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Background: Stress is a risk factor for musculoskeletal pain. We wanted to explore stress related physiology in healthy subjects in order to gain insight into mechanisms of pain development which may relate to the pathophysiology of musculoskeletal pain disorders. Methods: Continuous blood pressure, heart rate, finger skin blood flow, respiration, surface electromyography together with perception of pain, fatigue and tension were recorded on 35 healthy women and 9 healthy men before, during a 60 minute period with task-related low-grade mental stress, and in the following 30 minute rest period. Results: Subjects responded physiologically to the stressful task with an increase in trapezius and frontalis muscle activity, increased blood pressure, respiration frequency and heart rate together with reduced finger skin blood flow. The blood pressure response and the finger skin blood flow response did not recover to baseline values during the 30-minute rest period, whereas respiration frequency, heart rate, and surface electromyography of the trapezius and frontalis muscles recovered to baseline within 10 minutes after the stressful task. Sixty-eight percent responded subjectively with pain development and 64% reported at least 30% increase in pain. Reduced recovery of the blood pressure was weakly correlated to fatigue development during stress, but was not correlated to pain or tension. Conclusion: Based on a lack of recovery of the blood pressure and the acral finger skin blood flow response to mental stress we conclude that these responses are more protracted than other physiological stress responses. and neck [1-4]. Different theoretical models for possible Background A substantial epidemiological literature has shown that causal links between stress and health complaints have mental and social stress is a risk factor for development of been described. Eriksen and Ursin  describe a process musculoskeletal pain, especially for pain in the shoulder of psychological sensitisation and arousal leading to Page 1 of 12 (page number not for citation purposes) BMC Musculoskeletal Disorders 2007, 8:81 http://www.biomedcentral.com/1471-2474/8/81 intolerable subjective complaints. McEwen and co-work- They were recruited from public institutions and private ers [6,7] describe a similar model with more emphasis on companies in Trondheim. Subjects were excluded if they physiological responses, introducing the concept of allo- fulfilled all of the three following criteria: (1) headache or static load (i.e., the physiological result of chronic expo- musculoskeletal pain for more than one day per month, sure to stress). The lack of physiological recovery after and (2) had visited a physician, and (3) took medication stress is considered by both groups a key factor linking for the complaint (all three conditions to be fulfilled). In stress and disease. Furthermore, laboratory studies indi- addition, subjects considering their headache or pain to cate that autonomic activation and dysfunction is impli- be more than "unpleasant" (i.e. a higher degree of pain) cated in chronic pain . In the search for possible were excluded if (1) they experienced the pain more than biological correlates for the link between stress and dis- one day per month, or (2) had visited a physician for the ease, earlier laboratory studies have used short lasting pain, or (3) took medication for the pain (i.e. any of the stressors with analytical focus on the physiological reac- three conditions fulfilled). No participants took drugs tivity (response to the stress), while the important physi- with a possible interaction with neural, vascular or mus- ological recovery period has received little attention . cular function (e.g. antiepileptics, β-blockers, and antide- Little is known about the physiology of the recovery pressants). period after stressful and repetitive work-related tasks. Procedure In order to explore further the physiological basis for the All subjects answered a questionnaire on biographical link between stress and muscle pain, which again may data (marital status, weight, medication, and stimulants), relate to chronic pain development, we performed this exercise habits, and the neuroticism index of the Eysenck study on healthy subjects performing a long-lasting stress- Personality Questionnaire (EPQ-N). The question- ful task (1 hour) with a 30 minute recovery period. We naire further included an index of symptoms concerning used a stressful task of sufficient duration to mimic real- the autonomic nervous system ("autonomic symptom world (e.g. work-related) stress, adding external validity to index"). For this purpose a subset of ten questions were the methodology . The stressful task has previously chosen (No. 26–35) from the Composite Autonomic been used to explore the development of subjective com- Symptom Profile . The questions assessed different plaints and muscular activity to stress in pain-free controls domains of autonomic symptoms (orthostatic, sudomo-  and in patient groups with musculoskeletal pain or tor, gastrointestinal, visual, vasomotor, reflex syncope). headache [12-15]. However, activity in the autonomic Sub-indexing different autonomic domains was not done nervous system was not assessed in the previous studies. due to the limited number of questions. The answers were In the present study we measured muscle activity (surface graded. A serious extent of a symptom was given a higher electromyography) together with blood pressure, heart value than a less serious. E.g. the answer to the questions: rate, acral finger skin blood flow and respiration fre- "In the last year, to what extent have you been in a cold quency 10 minutes before, during the 60 minute stressful sweat?", were graded as: "have not had" (value 0), mild task and 30 minutes after. Development of pain, fatigue (value 1), moderate (value 2), severe (value 3). The high- and tension was recorded immediately before and every est possible sum score was 30. 