Psychophysiological responses to pain stimulation and cognitive tasks in female temporomandibular disorder patients
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Abstract
Background and purpose
Psychophysiological factors may contribute to the development of temporomandibular disorders (TMD). Both local orofacial and systemic responses have been investigated. However, most studies have concentrated on physiological responding during cognitive challenges, while responses during painful tasks may be highly relevant for the development of chronic pain conditions. Moreover, the relationship between experimental challenges and physiological responding may be influenced by affective responses during the experimental tasks, an issue not often considered in the literature.
Methods
This study compared electromyography (EMG) of the left masseter and left trapezius muscles, orofacial and digital skin blood-flow (SBF), mean arterial pressure (MAP), and heart rate (HR) at rest, during orofacial isometric contraction, electrocutaneous pain stimulation of the left hand, pressure pain stimulation of the masseter muscle and the sternum, and three cognitive tasks (reading aloud, a simulated job interview, and visuomotoric tracking). The participants were 25 TMD patients and 25 matched pain-free controls, all females. Affective responses were assessed with the State part of the State-Trait Personality Inventory and with Visual Analogue Scales.
Results
Masseter EMG levels were significantly lower in the TMD group relative to the control group during jaw contraction, pressure pain stimulation, the relaxation periods, and cognitive tasks. SBF, MAP, and HR responses were largely similar in the two groups, with SBF responses to pain stimulation evident at lower levels of stimulation than previously found. The TMD patients reported significantly higher levels of negative affect during the experiment.
Conclusions and implications
The low EMG responses in the TMD group may be taken in support of the Pain Adaptation Model of musculoskeletal pain, in which reduced muscular activity serves to protect a painful area. However, it may also be supportive of the Integrated Pain Adaptation Model, where higher central nervous structures influence local muscular output. The group similarities in systemic physiological responding in combination with the elevated levels of negative state affect in the TMD patients confirm previous reports of psychosocial differences being more reliable indicators of TMD than generalized physiological responding.
1 Introduction
Temporomandibular disorders (TMD) are a group of disorders with core symptoms of pain and/or mobility dysfunctions of the masticatory region [1]. For the many cases that are idiopathic, hypotheses of pathogenesis have focused on local peripheral factors like joint dysfunction and activation of masticatory muscles [2]. Although some studies report enhanced masseter muscle activity in TMD, it has not been possible to establish local muscle factors as pathogenic factors [2]. Most studies have focused on changes in orofacial electromyography (EMG) during rest and/or cognitive challenges [3,4,5]. Tasks that more directly target the chronic pain experience may be better suited for eliciting differences in emotional and physiological responding. Isometric contraction of the masseter muscles (biting or clenching) should be a relevant stimulus for eliciting physiological responses in TMD patients.
Several studies have reported generalized alterations in pain sensitivity in TMD patients. Relative to pain-free controls, some TMD patients exhibit general hyperalgesia [6]. Higher levels of tenderness and pain from anatomical regions outside the orofacial structures are commonly found [7], and an association between widespread chronic pain and TMD has been proposed [8]. Hence, it has been hypothesized that TMD is a psychophysiological disorder involving central pain-regulatory dysfunctions, resulting in maladaptive psychological and physiological responses to emotional and physical stress [9,10], and that TMD is closely related to other chronic pain conditions characterized by multiple complaints from several anatomical organs [11].
The studies describing the physiological responses to challenges in chronic pain patients have mainly employed non-painful arousing stimuli. If central sensitization plays a role in the development of TMD, one would expect that these patients exhibit hyper-responsiveness to at least some painful stimuli. We have not found studies that explicitly have addressed the psychophysiological response to painful stimulation as compared to non-painful tasks in TMD patients and pain-free controls. Therefore, the present study included measurements of physiological responses to both painful and non-painful experimental tasks.
Mammals have a repertoire of response patterns to challenge, threat, and injury. Several of these patterns are integrated in the periaqueductal grey (PAG) area of the brainstem [12]. The rostral part of the region that integrates active coping responses responding seems to control responses during confrontations. Stimulation of this area produces skin vasodilation of the orofacial region [12]. This raises the possibility that other orofacial responses, in addition to specific activation of the masseter muscle, characterize TMD. It may be relevant to investigate skin blood flow (SBF) as an indicator of responses of the orofacial region.
Some previous studies have reported vasoconstriction of the skin superficial to painful muscle [13,14]. Painful stimulation may elicit orofacial vasodilation depending on stimulation site, indicating the existence of specific orofacial vasodilatory reflex mechanisms [15]. These changes were not paralleled by changes in heart rate (HR). To our knowledge, explicit comparisons of focal (e.g., SBF and EMG) and systemic physiological responses (e.g., arterial pressure and HR) in TMD patients and pain-free controls during painful stimulation have not been performed.
Complicating the relationship between experimental challenges and physiological responding is the influence of affective responses during the experimental tasks. A study of EMG and electrodermal responses to laboratory challenges in TMD patients found that individual differences in affective experience during the experiment were related to different levels of physiological arousal [16]. However, that study did not include a control group of pain-free individuals [16].
In the present study, the primary outcome measure was psychophysiological responding in TMD patients versus healthy controls during orofacial muscle contraction and experimental painful stimulation. The secondary outcome measures were (1) psychophysiological responding in TMD patients versus controls during relaxation and non-painful cognitive tasks, and (2) subjective reports of affective state in TMD patients versus controls across the experimental conditions.
2 Materials and methods
2.1 Subjects
Twenty-eight female patients with TMD were recruited from the outpatient clinic of the Dental Faculty, University of Oslo (n = 19) and from one advertisement in an Oslo newspaper (n = 9). All patients, including those who were recruited through the newspaper ad, underwent a structured clinical examination based on the Research Diagnostic Criteria for TMD (RDC-TMD) by the Dental Faculty research physiotherapist [1]. Exclusion criteria (self-reported) were other chronic illnesses than TMD (e.g., rheumatic, vascular, or psychiatric disorders), pregnancy, and inability to understand spoken and written Norwegian. Exclusion criteria (self-reported) specifically targeting other orofacial-related illnesses than TMD were rheumatoid arthritis, temporal arteritis, trigeminal neuralgia, parotitis, and sinusitis. The two TMD samples were compared with regard to years of TMD symptoms, severity of symptoms, personality traits, and general health complaints. These analyses revealed no significant group differences (all ps > .05).
Fifty-seven healthy women were recruited among graduate students, from the central university administration, and from employers at an agency providing secretarial substitutes. Exclusion criteria (self-reported) were pregnancy, chronic physical and mental illnesses, daily use of medication apart from oral contraception, and inability to understand spoken and written Norwegian.
From these samples, 25 TMD patients were matched for age (±6 years), level of education, smoking, and exercise with 25 healthy controls (Table 1). Diagnostic findings according to the RDC-TMD, e.g., diagnostic subgroups, number of craniofacial muscles painful to palpation, are listed in Table 1.
