gender, race, educational level, pain intensity and duration in months and pressure pain threshold in the TMJ region and suboccipital muscles (Table 1). All subjects were classified as having myofascial temporomandibular dysfunction as classified by the axis I of the RDC/DTM. Other relevant classifications included (i) disc displacement with reduction – 25% in the active and 625% in the sham tDCS group; (ii) disc displacement without reduction – 125% in the active and 625% in the sham tDCS
group; (iii) arthralgia – 620% in the active and 680% in the sham tDCS group; (iv) osteoarthritis – 125% in the active and 625% in the sham tDCS group. There were no significant differences between groups at the baseline regarding any of the socio-demographic and clinical characteristics (Table 1). Pain intensity behaviour is displayed in Fig. 2. Intensity of pain decreased in both groups after the second day of treatment (repeated-measures ANOVA, time effect, F45,1375 = 287, P < 0001), but in slightly different patterns. Active tDCS-treated participants presented an almost continuous decrease in pain over the 10 days of assessment, whereas there was a stable period for sham tDCS between 5th and 9th days (repeated-measures ANOVA, group effect, F10,300 = 75, P < 005). Although mean pain intensity at the end of the study was lower in the active tDCS group, the difference was not significant (repeated-measures ANOVA, group 9 time interaction, F45,1375 = 15, P > 005). However, according to the assessment with the RDC/TMD after treatment, 12 participants (75%) of the active tDCS group and six (375%) of the sham tDCS group were no longer classified as having a diagnosis of TMD (v2 = 1, P < 005). Absolute benefit increase was 375% (CI 95%: 159% to 909%) and number needed to treat was 266. As we examined a probabilistic sample, these results show that 375% of the participants treated with tDCS and exercises are estimated to experience the positive outcome specifically due to the use of tDCS, and that for every three individuals with TMD treated with tDCS and exercise, one would be expected to become TMD symptom free.
Fig. 1. Study flowchart. © 2015 John Wiley & Sons Ltd
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Fig. 3. Muscle pressure pain threshold (PPT) registered after each treatment, analysed with repeated-measures ANOVA demonstrated for: (a) right trapezium a significant effect for time (F46,1405 = 50; P < 0000) but not an effect for time 9 group interaction (F46,1405 = 01; P > 005) (b) left trapezium a significant effect for time (F47,1159 = 82; P < 0000) but not an effect for time 9 group interaction (F47,1159 = 05; P > 005) (c) right levator scapulae a significant effect for time (F35,1084 = 51; P < 0000) but not an effect for time 9 group interaction (F35,1084 = 04; P > 005) (d) left levator scapular a significant effect for time (F44,1186 = 57; P < 0000) but not an effect for time 9 group interaction (F44,1186 = 06; P > 005); (e) right suboccipitalis with no significant effect for time or for time 9 group (F34,8736 = 22; P > 005) (F34,8736 = 07; P > 005); (f) left suboccipitalis a significant effect for time (F34,1146 = 25; P < 005) but not an effect for time 9 group interaction (F39,1146 = 08; P > 005). Group changes over the days of assessment (*). BL, baseline measurement. Data presented as mean and standard error of the mean.
(McNemar, v2 = 30, P = 007). Three participants received one-time medication (one from the active group and two from the sham group) due to orofacial pain, two with diclofenac and the third with dipyrone. The number of participants who correctly guessed the treatment to which they were assigned was 15 in the active tDCS group and seven in the sham tDCS group. One subject suffered burns on the fifth day of stimulus application, due to acne in the supraorbital region. At the end of the exercise sessions, the skin was completely healed with a small scar measuring 2 9 2 mm.