10 minutes during the stressful task and in the 30 minute rest period. All potential participants went through a short telephone interview to exclude those not fulfilling inclusion criteria. Firstly, we wanted to describe the autonomic and muscu- Subjects not excluded by the initial screening received the lar response and recovery profiles after low-grade mental questionnaire by post within two weeks of the test day. stress of long duration in healthy subjects. Secondly, we On the morning of the test day the subjects first went hypothesized that development of subjective complaints through a short interview controlling the answers from during a long lasting low-grade stressful task were related the questionnaire. Afterwards venous blood was sampled to the physiological response to the task. Lastly, we from the right cubital fossa. Subjects were instructed to hypothesized that those variables with the slowest recov- empty their bladder before starting the test. Brassieres ery profile would be related to the subjective complaints were removed and subjects wore only a light shirt on the induced by the stressful task. upper part of the body. The laboratory temperature was regulated to 24.5 ± 1.0°C and was recorded every ten min- Methods utes during the experiment. Subjects Forty-four healthy subjects participated in the study The subject was seated in an office chair with the lower (Table 1). The participants were recruited as controls for a arms resting on the table top before, during and after the group of pain patients with a female predominance, and test. Subjects got acquainted to the work-task by perform- therefore comprised thirty-five women and nine men. ing a mini-trial with instructions before the test started. Page 2 of 12 (page number not for citation purposes) BMC Musculoskeletal Disorders 2007, 8:81 http://www.biomedcentral.com/1471-2474/8/81 Table 1: Subject characteristics for the 44 participants Mean (SD) Range Age all (n = 44, years) 41 (12) 21–61 Age women (n = 35, years) 40 (12) 21–61 Age men (n = 9, years) 37 (12) 19–56 Weight (kg) 72 (14) 47–103 Height (cm) 168 (8) 145–190 Autonomic symptom index 5 (3) 1–13 EPQ-N 7 (4) 0–15 No. of subjects (%) Married/cohabitant (n) 31 (71%) Working (≥ 50%) (n) 38 (86%) Regular exercisers (≥ 1 session pr. week) (n) 14 (32%) Smokers (n) 12 (27%) Drinking alcohol ≥ 2 days pr. week * (n) 9 (20%) * One person drinking more than 3 days pr. week The mini-trial was performed without introducing stress- mal, fast, very fast) related to the subjects performance in imposing feedback on reaction time and was used to the mini-trial carried out before the experiment started. determine the subjects' habitual, non-stressed reaction Together with the feedback a new task was presented. time. Short maximal voluntary contractions were per- After the end of the stressful task, all measurements con- formed on each pair of muscles twice (frontalis muscle – tinued for thirty minutes. The test person was instructed raising eyebrows, temporalis – clenching teeth, neck – to sit still and relax during the rest period. Pain, perceived pushing head back against resistance, trapezius – pushing tension and fatigue was reported immediately before extended arms upwards against resistance at 45° angle out (baseline) and every ten minutes during and after the test from the body). The maximal contractions were carried by scoring on a 100 mm visual analogue scale (VAS) with out in order to normalize the muscle activity during test to the endpoints marked no pain/tension/fatigue and worst a percent of maximal force. However, the variability imaginable pain/tension/fatigue. The subjects were asked between the two maximal muscle contractions in the fron- to assess pain in locations corresponding to the electro- talis muscle was too large to make a reliable estimate of myography electrode positions; in the shoulders, neck, the maximal muscle force and thus none of the muscle temples and forehead on both sides. The subjects were not activity measurements were normalized. In order to meas- allowed to see previous records when scoring. ure the subjects habitual level of physiological activation, the laboratory experiment started with a five minute A second blood sample was drawn during 5 min immedi- period which served as a baseline period for the physio- ately after the test, before the 30 minute recovery period. logical variables. The subjects were alone in the room and Blood analysis was not a major aim of the study and these were not given any instructions other than to find a com- results are reported elsewhere (Nilsen et al., submitted). fortable position with their arms resting on the table in Physiological recordings front of them. To ensure that all subjects had the same low level of muscle activity before the test started a five minute Muscle activity