Demographic characteristics of the participants.
| TMD (n = 25) | Controls (n = 25) | |
|---|---|---|
| Age | 35.2 (SD 11.9, range 20–55 years) | 33.9 (SD 11.1, range 20–51)years |
| Body mass index | 23.1 (SD 3.8, range 16.5–29.9) | 21.8 (SD 2.9, range 18.2–28.6) |
| Regular physical exercise | 68.0% | 80.0% |
| College level education | 64.0% | 64.0% |
| Grade school only | 16.0% | 12.0% |
| Working full time (>37.5 h/week) | 56.0% | 48.0% |
| Working part time | 16.0% | 12.0% |
| Currently studying | 20.0% | 44.0% |
| Currently on sick leave | 9.0% | None |
| Disabled | None | None |
| Married/cohabiting | 48.0% | 44.0% |
| Divorced | 12.0% | 12.0% |
| Years of TMD diagnosis | 8.35 (SD 7.3, range 2–30) years | – |
| Subgroup of TMD | ||
| Arthralgia, arthrosis | 13.0% | – |
| Myalgia | 52.2% | – |
| Arthralgia + myalgia | 34.8% | – |
| Disc displacement | None | – |
| Unassisted opening (mm) | 43.6 (SD 7.9, range 29–65) | – |
| Number of painful craniofacial muscle sites | 10.5 (SD 4.3, range 2–18) | – |
| Subjective complaints of TMD symptoms | ||
| Insignificantly troubled | 4.8% | – |
| Slightly troubled | None | – |
| Moderately troubled | 33.3% | – |
| Significantly troubled | 42.9% | – |
| Seriously troubled | 19.0% | – |
| Oral splints/implants | 15.0% | – |
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Age, body mass index, years of TMD diagnosis, unassited opening, and number of painful craniofacial muscle sites in mean
The subjects were required to refrain from vigorous physical activity, drinking tea or coffee, smoking, and having large meals during the last 4 h before the experiment. Alcohol was not allowed the last 12 h before the experiment. All subjects received written information of the study, all signed an informed consent before the experiment, and were informed that they were free to withdraw any time. The study was conducted according to the Helsinki Declaration, and approved by the regional Medical Ethics Committee. All the subjects received NOK 500 (approximately USD 85, November 2010) for their participation.
2.2 Instruments and laboratory
2.2.1 Sensory threshold, pain threshold and tolerance of electrocutaneous stimulation (ES)
Electrocutaneous stimulation (50 ms pulses, 4 per s) was administered to the dorsal area of the subjects’ left hand through two electrodes with a diameter of 5 mm and a center-to-center distance of 20 mm by a Grass S48 Stimulator (Grass Techonolgies, Rockland, MA, USA) with a Grass stimulation isolation unit (SIU5B) and a Grass constant current unit (CCU1A) attached. The skin of the subjects’ left hand was cleansed with alcohol and Ag/AgCl paste applied to the electrodes. The maximum voltage was 150 V. The stimulation was controlled by the experimenter using an intensity control starting at 0 V.
The subjects were instructed to report immediately when they first noticed a sensation or «itching» (sensory threshold, E-STh), and when it became painful (pain threshold, E-PTh). The subjects were instructed to press a hand-held button the moment they found the pain to be so intense that they wanted to interrupt the stimulation (pain tolerance, E-PTo).
In addition to a baseline-test to familiarize the subjects with the stimulation procedure, one trial of electric stimulation was delivered before and after each experimental condition and during the distraction task, totalling six trials. At each point of stimulation, one single trial was used to determine the sensory, pain, and tolerance threshold, respectively. The electrical current was raised continuously until tolerance level, and there were no pauses or intervals after the sensory or pain threshold were reported.
2.2.2 Pain threshold and tolerance of algometric pressure (AP)
Pressure pain was measured by a pressure algometer (Somedic, Sollentuna, Sweden), with a 10 mm diameter stimulation probe. The rate of pressure increase was standardized by visual feedback provided by the algometer at 50 kPa/s.
Pressure algometry was applied perpendicularly to the central part of the right masseter muscle. The decision to stimulate only the right masseter was based on several studies reporting no statistical side difference in pressure pain thresholds in TMD patients [17,18,19,20]. AP of the sternum provided a non-muscular reference. The subjects were asked to raise their right index finger when the pressure became painful (pain threshold), and to press a terminate-test-button when it became so intense that they wanted to interrupt the stimulation (pain tolerance). In addition to a preliminary test to familiarize the subjects with the stimulation procedure, one trial of pressure stimulation was delivered to each subject before and after every experimental condition, totalling five trials.
2.2.3 Spontaneous or on-going pain
Before every pain assessment, spontaneous pain that was not related to the experimental stimulation (e.g., headache, joint pain) was evaluated using an electronic Visual Analogue Scale (eVAS) of 100 mm length ranging from “no pain at all” to “worst imaginable pain”.
The results of the pain tests in terms of threshold and tolerance values as well as of the assessments of sponatous pain are reported elsewhere [21].
2.2.4 Muscle activity
Surface electromyography (EMG) was recorded from the left m. masseter, the left m. biceps bracchius, and from the left and right m. trapezius. Electrodes (Blue Sensor E-10-VS, Medicotest A/S, Ølstykke, Denmark) with a diameter of 5 mm and a centerto-center distance of 20 mm, and a reference electrode placed at a bony structure, were attached to a preamplifier (1000× amplification, input impedance>5G Ohm, Premed, Oslo, Norway). The signals were run through an isolation amplifier (Burr-Brown ISO 122, Tucson, USA) without further amplification for subject safety. The skin was cleansed with ethanol and Ag/AgCl electrode paste applied to the electrodes. On the masseter muscle, the electrodes were placed on the belly of the muscle, approximately 2 cm anterior to and 1 cm above the angle of the jaw. The ground electrode was placed on the zygomatic bone. On the m. trapezius, the electrodes were placed above the descending part of the muscle, at 60% of the distance between the processes prominens (C7) and the acromion. The ground electrode was placed on the acromion. The root mean square values of the raw EMG signals were calculated over periods at 0.1 s. The signals were visually inspected for noise on an oscilloscope, and band-pass filtered with a bandwidth of 10–1000.
Only EMG responses from the masseter muscle and the left trapezius are presented, due to the data from the right trapezius being influenced by movements of the right arm and hand during the experimental manipulations.
EMG data were normalized in the following manner: data for the l. trapezius muscle was calculated as the % maximal voluntary contraction (MVC). Many individuals with clinically painful muscles are unwilling or unable to produce MVCs [22]. Therefore, the EMG data for the l. masseter are reported in absolute values only. To avoid artefacts caused by signals from the heart, the EMG data presented here are the means of the combined median values of each group.
2.2.5 Cardiovascular activity
Laser-doppler skin blood flux (LDF) changes were recorded with a Perimed Multichannel Laser Doppler System (PeriFlux 4001 Master, Perimed, Sweden). Miniature probes (Perimed, Sweden) were attached on the left m. masseter area (placing the sensor 2 cm anterior to the center of the EMG electrodes) and on the ventral side of the left thumb. This instrument expresses skin blood flow in arbitrary units of flux, proportional to the velocity and concentration of red blood cells moving in the superficial layer of the skin. Therefore, the analyses of group differences in LDF are based on the percentage of change from baseline. The analyses of within-subject differences are based on the arbitrary units [23].