Five months after concluding the treatment, the researchers were able to contact 87% of the subjects in the exercises + tDCS group and 62% of in the exercises + sham tDCS group by telephone. They were asked about their pain levels at that moment, and whether they had continued performing any of the exercises. To analyse the difference in mean pain intensity at that time we used the intention to treat analysis, with the last observation carried forward. Both groups continued with important gains, with mean pain levels of 175 19 for the active tDCS group and 253 213 for the sham tDCS group (t = 029, P = 076). In regard to exercise, 29% of the © 2015 John Wiley & Sons Ltd
TDCS AND EXERCISES FOR TMD (a)
(b)
(c)
(d)
Fig. 4. Joint pressure pain threshold registered after each treatment. Analysed with repeated-measures ANOVA demonstrated for (a) right anterior region of mandibular condyle a significant effect for time (F36,1045 = 83 P < 0000) but not an effect for time 9 group interaction (F36,1045 = 04 P > 005); (b) left anterior region of mandibular condyle a significant effect for time (F47,1366 = 101 P < 0000) but not an effect for time 9 group interaction (F47,1366 = 11 P > 005); (c) right posterior region of mandibular condyle a significant effect for time (F49,1434 = 177 P < 0000) but not an effect for time 9 group interaction (F49,1434 = 13 P > 005); (d) left posterior region of mandibular condyle a significant effect for time (F43,5502 = 13 P < 0000) but not an effect for time 9 group interaction (F43,5502 = 07 P > 005). Group changes over the days of assessment (*). Data presented as mean and standard error of the mean. Table 2. TMJ movements before and after treatment Group Active tDCS + exercises (n = 16)
Aperture of the mouth without pain Maximum aperture of the mouth Right Lateral excursion Left lateral excursion
Group Sham tDCS + exercises (n = 16)
Pre- treatment
Post-treatment
P intra-group*
Pre- treatment
Post-treatment
P Intra-group
P Inter group**
2950 750
3500 740
000
3280 1060
3720 1030
000
047
4370 500
4500 500
000
4420 910
4520 800
000
083
920 300 920 250
1040 200 1100 240
002 013
930 140 980 250
970 100 1035 160
002 012
025 024
All values in millimetres (mm) Values expressed as mean s.d. *Paired t-test values. **t-test for the differences of the mean.
subjects of the active tDCS group and 50% of the sham tDCS group continued to perform the exercises.
Discussion The main hypothesis of this study was that tDCS would interact with exercise to produce a greater reduction in chronic pain in young adults with TMD. Although we found a large effect size for the differ© 2015 John Wiley & Sons Ltd
ence in pain intensity just after the end of the treatment, difference in improvement in pain intensity between groups was not significant. Data analysis could not support the differences between sham and active tDCS. TMD is related to a significant increase in generalised pain sensitivity after isometric contraction of the oro-facial muscles, suggestive of a central sensitisation process (17). In a pilot study, the first to suggest the
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Fig. 3. Muscle pressure pain threshold (PPT) registered after each treatment, analysed with repeated-measures ANOVA demonstrated for: (a) right trapezium a significant effect for time (F46,1405 = 50; P < 0000) but not an effect for time 9 group interaction (F46,1405 = 01; P > 005) (b) left trapezium a significant effect for time (F47,1159 = 82; P < 0000) but not an effect for time 9 group interaction (F47,1159 = 05; P > 005) (c) right levator scapulae a significant effect for time (F35,1084 = 51; P < 0000) but not an effect for time 9 group interaction (F35,1084 = 04; P > 005) (d) left levator scapular a significant effect for time (F44,1186 = 57; P < 0000) but not an effect for time 9 group interaction (F44,1186 = 06; P > 005); (e) right suboccipitalis with no significant effect for time or for time 9 group (F34,8736 = 22; P > 005) (F34,8736 = 07; P > 005); (f) left suboccipitalis a significant effect for time (F34,1146 = 25; P < 005) but not an effect for time 9 group interaction (F39,1146 = 08; P > 005). Group changes over the days of assessment (*). BL, baseline measurement. Data presented as mean and standard error of the mean.
(McNemar, v2 = 30, P = 007). Three participants received one-time medication (one from the active group and two from the sham group) due to orofacial pain, two with diclofenac and the third with dipyrone. The number of participants who correctly guessed the treatment to which they were assigned was 15 in the active tDCS group and seven in the sham tDCS group. One subject suffered burns on the fifth day of stimulus application, due to acne in the supraorbital region. At the end of the exercise sessions, the skin was completely healed with a small scar measuring 2 9 2 mm.