was quantified by bilateral bipolar record- feedback period with muscle activity visualized on a ing of surface electromyography (SEMG) (electrode diam- screen followed. The subject experienced how it was pos- eter 6 mm, inter-electrode distance 20 mm). The system sible to influence the level of muscle activity by adopting noise level was less than 1.5 μV root mean square (RMS). different postures and thereafter concentrated on mini- The signals were bandpass-filtered (10–1250 Hz) and mising any muscle activity. The stressful task  was stored on a digitizing recorder (Earth Data 128). Data then performed: a two-choice reaction-time test on a were subsequently fed into an A/D converter (Powerlab monitor, lasting one hour. An open ("frame") and a solid 16S; ADInstruments Pty Ltd, Sydney, Australia; sampling ("brick") quadrangle were placed in a square pattern, and rate 2 kHz) for calculation of the RMS values (100 ms run- a written suggestion on how to move the brick to super- ning time window). Sharp transients and electrical activity impose on the frame was given. The subject responded by from the heart in the SEMG signals were removed with a pressing one of two keys ("correct" or "wrong") with the median filter (Matlab ver 6, The MathWorks inc.). right middle or index finger. The task was to be carried out as quickly and correctly as possible. The PC program pro- The following electrode sites were used: (1) Frontalis mus- vided feedback on whether an answer was correct or cle; both electrodes placed on a vertical line crossing the wrong, and on the response time (very slow, slow, nor- pupil, 10 mm and 30 mm above the upper border of the Page 3 of 12 (page number not for citation purposes) BMC Musculoskeletal Disorders 2007, 8:81 http://www.biomedcentral.com/1471-2474/8/81 eyebrow. (2) Temporal muscle; the lower electrode 10 ANOVA with repeated measurements was used for evalu- mm posterior to the lateral canthus of the orbit, and the ation of subgroup effects (sex, marital status, employment second electrode 20 mm above. (3) Splenius muscle; status, regular exercise, smokers, and alcohol drinking upper electrode 35 mm lateral to the spinous process of introduced sequentially one at a time as between-subject C2, and the second electrode 20 mm below. (4) Trapezius factors) with ten time intervals. For subgroup analysis of muscle; medial electrode 10 mm lateral to the midpoint the recovery period we calculated a recovery variable (the of a line connecting the acromion and the spinous process difference between the mean of the last 10 minutes of rest of C7, and the second electrode 20 mm lateral to the first (85–95 min) and the baseline period mean), a measure electrode. The ground electrode was placed on the considered to be more meaningful than the absolute level spinous process of C7. when comparing groups . Feedback data is displayed in figures, but feedback was not included in ANOVAs Activity in the autonomic nervous system was assessed by because we intended to study responses related to stress in measurements of continuous non-invasive finger blood this study. Recovery variables were analysed with one-way pressure (Portapres), measurements of skin blood ANOVA tests. flow with Laser-Doppler flowmetry (Moorlab, 4 channels, time constant 0.02 s, low-pass filter 22 kHz), and meas- For evaluation of the total response to the test we first per- urements of the respiration pattern with a thermistor formed repeated measures ANOVA tests (no between-sub- (Flaga, Embla S-AF-010) below the nose with active ele- jects factors, evaluating the within-subject effect of time) ments in each nostril and in front of the mouth. The with the same time intervals as in the subgroup analysis. blood pressure cuffs were mounted on the intermediate For further post-hoc exploration of the response and phalanx at the left middle and ring fingers. Finger skin recovery time-course we performed a series of paired-sam- blood flow was measured bilaterally with the electrodes ple tests (Student's t-tests for physiological variables (fibre separation 0.5 mm) placed on the volar side of the (Gauss-distributed) and Wilcoxon signed rank test for distal phalanx (pulp) of the thumb. Signals were sampled subjective variables (not Gauss-distributed)): We first at 200 Hz. evaluated the early response to the stressful task by com- paring the first part (0–10 min) of the stressful task to Respiration frequency was calculated by the Chart 4.2 baseline (immediately before the stressful task for the sub- software (ADInstruments Pty Ltd, Sydney, Australia). jective variables). Secondly, changes during the stressful Heart rate and blood pressure were calculated with the task (adaptation/summation effects) were investigated by Beatscope 1.0 software (TNO, Amsterdam, the Nether- a comparison of the first (0–10 min) and the last (50–60 lands). One blood pressure recording could not be ana- min) part of the stressful task. Thirdly, we evaluated the lyzed due to technical difficulties. recovery by comparing the change from the end of the stressful task (50–60 min) with the first part of the recov- Technical difficulties resulted in exclusion of seven sub- ery period (65–75 min) and the first (65–75 min) and last jects from analysis of respiration frequency and exclusion (85–95 min) part of the recovery period with baseline. of two subjects from analysis of heart rate and blood pres- sure responses. Physiological