As the EMG and LDF measurements are superficial and the probes do not exert pressure on the skin, there is probably very little risk of interference between EMG electrodes and LDF probes.
Mean arterial pressure (MAP) and HR were monitored by the Peñaz method (Finapres, Ohmeda 2300, Englewood, CO, USA). The cuff containing a photoelectronic sensor was attached to the middle phalanx of the third finger on the subjects’ left hand. This system provides a reliable measure of the MAP if the temperature of the hand is not too low. Change scores ( Δ-scores) were computed of MAP and HR by subtracting task values from baseline (pre-task relaxation) values [24].
All signals were AD-converted (12 bit A/D card, AT-MIO-16E-10, National Instruments, Austin, Texas, USA) with a sampling frequency of 2000 Hz, stored and reduced by LabView (National Instruments, Austin, TX, USA).
2.3 Procedure
For an overview of the experimental procedure, see Fig. 1.
Timeline of the experimental procedure.
The subjects were seated in an upright position in a sound-attenuated and electro-magnetically shielded room the size of 2.8 m × 2.9 m with a temperature of 22 °C. The only person present in the room apart from the participant was the female experimenter (CM). A research assistant monitored the experimenter and the subject behind a one-way mirror. The psychophysiological experiment lasted 2–2.5 h. All subjects went through the experimental manipulations in the same order. Upon entering the laboratory, the subjects went through two trials of pain stimulation to become familiarized with these tests and learn how to interrupt the stimulation.
2.3.1 Reading task
This task was intended as habituation to the laboratory and the experimental situation. After the subjects relaxed quietly for 1.5 min (baseline), they read aloud for 1.5 min from a chapter in a book of the ancient history of Australia, a topic intended as neutral or non-arousing. After reading, subjects again relaxed 1.5 min before a pain stimulation trial (ES and AP) was performed.
2.3.2 Personal involvement speech
After a relaxation period of 3 min (baseline), the subjects were instructed to prepare themselves for a simulated job interview, concentrating on their professional and personal skills, achievements they were proud of, work habits, etc. They were first told to plan their speech, and then to start talking when the experimenter asked them to. If the subjects had difficulties speaking freely, the experimenter prompted them by questions relevant to their education and work. Both the planning and the speaking phases lasted 3 min. After the interview, a pain stimulation trial (ES and AP) was performed followed by a relaxation period of 3 min.
2.3.3 Computer-based tracking test/cognitive distraction
This condition was initiated by a training period followed by 3 min relaxation (baseline). The task consisted of tracking a black square (1.5 × 1.5 cm) moving across the computer screen in front of the subjects, with the cursor controlled by the computer mouse. Every time the subject failed to keep the cursor on the black square, the screen turned red to provide the subject with immediate feedback of failure. After 1.5 min of tracking, E-STh, E-PTh and E-PTo were assessed while the subjects continued performing the task. After the pain stimulation, the subjects continued the task for an additional 1.5 min. All of the subjects were able to continue the task during the pain stimulation. The subjects’ performance on the task was not recorded. After this task, the subjects relaxed for 3 min before a pain stimulation trial (ES and AP) was performed.
2.3.4 Isometric jaw-muscle contraction (IMC)
After a 1.5 min relaxation period (baseline) the subjects bit on a custom made U-shaped occlusal force meter (height 1.5 cm, length 10 cm) for 1 min. The subjects were instructed to use sufficient bite force to keep a cursor posited at a mark on an oscilloscope, corresponding to 29.4 N. This is a relatively low level of force, and it was chosen to ensure that also the TMD patients were able to perform the contraction test for a full 1 min. Immediately after this task, a pain stimulation trial (ES and AP) was performed.
2.3.5 Maximal voluntary contraction (MVC) of the trapezius muscles
At the end of the experimental session, the subjects kept their upper arms abducted 45° in the scapular plane at maximum force for 10 s. They pulled force transducers through wires attached diagonally (about 90° to the upper arms) to fasteners on adjustable cuffs that were applied just above the elbow joints. The experimenter constantly encouraged them to pull as hard as possible to ascertain use of maximum force. Contraction was performed twice, and the MVC giving the highest EMG response was used. According to Mathiassen et al., the performing of MVC is not affected by preceding cognitive tasks [25].
2.3.6 Subject based reports of affect
After each cognitive task, the subjects reported on their affective experience during the task on 13 paper-and-pencil VAS scales, ranging from «not at all» (at 0 mm) to «maximally» (at 100 mm). From this report, two indices of affective experience during the tasks were computed. The positive affect index (PI) consisted of “was committed”, “was satisfied with own performance”, “felt relaxed”, “was in control”, and “own performance was important”. The negative affect index (NI) consisted of “felt tense”, “lost interest”, “did not bother to make an effort”, “felt embarrassed”, “got depressed”, “got worried”, “was annoyed”, and “felt distressed”.
The subjects filled in the state-version of the Spielberger State-Trait Personality Inventory before the habituation task, after the personally relevant stress task, and after the experiment was finished [26,27].
After the experimental session, the subjects answered several questionnaires on physical health, attitudes, coping styles and personality traits. These data fall outside of the aim and score of this paper and will be reported elsewhere.
2.4 Data analysis
The pain stimulation trials selected for analyses were the trials performed before and after the reading task. In order to obtain a more valid measure of group differences in pain sensitivity, these two stimulation trials were aggregated into one mean value. The purpose of the other pain stimulation trials of the experiment was the study of changes in pain perception related to attention manipulation and cardiovascular responding, and these are reported elsewhere.
The physiological data from the experimental tasks were averaged for 1-min (relaxation before reading and isometric contraction, reading task, tracking task, and isometric contraction) and 3-min periods (relaxation before job interview and tracking task, job interview). The data recorded during ES were averaged for 1-s epochs immediately preceding the report of threshold and tolerance. The data recorded during the AP were averaged for the entire stimulation period, which never lasted more than 10 s.
The statistical procedures were conducted using SPSS, release 14 (SPSS Inc., Chigaco, IL, USA). Preliminary analyses of the sample distributions included determination of kurtosis, skewness, and outliers. With the sample size used in this study, results may be unduly influenced by extreme scorers. In some of the analyses, one or two outliers (i.e., scores 3 SD above or below the mean) were excluded. The number of subjects included in the analyses is indicated in each table.
The alpha level was set at .05.
Independent samples t-tests were conducted to assess group differences in EMG, MAP, and HR during rest, experimental tasks, and pain stimulation, and affective responding after tasks. Group × phase interaction effects involving EMG, MAP, HR, and affective responding were computed using repeated-measures ANOVAs with post hoc comparisons. As the analysis of group differences in arbitrary units of LDF is not possible, no interaction analysis was undertaken with this particular parameter. For LDF data, percentage of change from baseline to task or pain stimulation was calculated and independent samples t-tests used to assess group differences. Main effects of changes in LDF from baseline to task were based on arbitrary units and conducted with repeated-measures ANOVAs. Changes in EMG from relaxation to task or pressure pain (%EMG) and normalized EMG data (%EMGMAX) were analyzed with independent samples t-tests. Cohen’s d’s were calculated to describe effect sizes.