Five months after concluding the treatment, the researchers were able to contact 87% of the subjects in the exercises + tDCS group and 62% of in the exercises + sham tDCS group by telephone. They were asked about their pain levels at that moment, and whether they had continued performing any of the exercises. To analyse the difference in mean pain intensity at that time we used the intention to treat analysis, with the last observation carried forward. Both groups continued with important gains, with mean pain levels of 175 19 for the active tDCS group and 253 213 for the sham tDCS group (t = 029, P = 076). In regard to exercise, 29% of the © 2015 John Wiley & Sons Ltd
TDCS AND EXERCISES FOR TMD
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17. Mohn C, Vassend O, Knardahl S. Experimental pain sensitivity in women with temporomandibular disorders and pain-free controls: the relationship to orofacial muscular contraction and cardiovascular responses. Clin J Pain. 2008;24:343–352. 18. Antal A, Paulus W. A case of refractory orofacial pain treated by transcranial direct current stimulation applied over hand motor area in combination with NMDA agonist drug intake. Brain Stimul. 2011;4:117–121. 19. Bolognini N, Vallar G, Casati C, Latif LA, El-Nazer R, Williams J et al. Neurophysiological and behavioral effects of tDCS combined with constraint-induced movement therapy in post-stroke patients. Neurorehabil Neural Repair. 2011;25:819–829. 20. Yap AU, Tan KBC, Chua EK, List T, Tan HH. Depression and somatization in patients with temporomandibular disorders. J Prosthet Dent. 2002;88:479–484. 21. Singh AM, Duncan RE, Neva JL, Staines WR. Aerobic exercise modulates intracortical inhibition and facilitation in a nonexercised upper limb muscle. BMC Sports Sci Med Rehabil. 2014;6:23. 22. Wright DJ, Williams J, Holmes PS. Combined action observation and imagery facilitates corticospinal excitability. Front Hum Neurosci. 2014;2:951. 23. Singh AM, Neva JL, Staines WR. Acute exercise enhances the response to paired associative stimulation-induced plasticity in the primary motor cortex. Exp Brain Res. 2014;232:3675–3685. 24. Ridding MC, Ziemann U. Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. J Physiol. 2010;588:2291–2304. 25. Kalamir A, Bonello R, Graham P, Vitiello AL, Pollard H. Intraoral myofascial therapy for chronic myogenous temporomandibular disorder: a randomized controlled trial. J Manipulative Physiol Ther. 2011;35:26–37. 26. de Felicio CM, de Oliveira MM, da Silva MA. Effects of orofacial myofunctional therapy on Temporomandibular Disorders. Cranio. 2010;28:249–259. 27. La Touche R, Fernandez-de-las-Pe~ nas C, Fernandez-Carnero ^ J, Escalante K, Angulo-D ıaz-Parre~ no S, Paris-Alemany A. The effects of manual therapy and exercise directed at the cervical spine on pain and pressure pain sensitivity in patients with myofascial temporomandibular disorders. J Oral Rehabil. 2009;36:644–652. 28. Craane B, Dijkstra PU, Stappaerts K, De Laat A. Randomized Controlled trial on physical therapy for TMJ closed lock. J Dent Res. 2012;91:364–369. 29. Michelotti A, Steenks MH, Farella M, Parisini F, Cimino R, Martina R. The additional value of a home physical therapy regimen versus patient education only for the treatment of myofascial pain of the jaw muscles: short-term results of a randomized clinical trial. J Orofac Pain. 2004;18:114–125. 30. Stuhr SH, Earnshaw DH, Duncombe AM. Use of orthopedic manual physical therapy to manage chronic orofacial pain and tension type headache in an adolescent. J Man Manip Ther. 2014;22:51–58.
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Supporting Information Additional Supporting Information may be found in the online version of this article: Video S1: Transcranial direct current stimulation and exercises for the treatment of chronic temporomandibular disorders: A blind randomized controlled trial.