responses (the difference between the aver- age of the whole stressful task (0–60 min) and the average Analysis and statistics of the baseline period) and subjective responses to the Mean values for each 10-minute period were calculated stressful task (the difference between the maximal value for all physiological recordings. Muscular activity and fin- during the 60 minute stress period and the value reported ger blood flow values are reported as the average of the left immediately before starting the test) were calculated as and right side for each region because ANOVA repeated summary-variables for correlation analysis. Subjects with measures analysis (rANOVA) revealed no side differences a pain response larger than zero were defined as pain for the finger skin blood flow and muscle activity except responders. For each subject the location with the highest for the frontalis muscle SEMG (left side (10.9 μV) > right pain response during the task was identified (i.e. only one side (9.2 μV); F(43) = 8.0, p = 0.007). However, perform- location for each subject). The pain response in this loca- ing all subsequent tests separately for right and left fronta- tion (maximal pain location) was treated as a separate lis muscles did not give deviant results from those summary variable in the analysis (and it is the pain scores reported. Pain scores are reported from the side with the in this specific location we have displayed graphically). highest response (there were no side differences in neither pain level (side effect) nor pain development (side × time Possible associations between variables were investigated effect) for any of the four regions (rANOVA, Fs ≤ 3.2, p ≥ by correlating the muscular responses (trapezius, splen- 0.08). ius, temporalis, frontalis) with the autonomic responses (systolic and diastolic blood pressure, heart rate, respira- Page 4 of 12 (page number not for citation purposes) BMC Musculoskeletal Disorders 2007, 8:81 http://www.biomedcentral.com/1471-2474/8/81 tion frequency and finger skin blood flow), and by corre- Comparing the last ten minutes of the stressful task to the lating physiological responses (as above) with subjective first ten minutes of the stressful task (Table 2 and 3) responses (maximal pain, tension and fatigue), and revealed a fall in heart rate with 2.5 beats/min (p = 0.001) finally by correlating the subjective responses with each and a reduced respiration frequency with 0.89 breaths/ other (i.e. maximal pain, tension and fatigue). The corre- min (p = 0.04), indicating adaptation to the task for these lation coefficients between pain and muscular responses two variables only. However, in the same time interval were calculated separately for each localisation (i.e. left temporalis muscle activity increased with 0.82 μV (p = temple pain with left temporalis muscle activity). Further- 0.03) and finger skin blood flow showed a trend towards more, as post-hoc analysis we searched for possible corre- lower values (p = 0.09). The other physiological variables lations between blood pressure/finger skin blood flow were stable throughout the stressful task (p ≥ 0.33). recovery variables and physiological responses, subjective responses and other recovery variables. We used Pearson The heart rate response correlated with the trapezius mus- correlation (r ) for physiological variables (Gauss-distrib- cle response (r = 0.44, p = 0.004) and the temporalis p p uted) and Spearman's rank order correlation (r ) when muscle response (temporalis vs. heart rate, r = 0.41, p = s p subjective data were involved (not Gauss-distributed). 0.008). The other correlations in the SEMG vs autonomic response matrix were non-significant (p > 0.06). Because Mauchly's test of sphericity was significant in all ANOVA repeated measures tests with time as a within- Physiological recovery subject effect we used Huynh-Feldt correction of degrees Upon cessation of the stressful task, heart rate (p < 0.001), of freedom for these results. Two-tailed p-values less than respiration frequency (p < 0.001) and muscle activity in 0.05 were considered to be significant. Because the the trapezius (p < 0.003) and the frontalis (p < 0.002) hypotheses testing in this study involved several auto- decreased significantly (50–60 min vs. 65–75 min). Tra- nomic subsystems with insufficient a priori knowledge on pezius and frontalis SEMG recovered to the baseline level possible relation to pain, we did not correct for multiple (baseline vs. 65–75 min, p ≥ 0.10) while heart rate and comparisons. respiration frequency recovered to a level lower than base- line (baseline vs. 65–75 min, p ≤ 0.03). However, systolic Ethics and diastolic blood pressure, finger skin blood flow and For transport expenses and the inconvenience (total time muscle activity in the splenius and temporalis muscles did expenditure for each participant was 4 hours) participants not change significantly upon cessation of the stressful received NOK 500 (USD 75). The Regional Committee for task (50–60 min vs. 65–75 min and 50–60 min vs. 85–95 Medical Ethics approved the protocol, and all participants min, p > 0.10). The systolic and diastolic blood pressure gave written informed consent before volunteering. level remained elevated and finger skin blood flow was Experiments were performed according to the Helsinki reduced during the whole recovery period (baseline vs. Declaration. 