Due to large intra-group variability, Mann–Whitney U-tests were used for the analyses of group differences in resting, task level and pain stimulation level EMG.
Due to technical problems, EMG data from four healthy participants were lost. The electrocutaneous stimulation produced noise in the EMG. Hence, EMG data are not presented for this type of stimulation.
3 Results
3.1 Orofacial psychophysiological responding during painful tasks
The results of the pain tests in terms of threshold and tolerance values as well as of the assessments of sponatous pain are reported elsewhere [21]. Briefly, there were no statistically significant group differences in electrocutaneous or pressure pain sensitivity at the assessments selected for the current study.
3.1.1 Masticatory load
The masseter EMG levels during IMC (z = 2.31, p < .05) was significantly lower in the TMD group. For both groups, masseter and trapezius EMG increased from relaxation to IMC (Table 2). There were no significant group differences in orofacial SBF during IMC, and the changes in orofacial SBF from relaxation to IMC were significant in both groups (Table 6).
Electromyography (EMG) levels at rest and during experimental tasks.
| Task | TMD patients Mean (SD)[a] | Controls Mean (SD)[a] | F (group × phase) | d |
|---|---|---|---|---|
| Relaxation EMG l. mas. | 1.5 (1.3) | 2.3 (1.3) | 2.58 ns | –0.56 |
| Reading EMG l. mas. | 1.8 (1.4) | 2.7 (1.5) | –0.61 | |
| F (phase) 50.75[***] | ||||
| Relaxation EMG l. trap. | 2.9 (3.3) | 5.7 (9.8) | 0.01 ns | –0.37 |
| Reading EMG l. trap. | 2.7 (2.7) | 5.5(10.5) | –0.37 | |
| F (phase) 0.19 ns | ||||
| Relaxation EMG l. mas. | 1.4(1.1) | 2.2 (1.3) | 2.15 ns | –0.69 |
| Job interview EMG l. mas. | 1.8 (1.3) | 3.1 (2.4) | –0.69 | |
| F (phase) 13.59[***] | ||||
| Relaxation EMG l. trap. | 3.5 (5.3) | 5.0 (8.9) | 2.23 ns | –0.21 |
| Job interview EMG l. trap. | 4.0 (6.1) | 4.4 (6.3) | –0.07 | |
| F (phase) 0.02 ns | ||||
| Relaxation EMG l. mas. | 1.4 (1.2) | 2.1 (1.2) | 0.32 ns | –0.66 |
| Tracking EMG l. mas. | 1.5 (1.3) | 2.1 (1.4) | –0.46 | |
| F (phase) 0.00 ns | ||||
| Relaxation EMG l. trap. | 2.0 (2.1) | 3.5 (3.9) | 0.06 ns | –0.46 |
| Tracking EMG l. trap. | 5.6 (6.3) | 7.4 (5.8) | –0.29 | |
| F (phase) 23.13[***] | ||||
| Relaxation EMG l. mas. | 1.2 (1.0) | 2.0(1.2) | 2.56 ns | –0.70 |
| IMC EMG l. mas. | 9.0 (9.0) | 12.2(11.6) | –0.31 | |
| F (phase) 46.73[**] | ||||
| Relaxation EMG l. trap. | 2.6 (3.6) | 5.4 (7.5) | 2.21 ns | –0.48 |
| IMC EMG l. trap. | 3.1 (4.1) | 7.1 (8.1) | –0.63 | |
| F (phase) 6.48[*] | ||||
| MVC l. trap. | 115.0(111.0) | 260.2(175.2) |
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Measurement units: µV; l. mas.: left masseter; l. trap.: left trapezius; IMC: isometric contraction of the masticatory muscles; MVC: maximal voluntary contraction; F (group × phase): significance test of group × phase interaction effects in change from relaxation to task. F (phase): significance test of changes from relaxation to task; ns: non-significant; d: Cohen’s d, effect size assessment of group differences. N = 45–46
3.1.2 Electrocutaneous pain
There were no significant group differences in %LDF change from baseline throughout the electrocutaneous stimulation period (Fig. 2).
Orofacial and digital LDF during electrocutaneous pain stimulation.
There were significant increases in orofacial LDF from E-PTh to E-PTo in the TMD group (F[1,24] = 7.2, p < .001), but not in the control group (Fig. 2). In both the TMD (F[1,24] = 20.06, p < .001) and the control group (F[1,24] = 14.76, p < .001), there were significant reductions in digital LDF from baseline to E-STh, and from E-STh to E-PTh (Fig. 2).
3.1.3 Pressure pain
Relative to the control group, the masseter EMG of the TMD group was significantly lower during masseter pressure stimulation (z = 2.43, p < .05). There were no statistically significant group × phase interaction effects regarding absolute EMG response to pressure pain stimulation. There were two significant phase effects, however (Table 3).
Changes in electromyography (EMG) from baseline to pressure pain stimulation.
| Pressure pain | TMD patients Mean (SD)[a] | Controls Mean (SD)[a] | F (group × phase) | d |
|---|---|---|---|---|
| Masseter | ||||
| l. masseter | 2.1 (2.3) | 3.6 (4.2) | 1.02 ns | –0.46 |
| F (phase) 5.94[*] | ||||
| l. trapezius | 4.3 (5.6) | 5.9 (7.9) | 2.34 ns | –0.23 |
| F (phase) 4.06[*] | ||||
| Sternum | ||||
| l. masseter | 1.7 (1.5) | 2.4 (1.4) | 0.08 ns | –0.47 |
| F (phase) 3.95 ns | ||||
| l. trapezius | 4.2 (4.9) | 6.4 (7.1) | 0.44 ns | –0.36 |
| F (phase) 3.94 ns |
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Measurement units: μV; t (group): significance test of group differences; F (group × phase): significance test of group × phase interactions in change from baseline (the resting period prior to the reading task, numbers given in Table 3) to pain stimulation; F (phase): significance test of changes from relaxation to task; ns: non-significant; d: Cohen’s d, effect size assessment of group differences. N = 46
In terms of %EMG change from relaxation to pressure stimulation, the masseter response of the TMD group (M = 106.0, SD = 10.1) was significantly greater than that of the control group (M = 98.3, SD = 5.9) (t[42] = 3.07, p < .01) during sternum pressure pain. There were no group differences in trapezius %EMG change from relaxation or %EMGMAX response during pressure pain stimulation (data not shown).
The analyses of group differences in %LDF from baseline to the onset of masseter and sternum stimulation revealed no significant effects (Table 4). However, there were significant phase effects, in that both groups responded to the pressure stimulation with orofacial and digital LDF changes (Table 4).