© 2015 John Wiley & Sons Ltd
Oral Rehabilitation
Journal of Oral Rehabilitation 2015 42; 723–732
Transcranial direct current stimulation and exercises for treatment of chronic temporomandibular disorders: a blind randomised-controlled trial L. B. OLIVEIRA*†, T. S. LOPES†, C. SOARES†, R. MALUF†, B. T. GOES*, ‡ & A . F . B A P T I S T A * ‡ *Bahian School of Medicine and Human Health, Salvador, †Adventist K . N . S A*
College of
‡
Bahia, Cachoeira, and Functional Electrostimulation Laboratory, Health Sciences Institute, Federal University of Bahia, Salvador, Brazil
SUMMARY To evaluate the effect of adding transcranial direct current stimulation (tDCS) to exercises for chronic pain, dysfunction and quality of life in subjects with temporomandibular disorders (TMD). Participants were selected based on the RDC/TMD criteria and assessed for pain intensity, pressure pain threshold over temporomandibular joint and cervical muscles and quality of life. After initial assessment, all individuals underwent a 4week protocol of exercises and manual therapy, together with active or sham primary motor cortex tDCS. Stimulation was delivered through sponge electrodes, with 2 mA amplitude, for 20 min daily, over the first 5 days of the trial. A total of 32 subjects (mean age 247 68 years) participated in the evaluations and treatment protocol. Mean pain intensity pre-treatment was 55 14 for active tDCS group, and 63 12 for sham tDCS. Both groups showed a decrease in pain intensity scores during the trial period (time factor – F45,1375 = 287,
Background Temporomandibular disorders (TMD) are considered a group of articular and muscular conditions in the orofacial area involving not only the temporomandibular joint (TMJ), but also other associated structures. Currently, TMD is identified as the main cause of oro-facial pain, with a prevalence of around 10% in the general population, with tendency to become chronic (1). It is known that the chronification of pain is associated with the phenomenon of pain memory in the © 2015 John Wiley & Sons Ltd
P < 0001; group factor – F10,300 = 77, P < 005). However, there were no differences between the groups regarding change in pain intensity (time*group interaction – F45,1375 = 15, P = 0137). This result remained the same after 5 months (t-test t = 029, P > 005). Pressure pain thresholds decrease and improvement in quality of life were also noticeable in both groups, but again without significant differences between them. Absolute benefit increase was 375% (CI 95%: 159% to 909%), and number needed to treat was 266. This study suggests that there is no additional benefit in adding tDCS to exercises for the treatment of chronic TMD in young adults. KEYWORDS: temporomandibular disorders, electrotherapy, quality of life, oro-facial pain, rehabilitation Accepted for publication 26 March 2015
central nervous system (CNS). Peripheral sensitisation associated with chronic tissue irritation leads to functional and structural changes in the CNS and contributes to the maintenance of the painful condition. These plastic modifications are known as maladaptive plasticity and have been implicated as key factors in chronic pain generation (2). As neuroplastic changes might play an important role in the maintenance of pain in TMD, the modulation of cortical neuron activity may contribute to reversing maladaptive plasticity and a consequent decrease in pain. doi: 10.1111/joor.12300
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L . B . O L I V E I R A et al. There is also evidence that exercises and postural training are better than placebo or no treatment for TMD (3). For other chronic conditions, exercises have been extensively studied; (4) however, it is not yet clear whether a brain with a low plastic capacity may prevent the benefits commonly generated by exercises, and even if there is some relationship between brain plastic capacity and the dose of exercises being administered. However, it is possible that conditioning the brain to exercise can have a positive effect (5). Over the past 10 years, several studies have been developed to assess the effects of transcranial direct current stimulation (tDCS) over the primary motor cortex area (M1), a region implicated in pain modulation. tDCS has demonstrated a beneficial clinical effect in controlling a number of painful syndromes of nociceptive or neuropathic origins and may also optimise the process of motor learning (6–8). However, its analgesic effect could not be confirmed in a recent systematic review (9). Although the use of tDCS alone may not be sufficient to promote a consistent analgesic effect, its use with exercises may have an additive effect or improve motor function and have an indirect effect on pain. So, this study was designed to test whether tDCS could influence the effects of exercises on participants with TMD and chronic pain. We hypothesised that active tDCS would enhance the effect of exercises in reducing pain and improving functional outcomes and quality of life.