85–95 min p ≤ 0.001). The finger skin blood flow recovery variable (Table 2) cor- Results All variables are listed in Table 2 with the results of the related negatively the systolic and diastolic blood pressure paired comparisons summarised in Table 3. recovery variables (r = -0.52, p = 0.001 and r = -0.40, p = p p 0.01 respectively). This means that a high blood pressure Physiological responses at the end of the recovery period was associated with a The development of all physiological variables is illus- small finger skin blood flow at the same time. The finger trated in Figure 1, 2 and 3. skin blood flow and blood pressure recovery variables did not correlate with other physiological (HR, muscle, respi- The stressful task induced a clear response evident in all ration) response or recovery variables (r ≤ 0.25, p ≥ 0.11). physiological variables (Table 2 and 3; baseline vs. 0–10 min, p ≤ 0.006) except for the splenius (p = 0.28) and Subjective responses and recovery temporalis muscle SEMG (p = 0.96). Development of tension, fatigue and pain scores in the maximal pain location is illustrated in Figure 4. Subjects Furthermore, age correlated negatively with the average reported increased tension (p = 0.02) and increased pain respiration frequency response (r = -0.44, p = 0.006) and in the temples (p = 0.03) and forehead (p = 0.01) already height correlated negatively with the average systolic ten minutes into the stressful task (0 min vs. 10 min), blood pressure response (r = -0.41, p = 0.008). None of while fatigue (p = 0.52) and pain in the shoulder and neck the other physiological responses (Table 2) correlated (p > 0.52) did not increase during the first ten minutes with age, height or weight. (Table 2 and 3). All subjective variables increased further during the stressful task (10 min vs. 60 min; p < 0.008 Page 5 of 12 (page number not for citation purposes) BMC Musculoskeletal Disorders 2007, 8:81 http://www.biomedcentral.com/1471-2474/8/81 Table 2: Mean values and the average responses for all variables Baseline During the stressful task Response* Variable Mean (SD) 0–10 min Mean 10–20 min 20–30 min 30–40 min 40–50 min 50–60 min Mean (SD) (SD) Mean (SD) Mean (SD) Mean (SD) Mean (SD) Mean (SD) Surface electromyography Trapezius (μV) 6.2 (6.2) 11.8 (13.7) 12.0 (12.8) 11.6 (13.8) 10.5 (11.3) 11.2 (12.4) 10.7 (11.8) 5.1 (11.4) Splenius (μV) 5.3 (3.2) 4.7 (2.7) 4.6 (2.3) 4.6 (2.6) 4.5 (3.0) 4.6 (3.5) 4.6 (3.1) -0.7 (3.1) Temporalis (μV) 6.5 (3.2) 6.4 (4.7) 7.0 (6.1) 6.6 (5.6) 7.1 (5.2) 7.3 (5.5) 7.2 (5.1) 0.5 (5.4) Frontalis (μV) 8.0 (5.9) 11.1 (5.8) 11.1 (6.1) 11.0 (6.6) 11.3 (6.4) 11.1 (6.5) 11.4 (6.5) 3.2 (4.8) Systolic BP (mmHg) 112 (16) 126 (17) 122 (16) 122 (15) 123 (15) 123 (15) 125 (15) 11.4 (7.8) Diastolic BP (mmHg) 62 (11) 72 (13) 69 (13) 69 (11) 71 (12) 70 (11) 71 (10) 8.6 (5.0) Heart rate (beats/min) 71 (8) 75 (10) 74 (9) 73 (9) 72 (9) 72 (9) 72 (8) 2.3 (4.3) Respiration (breaths/min) 15 (3) 17 (3) 17 (3) 16 (3) 16 (3) 16 (3) 16 (3) 1.5 (2.5) Skin blood flow (au) 279 (112) 248 (122) 251 (130) 246 (127) 249 (126) 237 (127) 229 (120) -35.3 (56.7) Pain (VAS 0–100 mm) 10 min 20 min 30 min 40 min 50 min 60 min Maximal location (mm) 2.4 (6.1) 3.0 (5.3) 3.6 (5.8) 6.7 (11.1) 9.0 (14.4) 11.9 (15.5) 14.0 (17.1) 15.4 (18.0) Shoulder (mm) 2.8 (6.3) 2.4 (5.6) 4.5 (7.0) 5.4 (8.8) 6.5 (12.4) 8.7 (13.3) 10.3 (14.4) 12.9 (16.1) Neck (mm) 2.4 (5.1) 3.1 (5.6) 3.5 (6.4) 5.0 (9.1) 6.4 (8.2) 8.6 (12.2) 9.8 (11.9) 11.5 (13.7) Temples (mm) 1.0 (2.2) 2.3 (5.2) 1.9 (4.1) 3.7 (8.2) 4.2 (9.1) 5.6 (10.8) 5.5 (11.7) 7.5 (13.7) Forehead (mm) 1.1 (2.5) 1.6 (3.3) 2.5 (6.0) 3.8 (8.8) 4.2 (9.1) 4.7 (9.5) 5.3 (11.1) 6.3 (12.0) Fatigue (VAS 0–100 mm) 8.9 (15.3) 7.7 (13.5) 10.8 (14.6) 19.0 (20.5) 22.2 (21.2) 29.8 (22.5) 33.1 (25.4) 27.2 (23.1) Tension (VAS 0–100 mm) 7.0 (12.4) 11.2 (13.2) 12.9 (14.0) 18.0 (19.1) 19.4 (20.2) 21.7 (20.6) 25.3 (23.1) 21.2 (21.2) Recovery period Recovery § Variable 65–75 min 75–85 min 85–95 min Surface electromyography Trapezius (μV) 5.4 (4.7) 5.6 (4.5) 6.2 (6.4) 0.14 (7.7) Splenius (μV) 4.7 (2.7) 4.9 (3.0) 4.9 (3.4) -0.33 (3.6) Temporalis (μV) 7.7 (4.9) 7.4 (5.3) 7.1 (4.2) 0.68 (3.8) Frontalis (μV) 9.0 (6.9) 8.2 (5.5) 8.3 (5.1) 0.26 (3.9) Systolic BP (mmHg) 123 (15) 122 (14) 124 (14) 12.1 (11.7) Diastolic BP (mmHg) 71 (10) 69 (9) 71 (10) 9.5 (6.6) Heart rate (beats/min) 69 (7) 69 (8) 69 (8) -1.9 (3.8) Respiration (breaths/min) 14 (2) 14 (2) 14 (3) -0.68 (2.7) Skin blood flow (au) 215 (105) 229 (111) 211 (106) -67.5 (89.1) Pain (VAS 0–100 mm) 75 min 85 min 95 min Maximal location (mm) 6.9 (15.2) 7.6 (14.9) 5.8 (13.5) 3.3 (11.4) Shoulder (mm) 6.2 (15.0) 6.2 (14.9) 5.3 (13.7) 2.5 (11.4) Neck (mm) 5.5 (11.0) 6.1 (12.5) 5.5 (11.5) 3.0 (10.1) Temples (mm) 1.9 (5.9) 1.7 (4.5) 1.7 (5.2) 0.67 (4.7) Forehead (mm) 2.2 (6.1) 1.8 (4.5) 1.8 (5.1) 0.63 (4.6) Fatigue (VAS 0–100 mm) 17.2 (20.2) 17.5 (21.8) 15.0 (20.2) 6.7 (19.3) Tension (VAS 0–100 mm) 8.2 (16.0) 8.1 (16.5) 4.8 (12.0) -1.4 (12.0) au: arbitrary units. BP: blood pressure * Response = Average during stressful task (0–60 min) – baseline for the physiological variables, and maximal during stressful task (0–60 min) – baseline for the subjective variables. §Recovery = The last ten minutes of the recovery period (85–95 min) – baseline (summary statistics used in correlation analysis). except for a trend in temple pain (p = 0.06)), and were sig- than 30 mm during the test (Table 4). The pain response nificantly reduced ten minutes into the recovery period was most evident in the neck and/or shoulder (Table 4). (60 min vs. 75 min, p < 0.008). However, fatigue and pain in neck (and maximal pain) did not recover to baseline (0 Pain responses did not correlate with tension and fatigue min vs. 95 min; p < 0.04). Pain in the shoulders showed a responses (r ≤ 0.19, p ≥ 0.20), however, fatigue and ten- trend towards non-recovery ten minutes into the recovery sion responses were correlated (r = 0.48, p = 0.001). period (p = 0.08) but recovered to baseline after 30 min- utes (p = 0.20), while tension and pain in temples and Pain, tension and fatigue responses did not correlate sig- forehead returned to baseline ten minutes into the recov- nificantly with physiological responses (r ≤ 0.28, p ≥ ery period (p > 0.48). 