Changes in laser-doppler flowmetry (LDF) from baseline to pressure pain stimulation.
| Pressure pain | TMD patients Mean (SD)% change | Controls Mean (SD)% change | t (group) | d |
|---|---|---|---|---|
| Masseter | ||||
| Orofacial | 120.2 (33.1) | 130.3 (45.6) | 0.89 ns | –0.25 |
| F (phase) 13.33[***] | ||||
| Digital | 85.1 (33.7) | 91.0 (56.8) | 0.44 ns | –0.13 |
| F (phase) 3.55 ns | ||||
| Sternum | ||||
| Orofacial | 110.5 (40.6) | 132.1 (67.9) | 1.34 ns | –0.39 |
| F (phase) 20.14[***] | ||||
| Digital | 79.4 (23.9) | 92.5 (49.1) | 1.20 ns | –0.34 |
| F (phase) 31.41[***] |
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Measurement unit: percentage of change from baseline to task (the resting period prior to the reading task); t (group): significance test of group differences, in change scores (2-tailed); F (phase): significance test of changes from relaxation (the resting period prior to the reading task, numbers given in Table 3) to task, in arbitrary units; ns: non-significant; d: Cohen’s d, effect size assessment of group differences. N = 49–50
3.2 Generalized psychophysiological responding during painful tasks
3.2.1 Masticatory load
For both groups, the increase in MAP from relaxation to IMC was significant (Table 7).
3.2.2 Electrocutaneous pain
There were no significant group × phase interactions regarding the increase in MAP from baseline to E-STh and throughout the stimulation period. Both groups evidenced significant changes in MAP from E-PTh to E-PTo (F[1,48] = 10.80, p < .001) (Fig. 3).
MAP and HR during electrocutaneous pain stimulation.
Similarly, there were no significant group × phase interactions regarding the increase in HR from baseline to E-STh and throughout the stimulation period. Both groups evidenced significant increases in HR across the stimulation period (F[1,48] = 16.34, p < .001) (Fig. 3).
No group differences were found in the t-tests of MAP and HR change (from baseline to the onset of electrocutaneous stimulation (Δ-scores) (data not shown).
3.2.3 Pressure pain
There were no interaction effects, but significant changes in MAP and HR from baseline to pressure stimulation for both groups (Table 5).
No physiological registrations at separate threshold- and tolerance levels were made during pressure pain stimulation, therefore, no analysis of the LDF, MAP, and HR changes due to increasing levels of this type of pain could be performed.
Changes in mean arterial pressure (MAP) and heart rate (HR) from baseline to pressure pain stimulation.
| Pressure pain | TMD patients Mean (SD) | Controls Mean (SD) | F (group × phase) | d |
|---|---|---|---|---|
| Masseter | ||||
| MAP | 105.5 (11.5) | 104.5 (13.8) | 0.19 ns | 0.08 |
| F (phase) 18.80[***] | ||||
| HR | 72.9(11.0) | 70.7 (12.7) | 0.55 ns | 0.19 |
| F (phase) 22.52[***] | ||||
| Sternum | ||||
| MAP | 105.7 (13.3) | 106.0 (15.6) | 0.03 ns | –0.02 |
| F (phase) 20.34[***] | ||||
| HR | 70.2 (9.8) | 66.1 (12.3) | 2.98 ns | 0.37 |
| F (phase) 0.38 ns |
-
Measurement units: mmHg (MAP), bpm (HR); F (group × phase): significance test of interaction effects in change from baseline (the resting period prior to the reading task, numbers given in Table 5) to pain stimulation; F (phase): significance test of changes from relaxation (the resting period prior to the reading task, numbers given in Table 3) to task; ns: non-significant; d; Cohen’s d, effect size assessment of group differences. N = 49–50
No group differences were found in the t-tests of MAP and HR change (from baseline to the onset of pain stimulation, Δ-scores) (data not shown).
3.3 Orofacial psychophysiological responding during cognitive tasks
The resting masseter EMG levels prior to reading (z = 2.29, p < .05), job interview (z = 2.13, p < .05), tracking (z = 2.12, p < .05) and the IMC (z = 2.17, p < .05) were significantly lower in the TMD group (Table 2).
The masseter EMG levels during reading (z = 2.53, p < .05) and the job interview (z = 2.48, p < .05) were significantly lower in the TMD group.
The MVC response of the l. trapezius was significantly lower for the TMD patients than for the healthy controls (z = 3.03, p < .01).
There were no significant group × phase interaction effects regarding any of the changes in masseter or trapezius EMG from relaxation to task, but several significant phase effects (Table 2).
As the EMG levels during the relaxation periods were lower in the TMD group, percentages of EMG change from relaxation to task were calculated. There were no significant group differences in these variables (data not shown).
In terms of %EMGMAX response, the change in trapezius EMG due to the job interview of the TMD patients (M= 3.5, SD = 2.8) was significantly greater than that of the control group (M= 1.7, SD = 1.4) (t[46] = 2.80, p < .01).
There were no significant group differences in percentage of change in LDF from baseline to task (Table 6). However, there were several significant phase effects (Table 6).
Changes in laser-doppler flowmetry (LDF) levels from relaxation to task.
| TMD patients Mean (SD) % change | Controls Mean (SD) % change | t (group) | d | |
|---|---|---|---|---|
| Reading aloud | ||||
| Orofacial | 247.3(124.8) | 245.8(146.1) | –0.04 ns | 0.01 |
| F (phase) 73.81[***] | ||||
| Digital | 84.8 (20.9) | 96.5 (23.3) | –1.33 ns | –0.53 |
| F (phase) 6.67* | ||||
| Job interview | ||||
| Orofacial | 228.7 (88.5) | 221.8(100.3) | –0.26 ns | 0.07 |
| F (phase) 119.78[***] | ||||
| Digital | 77.8(41.9) | 102.5 (51.2) | –1.80 ns | –0.53 |
| F (phase) 7.63[**] | ||||
| Tracking | ||||
| Orofacial | 106.1 (83.5) | 104.2(91.3) | –0.64 ns | 0.02 |
| F (phase) 0.03 ns | ||||
| Digital | 77.9 (32.7) | 85.3 (26.3) | –0.78 ns | –0.25 |
| F (phase) 16.56[***] | ||||
| IMC | ||||
| Orofacial | 101.6(21.3) | 113.7(22.4) | –1.94 ns | –0.55 |
| F (phase) 0.42 ns | ||||
| Digital | 82.2 (27.5) | 90.9 (22.6) | –1.21 ns | –035 |
| F (phase) 21.08[***] |
-
IMC: isometric contraction of the masticatory muscles. t (group): significance test of group differences, in change scores (2-tailed); F (phase): significance test of changes from relaxation to task, in arbitrary units; ns: non-significant; d: Cohen’s d, effect size assessment of group differences. N = 45–49
3.4 Generalized psychophysiological responding during cognitive tasks
The resting MAP level prior to the job interview was significantly higher in the TMD patients (t[49] = −2.32, p < .05) (Table 7).