10 the worst pain ever felt) during the last 6 months. The exclusion criteria were as follows: individuals who had received any type of physiotherapy treatment in the last month, the presence of rheumatic or cardiovascular diseases or convulsion and the presence of metal implant in the brain or skull. After the first comprehensive evaluation, the secretary of the clinical facility, who was not involved with any other procedures of the study, randomised participants who fulfilled the inclusion criteria for treatment and accepted to participate in the study. Randomisation occurred by the simple random method, in which each subject was invited to remove a small sealed envelope from a larger opaque envelope indicating two treatment groups: (a) active group, submitted to exercises + tDCS; (b) control group, who underwent exercises + sham tDCS, with 16 subjects being allocated to each group. The principal researcher performed all evaluations and the exercise protocol. A second researcher applied tDCS to all the patients and was blind to assessment and exercise protocols. Two other researchers analysed the data. All the procedures were conducted according to the World Medical Association Declaration of Helsinki. Ethical approval for this study was granted by the Bahia’s Adventist College Ethics Committee, approval number 0142/11. All participants signed a term of voluntary and informed consent approved by the research ethics committee, before randomisation.
Methods
Assessment instruments
Study design and study population This was a double-blinded randomised clinical trial. The participants of this study were selected from an initial epidemiological study conducted at the Adventist College of Bahia, Brazil. The population consisted of 880 young adults aged from 18 to 40 years, composed by students and staff. Of those, 190 presented moderate to severe TMD symptoms and were invited to visit the physiotherapy clinic for a complete evaluation. Fortyeight subjects reported to the clinical facility. Among those we invited to participate in the study, all individuals who were diagnosed with TMD based on the Research Diagnosis Criteria for Temporomandibular Disorders (RDC/TMD) Ia or Ib. They should present with oro-facial mean pain intensity equal to or over 4/ 10 on a visual analogue scale (VAS being 0 no pain and
The da Fonseca questionnaire (10) was used for the initial screening. Patients who were classified as having moderate or severe TMD were invited to visit the clinic for further evaluation with the Research Diagnostic Criteria for Temporomandibular Disorders (RDC/TMD) (11, 12), a visual analogue scale (VAS) to assess pain intensity at rest and the WHOQOL-BREF (13) to assess quality of life. Pressure pain threshold was assessed through a mechanical pressure algometer (Force Dial*). The probe (1 cm2) was positioned over the anterior and posterior regions of the TMJ condyle, suboccipital muscles (over the nuchal line of the occiput), upper portion of the trapezium (over the middle of the supraspinal fossa) and levator scapulae (over the
*Wagner Instruments, Greenwich, CT, USA. © 2015 John Wiley & Sons Ltd
TDCS AND EXERCISES FOR TMD superior angle of the scapulae). Pressure was applied at the rate of 1 kg s 1, until pain was first elicited. The average of three trials was used in the analysis. The RDC/TMD and WHOQOL were administered in the first and last days of treatment, while the pain intensity and pressure pain threshold were assessed daily. At the end of the protocol, participants were asked to identify their tDCS group as active or sham. Treatment protocol The treatment protocol was conducted during a 4-week period. During the first week, participants went to the clinic for five consecutive days; first undergoing the initial assessment and the exercise protocol, which lasted 15 min. After the exercises, participants received the tDCS intervention applied by a blinded researcher, for 20 min in a separate and quiet room. The tDCS protocol consisted of 20 min of direct current stimulation (Striat†), at amplitude of 2 mA, with the anode placed in the C3 or C4 region of the motor cortex (EEG 10–20 system) contralateral to the TMJ that presented the higher pain intensity. The cathode was placed over the opposite supra orbital region (14). For the sham tDCS, the electrodes were positioned and the participants were stimulated for 30 s. Then, the equipment was turned off and removed after 20 min. During the following 3 weeks, participants underwent only assessment and performed the exercise protocol 2 days per week until they completed 10 sessions, when they were completely re-evaluated. The principal investigator was blind to randomisation and tDCS treatment; she conducted the daily assessment and only the exercises intervention. Before starting the active protocol, myofascial release technique was performed in the cervical region. The aim of this technique is to move soft tissue layers one over the other, to improve movement between skin, fascia and muscles (15). Soon after, the exercise protocol proposed by Mariano Rocabado (16) was implemented (see supplementary video). It consisted of six repetitions of each exercise at the clinic, progressing from lying down to the sitting position, with the recommendation to practice exercise number two at home at least six times a day. Briefly, the exercises involved (i) cervical traction and self-stretching of the posterior muscles of the head and neck, maintained
†
Ibramed, S~ao Paulo, Brazil.