0.071, correlation coefficients between pain and muscular responses were calculated separately for each localisa- Thirty subjects (68.2%) reported an increase in pain in at tion). However, the fatigue response correlated with systo- least one location during the test and twenty-eight sub- lic (r = 0.34, p = 0.03, Figure 5) and diastolic blood jects (63.6%) had an increase in pain VAS score of more pressure recovery (r = 0.31, p = 0.047) indicating a larger Page 6 of 12 (page number not for citation purposes) BMC Musculoskeletal Disorders 2007, 8:81 http://www.biomedcentral.com/1471-2474/8/81 Table 3: Test statistics for evaluation of the response and recovery to the stressful task Variable rANOVA* Baseline vs. 0–10 min 0–10 vs. 50–60 min 50–60 vs. 65–75 min Surface electromyography Trapezius (μV) F(2.5,105.6) = 7.3, p < 0.001 t(43) = -2.9, p = 0.006 t(43) = 1.0, p = 0.33 t(43) = 3.1, p = 0.003 Splenius (μV) F(3.3,144.0) = 0.96, p = 0.42 t(43) = 1.1, p = 0.28 t(43) = 0.5, p = 0.62 t(43) = -0.2, p = 0.80 Temporalis (μV) F(2.7,117.8) = 1.2, p = 0.31 t(43) = 0.0, p = 0.96 t(43) = -2.3, p = 0.03 t(43) = -0.9, p = 0.39 Frontalis (μV) F(3.2,138.2) = 11.3, p < 0.001 t43) = -3.8, p < 0.001 t(43) = -0.4, p = 0.69 t(43) = 3.3, p = 0.002 Systolic blood pressure (mmHg) F(2.8,14.3) = 11.4, p < 0.001 t(40) = -7.0, p < 0.001 t(40) = 0.3, p = 0.78 t(41) = 1.5, p = 0.15 Diastolic blood pressure (mmHg) F(3.0,118.2) = 17.4, p < 0.001 t(40) = -7.6, p < 0.001 t(40) = 0.4, p = 0.66 t(41) = 0.1, p = 0.96 Heart rate (beats/min) F(2.6,103.2) = 24.1, p < 0.001 t(40) = -4.5, p < 0.001 t(42) = 3.7, p = 0.001 t(42) = 8.1, p < 0.001 Respiration (breaths/min) F(4.3,155.2) = 21.7, p < 0.001 t(36) = -4.6, p < 0.001 t(36) = 2.1, p = 0.04 t(36) = 6.1, p < 0.001 Finger skin blood flow (au) F(2.6,113.2) = 6.2, p < 0.001 t(43) = 3.6, p = 0.001 t(43) = 1.8, p = 0.09 t(43) = 1.6, p = 0.12 Pain (VAS 0–100 mm) Maximal location (mm) F(3.2,139.4) = 7.8, p < 0.001 Z = -1.4, p = 0.17 Z = -4.6, p < 0.001 Z = -4.0, p < 0.001 Shoulder (mm) F(2.7,112.5) = 3.8, p = 0.02 Z = -0.3, p = 0.75 Z = -4.3, p < 0.001 Z = -3.5, p < 0.001 Neck (mm) F(2.4,98.9) = 4.5, p = 0.01 Z = -0.6, p = 0.52 Z = -4.3, p < 0.001 Z = -3.2, p = 0.001 Temples (mm) F(2.0,86.5) = 4.1, p = 0.02 Z = -2.2, p = 0.03 Z = -1.9, p = 0.06 Z = -2.7, p = 0.006 Forehead (mm) F(2.1,89.5) = 4.0, p = 0.02 Z = -2.5, p = 0.01 Z = -2.7, p = 0.008 Z = -2.7, p = 0.008 Fatigue (VAS 0–100 mm) F(3.2,129.0) = 17.0, p < 0.001 Z = -0.6, p = 0.52 Z = -5.2, p < 0.001 Z = -4.4, p < 0.001 Tension (VAS 0–100 mm) F(2.6,104.7) = 16.1, p < 0.001 Z = -2.4, p = 0.02 Z = -4.5, p < 0.001 Z = -4.9, p < 0.001 50–60 vs. 85–95 min Baseline vs. 65–75 min Baseline vs. 85–95 min Surface electromyography Trapezius (μV) t(43) = 2.8, p = 0.008 t(43) = 0.9, p = 0.40 t(43) = -0.12, p = 0.99 Splenius (μV) t(43) = -7.1, p = 0.48 t(43) = 1.4, p = 0.16 t(43) = 0.65, p = 0.54 Temporalis (μV) t(43) = 0.2, p = 0.83 t(43) = -2.0, p = 0.05 t(43) = -1.2, p = 0.24 Frontalis (μV) t(43) = 4.5, p < 0.001 t(43) = -1.7, p = 0.10 t(43) = -0.44, p = 0.67 Systolic blood pressure (mmHg) t(41) = 0.54, p = 0.60 t(40) = -7.1, p < 0.001 t(40) = -6.5, p < 0.001 Diastolic blood pressure (mmHg) t(41) = -0.4, p = 0.69 t(40) = -9.5, p < 0.001 t(40) = -9.2, p < 0.001 Heart rate (beats/min) t(42) = 7.0, p < 0.001 t(40) = 3.1, p = 0.004 t(40) = 3.2, p = 0.003 Respiration (breaths/min) t(36) = 5.6, p < 0.001 t(36) = 2.2, p = 0.03 t(36) = 1.5, p = 0.14 Finger skin blood flow (au) t(43) = 1.7, p = 0.10 t(43) = 5.4, p < 0.001 t(43) = 5.0, p < 0.001 Pain (VAS 0–100 mm) 60 vs. 95 min 0 vs. 75 min 0 vs. 95 min Maximal location (mm) Z = -4.0, p < 0.001 Z = -2.5, p = 0.01 Z = -2.4, p = 0.015 Shoulder (mm) Z = -3.5, p < 0.001 Z = -1.7, p = 0.08 Z = -1.3, p = 0.20 Neck (mm) Z = -2.7, p = 0.007 Z = -2.1, p = 0.04 Z = -2.2, p = 0.03 Temples (mm) Z = -2.7, p = 0.007 Z = -0.4, p = 0.72 Z = -0.51, p = 0.61 Forehead (mm) Z = -2.7, p = 0.007 Z = -0.7, p = 0.48 Z = -0.40, p = 0.69 Fatigue (VAS 0–100 mm) Z = -4.4, p < 0.001 Z = -3.2, p = 0.001 Z = -2.6, p = 0.009 Tension (VAS 0–100 mm) Z = -4.8, p < 0.001 Z = -0.3, p = 0.78 Z = -1.5, p = 0.13 au: arbitrary units. BP: blood pressure * ANOVA repeated measures (no between-subjects factors, time effect) with ten time intervals (baseline, 0–10, .., 85–95 min) and Huynh-Feldt corrected degrees of freedom. All other statistics are paired statistics (Student's paired t-tests for physiological variables and Wilcoxon paired statistics for subjective variables used in explorative contrast analysis). fatigue response during the stressful task for those subjects Subgroup analyses who recovered less during the rest period. However, no Subgroup