Mean arterial pressure (MAP) and heart rate (HR) levels at rest and during experimental tasks.
| Task | TMD patients Mean (SD) | Controls Mean (SD) | F (group × phase) | d |
|---|---|---|---|---|
| Relaxation MAP | 101.6(10.2) | 96.8 (9.8) | 0.05 ns | 0.47 |
| Reading MAP | 110.3(10.6) | 106.4 (9.3) | 0.39 | |
| F (phase) 137.43[***] | ||||
| Relaxation HR | 68.0 (9.9) | 67.1 (11.7) | 0.79 ns | 0.08 |
| Reading HR | 76.6(10.4) | 74.5(11.6) | 0.19 | |
| F (phase) 139.78[***] | ||||
| Relaxation MAP | 101.6(12.4) | 94.3 (9.2) | 0.00 ns | 0.67 |
| Job interview MAP | 115.4(13.7) | 110.2(14.0) | 0.38 | |
| F (phase) 114.57[***] | ||||
| Relaxation HR | 68.6 (8.9) | 65.9(11.4) | 1.91 ns | 0.26 |
| Job interview HR | 78.1 (10.7) | 78.1 (13.4) | 0.00 | |
| F (phase) 124.79[***] | ||||
| Relaxation MAP | 100.9(12.3) | 100.2(13.4) | 0.02 ns | 0.05 |
| Tracking MAP | 105.6(13.9) | 105.1 (13.3) | 0.04 | |
| F (phase) 73.36[***] | ||||
| Relaxation HR | 68.6 (9.6) | 66.4(11.6) | 0.18 ns | 0.21 |
| Tracking HR | 74.3 (10.7) | 71.2(13.2) | 0.26 | |
| F (phase) 25.20[***] | ||||
| Relaxation MAP | 99.8(12.5) | 97.0(11.9) | 0.01 ns | 0.23 |
| IMC MAP | 103.7(13.1) | 102.5 (14.3) | 0.09 | |
| F (phase) 38.19[***] | ||||
| Relaxation HR | 67.4 (9.2) | 65.3 (9.2) | 1.11 ns | 0.23 |
| IMC HR | 67.9 (8.3) | 65.8 (9.9) | 0.23 | |
| F (phase) 1.11 ns |
-
Measurement units: mmHg (MAP), bpm (HR); IMC: isometric contraction of the masticatory muscles; F (group × phase): significance test of group × phase interactions in change from relaxation to task; F (phase): significance test of changes from relaxation to task. ns: non-significant; d: Cohen’s d, effect size assessment of group differences. N = 47–50
There was no statistically significant group × phase interaction effect on any of the changes in MAP or HR from baseline to task, but most of the phase effects were significant (Table 7).
There were no significant group effects on the Δ-scores of MAP and HR for any task (data not shown).
As the experimental tasks were presented in the same order for all the participants, carry-over effects may occur. In order to investigate this possibility, repeated measures analyses were conducted of the physiological responses during the recovery periods after each task (data not shown). There were no effects of group or condition on any of the physiological measures, the exception being digital LDF, which was significantly lower after the job interview than after the reading task (F[1,47] = 6.58, p < .01) for both groups. This may be the result of a pain stimulation trial that was performed immediately prior to the post-interview recovery period.
3.5 Affective responding during the experiment
At the start of the experiment, the TMD group reported significantly more state anxiety than the controls (t[48] = 2.49, p < .05). After the job interview, the TMD patients reported significantly more state anxiety (t[48] = 2.28, p < .05) and state depression (t[48] = 2.26, p < .05) than the control group did (Fig. 4). There were no significant group differences in state anger or state curiosity (data not shown).
Main scores of state-anxiety and state-depression at baseline (at the start of the experiment), after the interview, and after isometric contraction.
Repeated measures ANOVAs of the responses to the STPI-State revealed no significant group × phase interaction effects. There were significant effects of phase, in that all subjects rated themselves as more anxious after the job interview (F[1,47] = 9,32, p < .001) and as less depressed at the end of the experiment (F[1,47] = 9.29, p < .001) compared to the other assessments (Fig. 4). Both groups reported lower levels of curiosity after the job interview compared to the other assessments (F[1,47] = 8.11, p < .001) (data not shown). There were no significant phase effects of state anger (data not shown).
Regarding the paper-and-pencil VAS assessments of psychological experience to the experimental tasks (data not shown), the TMD patients rated the job interview as more negative (NI) (t[48] = 2.21, p < .05) and less positive (PI) (t[48] = 2.30, p < .05) than the control group did. There were no significant group × phase interaction effects regarding responses to the VAS assessments. There were effects of phase, as all the participants rated the job interview to be a less positive (F[1,48] = 14.46, p < .001) and more negative (F[1,48] = 13.78, p < .001) experience than the reading and tracking tasks.
4 Discussion
There were significantly lower levels in masseter EMG in the TMD group during masticatory load, pressure pain stimulation of the orofacial region, relaxation, and cognitive tasks. Moreover, compared to the controls, the TMD patients exhibited higher levels of negative affect on some of the assessments during the experiment. However, this study generated no group differences in generalized physiological responding to pain stimulation or cognitive challenges.
4.1 Muscular responding during painful and non-painful tasks
Our findings of lower masseter EMG responding in the TMD group compared to the controls during masticatory load are in accordance with other studies [30,31]. Others, however, have demonstrated elevated masseter EMG during clenching in TMD groups compared to controls [32,33]. However, the two latter studies tested only pain-free women, and the number of subjects was low (N = 8–14). Possibly, masticatory clenching in chronic orofacial pain patients may generate different muscular responses than in pain-free individuals.
The masseter EMG was significantly lower in the TMD group during ipsilateral masseter pressure pain. It may be argued that the lower EMG levels in the TMD group may be due to chronic pain patients’ tendency to report lower experimental pain thresholds in general and thus to reach their threshold levels faster than healthy controls. However, compared to the control group, the TMD participants in the present study did not exhibit significantly lower pressure pain thresholds during the relevant assessments [21]. This indicates that their lower EMG responding during pressure pain is not a factor of a shorter duration of pressure stimulation.
Compared to the pain-free controls, the TMD patients exhibited lower masseter EMG during the reading aloud task and the simulated job-interview. Previous findings of symptom-specific psychophysiological responses in pain patients suggest that personally relevant emotional challenges result in muscular hyperactivity, which in turn may generate chronic muscle pain [3,28]. The lower masseter EMG of the present TMD patients compared to the control group is at variance with this theory, but may be interpreted as a consequence of pain. The Pain Adaptation Model explains muscle hypoactivity as resulting from reduced agonist muscle activity in order to avoid an exacerbation of pain [29]. Pain was induced and/or exacerbated during masticatory load and pressure stimulation, and both the reading task and the job interview implied movement of the jaw due to speaking. These activities may have triggered guarding behaviour of the orofacial muscles, and the present results may be taken in support of the Pain Adaptation Model [29].
However, the recently formulated Integrated Pain Adaptation Model may also be able to explain the current results [34]. This model suggests that it is not possible to ascribe a uniform effect of pain on motor activity, and that muscular responses to pain will vary as a result of individual characteristics such as motivation, pain-related affect, and other psychosocial variables. One implication of the model is that if an individual is highly distressed during pain, the concurrent central nervous system activity may influence the muscular output. The TMD group’s high self-reported levels of affective distress during the experiment could be interpreted as support in favour of the Integrated Pain Adaptation Model [34]. Bearing in mind the novelty of this model and the as yet lacking exploration of its hypotheses, the interpretation of our results remains somewhat speculative. Moreover, we did not control for consumption of analgesic or muscle relaxant medication in the TMD group. Muscle relaxants in particular may attenuate EMG responding and our lack of control for this possible confounding factor is a limitation of the present study [35].