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for 20 s – goal: relaxation of the suboccipital muscles and cervical spine; (ii) active mouth opening until the amplitude limit imposed by keeping the tip of the tongue in contact with the hard palate – goal: relearning pure rotational motion of the condyle in the glenoid fossa; (iii) lateral movement of the mandible with hyperboloid: teeth gently holding the hyperboloid and performing rolling motions – goal: increase the range of motion; (iv) protrusion of the mandible with bite action starting at the end of protraction returning to over bite position with hyperboloid – goal: mobilisation of the disc into its correct intraarticular position; (v) contraction of the masseter muscle – goal: muscle strengthening; (vi) joint mobilisation performed by the therapist, by introducing the hand into the oral region, pressing down over the last molar on the limited side. This manoeuvre should be performed only in the presence of limited range of motion (opening 005). However, according to the assessment with the RDC/TMD after treatment, 12 participants (75%) of the active tDCS group and six (375%) of the sham tDCS group were no longer classified as having a diagnosis of TMD (v2 = 1, P < 005). Absolute benefit increase was 375% (CI 95%: 159% to 909%) and number needed to treat was 266. As we examined a probabilistic sample, these results show that 375% of the participants treated with tDCS and exercises are estimated to experience the positive outcome specifically due to the use of tDCS, and that for every three individuals with TMD treated with tDCS and exercise, one would be expected to become TMD symptom free.
Fig. 1. Study flowchart. © 2015 John Wiley & Sons Ltd
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Results Forty-eight individuals went to the clinical setting for complete evaluation. Thirty-eight were eligible because they had the inclusion criteria. Only 32 agreed to participate and were randomised to both groups after signing the free informed consent. The other six participants who did not agree to participate in the study had the same characteristics as the studied group regarding age (compared to active tDCS, P = 068; compared to sham tDCS, P = 028), sex distribution (compared to active tDCS, P = 050; compared to sham tDCS, P = 054), skin colour (compared to active tDCS, P = 024; compared to sham tDCS, P = 024), educational level (compared to active tDCS, P = 053; compared to sham tDCS, P = 053), baseline VAS (compared to active tDCS, P = 078); compared to sham tDCS, P = 010) and pain duration (compared to active tDCS, P = 099; compared to sham tDCS, P = 075). The study began in September 2011 and finished in June 2012. The final sample consisted of 16 participants per group (Fig. 1). All subjects were classified as having myofascial temporomandibular dysfunction. There were no differences between pre-treatment groups based on age, gender, race, educational level, pain intensity and duration in months and pressure pain threshold in the TMJ region and suboccipital muscles (Table 1). All subjects were classified as having myofascial temporomandibular dysfunction as classified by the axis I of the RDC/DTM. Other relevant classifications included (i) disc displacement with reduction – 25% in the active and 625% in the sham tDCS group; (ii) disc displacement without reduction – 125% in the active and 625% in the sham tDCS
group; (iii) arthralgia – 620% in the active and 680% in the sham tDCS group; (iv) osteoarthritis – 125% in the active and 625% in the sham tDCS group. There were no significant differences between groups at the baseline regarding any of the socio-demographic and clinical characteristics (Table 1). Pain intensity behaviour is displayed in Fig. 2. Intensity of pain decreased in both groups after the second day of treatment (repeated-measures ANOVA, time effect, F45,1375 = 287, P < 0001), but in slightly different patterns. Active tDCS-treated participants presented an almost continuous decrease in pain over the 10 days of assessment, whereas there was a stable period for sham tDCS between 5th and 9th days (repeated-measures ANOVA, group effect, F10,300 = 75, P < 005). Although mean pain intensity at the end of the study was lower in the active tDCS group, the difference was not significant (repeated-measures ANOVA, group 9 time interaction, F45,1375 = 15, P > 005). However, according to the assessment with the RDC/TMD after treatment, 12 participants (75%) of the active tDCS group and six (375%) of the sham tDCS group were no longer classified as having a diagnosis of TMD (v2 = 1, P < 005). Absolute benefit increase was 375% (CI 95%: 159% to 909%) and number needed to treat was 266. As we examined a probabilistic sample, these results show that 375% of the participants treated with tDCS and exercises are estimated to experience the positive outcome specifically due to the use of tDCS, and that for every three individuals with TMD treated with tDCS and exercise, one would be expected to become TMD symptom free.