analyses with the dichotomized variables in significant correlations were found between the blood Table 1 (sex, marital status, employment status, regular pressure recovery and the pain and tension response vari- exercisers, smokers, and alcohol drinking) revealed that ables (r ≤ 0.16, p ≥ 0.31) and finger skin blood flow women had lower respiratory frequency (15.2 vs. 17.1 recovery was not correlated to subjective responses (r ≤ breaths/min, rANOVA; sex effect F(1,35) = 4.5, p = 0.04) 0.16, p ≥ 0.29). and higher frontalis SEMG (11.1 vs. 6.1 μV, rANOVA; sex effect F(1,42) = 6.7, p = 0.01). Moreover, smokers had Except for a correlation between the autonomic symptom higher blood systolic blood pressure level (130 mmHg vs. index (Table 1) and the blood pressure response (Table 2, 120 mmHg, rANOVA; smoking effect F (1,36) = 4.7, p = r = 0.38, p = 0.014), the physiological responses were not 0.04) and we found a time × marital status interaction for correlated to the Nevroticism index or the "autonomic maximal pain (rANOVA; F(3.0,141.2) = 2.6, p = 0.048) symptom index". The Nevroticism index (EPQ-N, Table with higher maximal pain response for those living alone 1) correlated with pain and fatigue responses (r ≥ 0.36, p compared to cohabitants (17.7 vs 14.5 mm VAS). Sub- ≤ 0.016). group analysis of the recovery variables did however not reveal any differences (One-way ANOVA Fs ≤ 2.9, p ≥ 0.097). It must be noted that some subgroups had few Page 7 of 12 (page number not for citation purposes) Heart Rate (beats/min) Blood pressure (mmHg) BMC Musculoskeletal Disorders 2007, 8:81 http://www.biomedcentral.com/1471-2474/8/81 Systolic blood pressure Trapezius Diastolic blood pressure Splenius 325 130 Finger skin blood flow Temporalis Frontalis Time (minutes) Time (minutes) Mea (Baseline, Feedback), during after Figure 2 n (65– blood pressur 75, 75–85, 85–95 e and finmin) the str g (0–10, 10– er skin blood flow 20, .., 50 essful task –60 min) a (SBF) befor nd e lin (65–75, 75– Figure 1 Surface electromyograph e, Feedback), dur 85, 85–95 min) th ing (0–10, ic (SEM e stressfu 10– G) activitity 20, .., 50– l task 60 min) an before (Base- d after Mean blood pressure and finger skin blood flow (SBF) before Surface electromyographic (SEMG) activitity before (Base- (Baseline, Feedback), during (0–10, 10–20, .., 50–60 min) and line, Feedback), during (0–10, 10–20, .., 50–60 min) and after after (65–75, 75–85, 85–95 min) the stressful task. Mean val- (65–75, 75–85, 85–95 min) the stressful task. Mean RMS val- ues for periods of 10 minutes (Baseline, Feedback: 5 min) are ues for periods of 10 minutes (Baseline, Feedback: 5 min) are shown. Au = arbitrary units. shown. cases (Table 1), and were not ideal for subgroup effect the first ten minutes of the stressful task and stayed ele- analysis. vated both during and after the stressful task. Discussion Slow recovery of blood pressure following experimental Major findings in the present study on stress responses in stress has previously been reported by Steptoe and co- healthy subjects can be summarized as: 1) A significant proportion of healthy subjects (64%) respond with a pain increase of more than 30 mm (VAS 0–100) in at least one 18 Respiration frequency 76 Heart rate of the four muscle groups investigated. 2) Pain develops gradually as a response to a stressful task. 3) The trapezius and frontalis muscles are activated in response to the task with fast recovery after a stressful task. 4) The HR-response habituates gradually during a long-lasting stressful task and recovers fully afterwards. 5) There is a lack of skin blood flow and blood pressure recovery after a stressful task of long duration. 6) Physiological responses (and recovery) are not correlated with pain responses, but 7) lack of blood pressure recovery is correlated to the fatigue 14 response to the preceding stressful task. The most important finding is that blood pressure and fin- ger skin blood flow did not recover to baseline during the Time (minutes) 30-min rest period, contrasting the recovery pattern of the other autonomic and muscular responses. The finger skin Respiration back), during (0–10, 10–20, .. 75–85, 85–9 Figure 3 frequency a 5 min) the stressful task nd heart , 50–60 rate bef min) and after (65–75, ore (Baseline, Feed- blood flow apparently had biphasic response pattern with Respiration frequency and heart rate before (Baseline, Feed- a fast reduction during the first ten minutes of the stressful back), during (0–10, 10–20, .., 50–60 min) and after (65–75, task and a further monotonic reduction (trend) during the 75–85, 85–95 min) the stressful task. Mean values for periods of 10 minutes (Baseline, Feedback: 5 min) are shown. stressful task, while the blood pressure increased during Page 8 of 12 (page number not for citation purposes) Baseline Feedback 0-10 10-20 20-30 30-40 40-50 50-60 65-75 75-85 85-95 Baseline Feedback 0-10 10-20 20-30 30-40 40-50 50-60 65-75 75-85 85-95 Baseline Feedback 0-10 10-20 20-30 30-40 40-50 50-60 65-75 75-85 85-95 SEMG (µV) Respiration frequency (breaths/min) Finger skin blood flow (a.u.) BMC Musculoskeletal Disorders 2007, 8:81 http://www.biomedcentral.com/1471-2474/8/81 complaints emphasize lack of recovery after stress as an important factor for development of subjective com- plaints [5-7]. According to these models, a person with a Pain Fatigue reduced ability to recover after stress is more prone to Tension develop