4.2 Cardiovascular responding during painful and non-painful tasks
There were no group differences in orofacial SBF during the experiment. In pain-free individuals, focal skin vasoconstriction has previously been reported during contractions of the trapezius muscles in combination with a cognitive task [14]. In fibromyalgia patients, vasoconstriction and reduced temperature of the skin superficial to tender points have been demonstrated [13]. The authors suggest that dysregulated sympathetic nervous processes, resulting in abnormal secretion of adrenaline and noradrenaline, may produce this local hypoxia [13]. Although not statistically significant, the increase in orofacial SBF of the TMD patients from relaxation to orofacial clenching was not as large as that of the control group in our study.
Both groups exhibited increased orofacial SBF and reduced digital SBF at the onset of electrocutaneous and masseter pressure stimulation relative to the baseline period. As the digital vasoconstriction was seen not only in response to electrocutaneous stimulation of the ipsilateral hand, but also in response to pressure stimulation of the masseter, the present study together with the results of Vassend and Knardahl [36] challenge the claim of Kemppainen et al. [15,37] that constriction or dilatation of the skin blood vessels occur in response to regional pain stimulation only. We demonstrated the blood flow changes as early as at the onset of stimulation, while Kemppainen et al. showed the vascular changes to require stimulation at the pain threshold level [15,37]. Kemppainen et al.’s subjects (Ns = 6–8) were colleagues and students of the experimenters who had participated in several similar studies and who may have developed a habituated LDF response to pain stimulation. The participants of the present study (N = 50) were not familiar with this type of studies and were unknown to us. This might have resulted in their demonstrating vascular responses at an earlier stage of the electrocutaneous and pressure stimulation.
Our findings indicate that skin blood flow responses are sensitive to low levels of sensory stimulation. This recording method seems to be a promising tool for future psychophysiological research.
Regarding systemic physiological responding to the experimental manipulations in the two groups, the overall picture is one of remarkable similarity. Apart from a higher MAP level prior to the job interview in the TMD group, there were no significant group differences in baseline-level cardiovascular physiology. Both groups demonstrated increased levels of MAP and HR during the experimental tasks relative to the preceding resting periods, indicating that the experimental manipulations had the desired arousing effects.
Relative to the controls, the TMD patients were clearly more distressed during the experiment, as evidenced by their report of higher levels of state anxiety and depression as well as a more negative experience of the job-interview. However, as noted above, the physiological responses to the cognitive tasks were largely similar in the two groups. Similar findings of group differences in negative affect, but not in physiological responding, are well known in TMD patients. Consistently, TMD patients as well as other chronic pain groups, tend to report elevated levels of psychological distress, e.g., depressive symptoms, irritability, and negative rumination, while physical examinations show nothing abnormal apart from increased musculoskeletal pain and fatigue [38]. Possibly, TMD patients may experience more psychological distress in novel or challenging situations, and this response tendency may be part of the explanation for their relatively higher levels of trait-like negative affect and report of subjective health complaints.
4.3 Limitations of the present study
The sample sizes were relatively low. Some of the non-significant group differences may have turned out statistically significant with larger samples.
Second, all the subjects were women. Women tend to respond differently to acute pain stimulation than men do [39]. This gender-dependent response may be related to differences of reproductive hormones. Menstrual cycle was not controlled for in the current study. Hence, our results may not generalize to the male population. Previous research in this field has typically involved mixed-gender samples of chronic pain patients or all-male samples [15,37].
Third, there is some evidence that personality traits and ways of coping with challenges may influence psychophysiological responding [40]. The low number of subjects in the present study did not permit statistical analyses that included control for personality traits or other measures of individual differences. However, in a study of a larger sample of the healthy participants in this project, there were no effects of personality traits on CV responses during the different experimental tasks [36].
5 Conclusions
The low EMG responses in the TMD group are carefully supportive of both the Pain Adaptation Model and the Integrated Pain Adaptation Model. The striking group similarities in cardiovascular responding in combination with the elevated levels of negative state affect in the TMD patients suggest that psychological factors are better able to separate cases from controls than are the assessments of generalized physiological responding employed in this study.
DOI of refers to article: 10.1016/j.sjpain.2011.01.004.
Acknowledgements
Dr. Berit Schie Krogstad performed the diagnostic assessment of the TMD patients. Ms. Cathrine Bjordal Bergheim, Ms. Merete Nyrerød, and Ms. Eva Helene Mjelde provided technical assistance during the psychophysiological experiment. Mr. Øystein Klingenberg, Dr. Dagfinn Matre, and Mr. Dag Erik Eilertsen were responsible for computer programming. This study was supported by Grant 112672/330 from the Norwegian Research Council.
References
[1] Dworkin SF, LeResche L. Research diagnostic criteria for temporomandibular disorders. J Craniomandib Disord Facial Oral Pain 1992;6:301–55.Search in Google Scholar
[2] Svensson P, Graven-Nielsen T. Craniofacial muscle pain: review of mechanisms and clinical manifestations. J Orofac Pain 2001;15:117–45.Search in Google Scholar
[3] Flor H, Birbaumer N, Schulte W, Roos R. Stress-related elecromyographic responses in patients with chronic temporomandibular pain. Pain 1991;46:145–52.Search in Google Scholar
[4] Nicholson RA, Townsend DR, Gramling SE. Influence of a scheduled-waiting task on EMG reactivity and oral habits among facial pain patients and no-pain controls. Appl Psychophysiol Biofeedback 2000;25:203–19.Search in Google Scholar
[5] Schroeder H, Siegmund H, Santibanez HG, Kluge A. Causes and signs of temporomandibular joint pain and dysfunction: an electromyographic investigation. J Oral Rehabil 1991;18:301–10.Search in Google Scholar
[6] Sarlani E, Greenspan JD. Evidence for generalized hyperalgesia in temporomandibular disorder patients. Pain 2003;102:221–6.Search in Google Scholar
[7] Vassend O, Krogstad BS, Dahl BL. Negative affectivity, somatic complaints, and symptoms of temporomandibular disorders. J Psychosom Res 1995;39: 889–99.Search in Google Scholar