Fig. 1. Study flowchart. © 2015 John Wiley & Sons Ltd
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L . B . O L I V E I R A et al. (a)
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Fig. 3. Muscle pressure pain threshold (PPT) registered after each treatment, analysed with repeated-measures ANOVA demonstrated for: (a) right trapezium a significant effect for time (F46,1405 = 50; P < 0000) but not an effect for time 9 group interaction (F46,1405 = 01; P > 005) (b) left trapezium a significant effect for time (F47,1159 = 82; P < 0000) but not an effect for time 9 group interaction (F47,1159 = 05; P > 005) (c) right levator scapulae a significant effect for time (F35,1084 = 51; P < 0000) but not an effect for time 9 group interaction (F35,1084 = 04; P > 005) (d) left levator scapular a significant effect for time (F44,1186 = 57; P < 0000) but not an effect for time 9 group interaction (F44,1186 = 06; P > 005); (e) right suboccipitalis with no significant effect for time or for time 9 group (F34,8736 = 22; P > 005) (F34,8736 = 07; P > 005); (f) left suboccipitalis a significant effect for time (F34,1146 = 25; P < 005) but not an effect for time 9 group interaction (F39,1146 = 08; P > 005). Group changes over the days of assessment (*). BL, baseline measurement. Data presented as mean and standard error of the mean.
(McNemar, v2 = 30, P = 007). Three participants received one-time medication (one from the active group and two from the sham group) due to orofacial pain, two with diclofenac and the third with dipyrone. The number of participants who correctly guessed the treatment to which they were assigned was 15 in the active tDCS group and seven in the sham tDCS group. One subject suffered burns on the fifth day of stimulus application, due to acne in the supraorbital region. At the end of the exercise sessions, the skin was completely healed with a small scar measuring 2 9 2 mm.
Five months after concluding the treatment, the researchers were able to contact 87% of the subjects in the exercises + tDCS group and 62% of in the exercises + sham tDCS group by telephone. They were asked about their pain levels at that moment, and whether they had continued performing any of the exercises. To analyse the difference in mean pain intensity at that time we used the intention to treat analysis, with the last observation carried forward. Both groups continued with important gains, with mean pain levels of 175 19 for the active tDCS group and 253 213 for the sham tDCS group (t = 029, P = 076). In regard to exercise, 29% of the © 2015 John Wiley & Sons Ltd
TDCS AND EXERCISES FOR TMD (a)
(b)
(c)
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Fig. 4. Joint pressure pain threshold registered after each treatment. Analysed with repeated-measures ANOVA demonstrated for (a) right anterior region of mandibular condyle a significant effect for time (F36,1045 = 83 P < 0000) but not an effect for time 9 group interaction (F36,1045 = 04 P > 005); (b) left anterior region of mandibular condyle a significant effect for time (F47,1366 = 101 P < 0000) but not an effect for time 9 group interaction (F47,1366 = 11 P > 005); (c) right posterior region of mandibular condyle a significant effect for time (F49,1434 = 177 P < 0000) but not an effect for time 9 group interaction (F49,1434 = 13 P > 005); (d) left posterior region of mandibular condyle a significant effect for time (F43,5502 = 13 P < 0000) but not an effect for time 9 group interaction (F43,5502 = 07 P > 005). Group changes over the days of assessment (*). Data presented as mean and standard error of the mean. Table 2. TMJ movements before and after treatment Group Active tDCS + exercises (n = 16)
Aperture of the mouth without pain Maximum aperture of the mouth Right Lateral excursion Left lateral excursion
Group Sham tDCS + exercises (n = 16)
Pre- treatment
Post-treatment
P intra-group*
Pre- treatment
Post-treatment
P Intra-group
P Inter group**
2950 750
3500 740
000
3280 1060
3720 1030
000
047
4370 500
4500 500
000
4420 910
4520 800
000
083
920 300 920 250
1040 200 1100 240
002 013
930 140 980 250
970 100 1035 160
002 012
025 024
All values in millimetres (mm) Values expressed as mean s.d. *Paired t-test values. **t-test for the differences of the mean.
subjects of the active tDCS group and 50% of the sham tDCS group continued to perform the exercises.
Discussion The main hypothesis of this study was that tDCS would interact with exercise to produce a greater reduction in chronic pain in young adults with TMD. Although we found a large effect size for the differ© 2015 John Wiley & Sons Ltd
ence in pain intensity just after the end of the treatment, difference in improvement in pain intensity between groups was not significant. Data analysis could not support the differences between sham and active tDCS. TMD is related to a significant increase in generalised pain sensitivity after isometric contraction of the oro-facial muscles, suggestive of a central sensitisation process (17). In a pilot study, the first to suggest the
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Fig. 3. Muscle pressure pain threshold (PPT) registered after each treatment, analysed with repeated-measures ANOVA demonstrated for: (a) right trapezium a significant effect for time (F46,1405 = 50; P < 0000) but not an effect for time 9 group interaction (F46,1405 = 01; P > 005) (b) left trapezium a significant effect for time (F47,1159 = 82; P < 0000) but not an effect for time 9 group interaction (F47,1159 = 05; P > 005) (c) right levator scapulae a significant effect for time (F35,1084 = 51; P < 0000) but not an effect for time 9 group interaction (F35,1084 = 04; P > 005) (d) left levator scapular a significant effect for time (F44,1186 = 57; P < 0000) but not an effect for time 9 group interaction (F44,1186 = 06; P > 005); (e) right suboccipitalis with no significant effect for time or for time 9 group (F34,8736 = 22; P > 005) (F34,8736 = 07; P > 005); (f) left suboccipitalis a significant effect for time (F34,1146 = 25; P < 005) but not an effect for time 9 group interaction (F39,1146 = 08; P > 005). Group changes over the days of assessment (*). BL, baseline measurement. Data presented as mean and standard error of the mean.
(McNemar, v2 = 30, P = 007). Three participants received one-time medication (one from the active group and two from the sham group) due to orofacial pain, two with diclofenac and the third with dipyrone. The number of participants who correctly guessed the treatment to which they were assigned was 15 in the active tDCS group and seven in the sham tDCS group. One subject suffered burns on the fifth day of stimulus application, due to acne in the supraorbital region. At the end of the exercise sessions, the skin was completely healed with a small scar measuring 2 9 2 mm.
Five months after concluding the treatment, the researchers were able to contact 87% of the subjects in the exercises + tDCS group and 62% of in the exercises + sham tDCS group by telephone. They were asked about their pain levels at that moment, and whether they had continued performing any of the exercises. To analyse the difference in mean pain intensity at that time we used the intention to treat analysis, with the last observation carried forward. Both groups continued with important gains, with mean pain levels of 175 19 for the active tDCS group and 253 213 for the sham tDCS group (t = 029, P = 076). In regard to exercise, 29% of the © 2015 John Wiley & Sons Ltd
TDCS AND EXERCISES FOR TMD
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Supporting Information Additional Supporting Information may be found in the online version of this article: Video S1: Transcranial direct current stimulation and exercises for the treatment of chronic temporomandibular disorders: A blind randomized controlled trial.
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