[8] Hedenberg-Magnusson B, Ernberg M, Kopp S. Symptoms and signs of temporomandibular disorders in patients with fibromyalgia and local myalgia of the temporomandibular system. Acta Odontol Scand 1997;55: 344–9.Search in Google Scholar
[9] Fillingim RB, Maixner W, Kincaid S, Sigurdsson A, Harris MB. Pain sensitivity in patients with temporomandibular disorders: relationship to clinical and psychosocial factors. Clin J Pain 1996;12:260–9.Search in Google Scholar
[10] Maixner W, Fillingim R, Booker D, Sigurdsson A. Sensitivity of patients with painful temporomandibular disorders to experimentally evoked pain. Pain 1995;63:341–51.Search in Google Scholar
[11] Aaron LA, Burke MM, Buchwald D. Overlapping conditions among patients with chronic fatigue syndrome, fibromyalgia, and temporomandibular disorders. Arch Intern Med 2000;160:221–7.Search in Google Scholar
[12] Bandler R, Shipley MT. Columnar organization in the midbrain periaqueductal gray: modules for emotional expression? Trends Neurosci 1994;17:379–89.Search in Google Scholar
[13] Jeschonneck M, Grohmann G, Hein G, Sprott H. Abnormal microcirculation and temperature in skin above tender points in patients with fibromyalgia. Rheumatology 2000;39:917–21.Search in Google Scholar
[14] Larsson SE, Larsson R, Zhang Q, Cai H, Öberg PÅ. Effects of psychophysiological stress on trapezius muscles blood flow and electromyography during static load. Eur J Appl Physiol 1995;71:493–8.Search in Google Scholar
[15] Kemppainen P, Forster C, Handwerker HO. The importance of stimulus site and intensity in differences of pain-induced vascular reflexes in human orofacial regions. Pain 2001;91:331–8.Search in Google Scholar
[16] Ohrbach R, Blascovich J, McCall WD, Dworkin SF. Psychophysiological assessment of stress in chronic pain: comparisons of stressful stimuli and of response systems. J Dent Res 1998;77:1840–50.Search in Google Scholar
[17] Isserlée H, De Laat A, De Mot B, Lysens R. Pressure-pain threshold variation in temporomandibular disorder myalgia over the course of the menstrual cycle. J Orofac Pain 2002;16:105–17.Search in Google Scholar
[18] Svensson P, Arendt-Nielsen L, Nielsen H. Effect of chronic and experimental jaw muscle pain on pain-pressure thresholds and stimulus–response curves. J Orofac Pain 1995;9:347–56.Search in Google Scholar
[19] McMillan AS, Blasberg B. Pain-pressure threshold in painful jaw muscles following trigger point injection. J Orofac Pain 1994;8:384–90.Search in Google Scholar
[20] List T, Helkimo M, Karlsson R. Pressure pain thresholds in patients with craniomandibular disorders before and after treatment with acupuncture and occlusal splint therapy: a controlled clinical study. J Orofac Pain 1993;7:275–82.Search in Google Scholar
[21] 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;24:343–52.Search in Google Scholar
[22] Geisser ME, Ranavaya M, Haig AJ, Roth RS, Zucker R, Ambroz C, Caruso M. A meta-analytic review of surface electromyography among persons with low back pain and normal, healthy controls. J Pain 2005;6:711–26.Search in Google Scholar
[23] Vassend O, Knardahl S. Effects of electrocutaneous pain stimulation on facial blood flow. Biol Psychol 2005;68:163–78.Search in Google Scholar
[24] Fahrenberg J, Foerster F, Wilmers F. Is elevated blood pressure level associated with higher cardiovascular responsiveness in laboratory tasks and with response specificity? Psychophysiol 1995;32:81–91.Search in Google Scholar
[25] Mathiassen SE, Winkel J, Hägg GM. Normalization of surface EMG amplitude from the upper trapezius muscle in ergonomic studies – a review. J Electromyogr Kinesiol 1995;5:197–226.Search in Google Scholar
[26] Spielberger CD. 1979. Preliminary manual for the State-Trait Personality Inventory. Unpublished manual. Tampa: University of South Florida; 1979.Search in Google Scholar
[27] Håseth K, Spielberger CD. Foreløpig manual for Det norske tilstand-trekk personlighets-inventorium (STPI-N). Unpublished manuscript. Oslo: University of Oslo; 2000.Search in Google Scholar
[28] Flor H, Birbaumer N, Schugens MM, Lutzenberger W. Symptom-specific psychophysiological responses in chronic pain patients. Psychophysiology 1992;29:452–60.Search in Google Scholar
[29] 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;69:683–94.Search in Google Scholar
[30] Pinho JC, Caldas FM, Mora MJ, Santana-Penín U. Electromyographic activity in patients with temporomandibular disorders. J Oral Rehabil 2000;27:985–90.Search in Google Scholar
[31] Liu ZJ, Yamagata K, Kasahara Y, Ito G. Electromyographic examination of jaw muscles in relation to symptoms and occlusion of patients with temporomandibular disorders. J Oral Rehabil 1999;26:33–47.Search in Google Scholar
[32] Glaros AG, Burton E. Parafunctional clenching, pain, and effort in temporomandibular disorders. J Behav Med 2004;27:91–100.Search in Google Scholar
[33] Glaros AG, Baharloo L, Glass EG. Effects of parafunctional clenching and estrogen on temporomandibular disorder pain. J Craniomandib Pract 1998;16:78–83.Search in Google Scholar
[34] Peck CC, Murray GM, Gerzina TM. How does pain affect jaw muscle activity? The Integrated Pain Adaption Model. Aust Dent J 2008;53:201–7.Search in Google Scholar
[35] Adel M, Book WJ, Eisenkraft JB. Adverse effects of nondepolarising neuromuscular blocking agents. Drug Saf 1994;10:420–38.Search in Google Scholar
[36] Vassend O, Knardahl S. Personality, affective responses, and facial blood flow during brief cognitive tasks. Int J Psychophysiol 2005;55:265–78.Search in Google Scholar
[37] Kemppainen P, Leppänen H, Jyväsjärvi E, Pertovaara A. Blood flow increases in the orofacial area of humans induced by painful stimulation. Brain Res Bull 1994;33:655–62.Search in Google Scholar
[38] Gatchel RJ, Turk DC. Psychosocial factors in pain. New York: Guilford Press; 1999.Search in Google Scholar
[39] Fillingim RB. Sex, gender, and pain. Seattle: IASP Press; 2000.Search in Google Scholar
[40] Stough C, Donaldson C, Scarlata B, Ciorciari J. Psychophysiological correlates of the NEO-PI-R openness, agreeableness and conscientiousness: preliminary results. Int J Psychophysiol 2001;41:87–91.Search in Google Scholar
© 2010 Scandinavian Association for the Study of Pain
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Articles in the same Issue
- Editorial comment
- Depression in people with pain: There is still work to do Commentary on ‘Understanding the link between depression and pain’
- Review
- Understanding the link between depression and pain
- Editorial comment
- Chronic postoperative pain and sensory changes: Two sides of the same coin?
- Original experimental
- Chronic postoperative pain and sensory changes following reduction mammaplasty
- Editorial comment
- Poor sleep and pain: Does spinal oxidative stress play a role?
- Original experimental
- Intrathecal administration of antioxidants attenuates mechanical pain hypersensitivity induced by REM sleep deprivation in the rat
- Editorial comment
- Temporomandibular disorders – A tough case to break!
- Original experimental
- Psychophysiological responses to pain stimulation and cognitive tasks in female temporomandibular disorder patients
- Editorial comment
- Dynamic mechanical allodynia: A homogeneous entity?
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- Dynamic mechanical allodynia in the secondary hyperalgesic area in the capsaicin model—Perceptually similar phenomena as in painful neuropathy?