subjective complaints. However, as the present study illustrates, when re-examining these theoretical models in the laboratory one may have to register physio- logical variables over longer recovery periods than we have done in our study to be able do detect possible dif- ferences in physiological recovery between patients and healthy controls. A long-lasting, presumably sympathetically mediated 4 vasoconstriction is evident in the present study. Environ- mental temperature was monitored throughout the exper- iment and was stable and not related to skin blood flow (data not shown). The slightly different time course of Time (minutes) blood pressure and the finger skin blood flow response Tension, b m Figure 4 eifor n) the stressful task e (0 min), during (1 fatigue and pain scores in 0, 20, .., 60 min) the maximal and after pa (75, 85, 95 in location indicate differential control of vascular beds. This is inter- Tension, fatigue and pain scores in the maximal pain location preted as an example of the specificity of different neuro- before (0 min), during (10, 20, .., 60 min) and after (75, 85, 95 anatomical circuits within the autonomic nervous system min) the stressful task.  and corresponding differentiation of sympathetic responses with respect to target organ and response local- isation within the vascular system [23-25]. workers [20,21]. They applied the colour-word test and mirror tracing for a total stress period of 10 min, causing Although the reduction of finger skin blood flow was not a stress response marginally higher than in the present related to subjective complaints in the present study, it is series, judged by the increase in heart rate (Δheart rate ~7 potentially relevant that some patients with musculoskel- vs. 5 bpm) and blood pressure (Δblood pressure ~14 vs. etal complaints report a cold feeling in wrist/hand 11 mmHg). In their study blood pressure had partially [26,27]. A recent study, using infrared thermography to recovered 20–25 min after the test (female subjects) while measure dorsal hand skin temperature, showed that post- in the present study no recovery was observed after 30 exercise hyperaemia was blunted in patients with chronic min. Assuming a similar level of stress in the two series, upper extremity pain who reported cold hands induced by the slower time course of blood pressure recovery in the keyboard use . present study can be due to the longer duration of the stress period. A previous study on pain-free subjects using a similar pro- tocol, but without measurements of blood pressure, heart The present study of healthy controls shows that slow vas- rate and respiration frequency, found a correlation cular recovery after mental stress is a normal phenome- between pain development and muscle activity in the non and is not related to simultaneous pain development. right trapezius muscle (r = 0.37, p < 0.03) during the The theoretical models linking stress and subjective health stressful task . In the present study we found no corre- Table 4: Subjective responses categorized in three groups VAS = 0 VAS 1–30 VAS > 30 Pain: Shoulders (n (%)) 17 (38.6%) 3 (6.8%) 24 (54.5%) Neck (n (%)) 19 (43.2%) 1 (2.3%) 24 (54.5%) Temples (n (%)) 27 (61.4%) 5 (11.4%) 12 (27.3%) Forehead (n (%)) 24 (54.5%) 8 (18.2%) 12 (27.3%) Maximal pain location 14 (31.8%)* 2 (4.5%) 28 (63.6%) Fatigue (n (%)) 5 (11.6%) 1 (2.3%) 37 (86.0%) Tension (n (%)) 4 (9.5%) 3 (7.1%) 35 (83.3%) a b Pain response = (maximal pain during test – pain before test), Maximal pain response irrespective of location,* = No pain development in any location. Page 9 of 12 (page number not for citation purposes) VAS (0-100) mm BMC Musculoskeletal Disorders 2007, 8:81 http://www.biomedcentral.com/1471-2474/8/81 per minute (bpm) on average, and 5 bpm the first 10 min. Other studies of stress responses have exposed subjects to stress for a shorter period of time and report elevated heart rate responses of 10–20 bpm indicating a higher level of stress [29-31]. The pain reported in the present study is indeed low-level and not directly comparable to labora- tory studies of acute pain. The level of tension and fatigue was considerably higher than the pain level in the present study. However, the levels of pain, tension and fatigue obtained in this laboratory study corresponds well with the values obtained from healthy subjects in field studies of workers in stressful work situations with low biome- chanical load [32,33]. Therefore, we believe that the level of subjective complaints reported in this laboratory study is comparable to the subjective complaints healthy sub- jects experience during stressful and repetitive office work, although laboratory experiments never can substitute real-life experiments. Extending the duration of the stress B agains Figure 5 lood pressure recovery (va t the fatigue response wi lue th at 95 linear regres min – basi seline) plotted on line shown exposure (as we have done in the present study) has been Blood pressure recovery (value at 95 min – baseline) plotted suggested as one way to increase the external validity of against the fatigue response with linear regression line shown. The association is significant (r = 0.34, p = 0.03). studies on cardiovascular responses to stress . The subject's perception of the stressor was not considered lation between pain response and muscle activity. Because in terms of stress level in the present study, but evaluated the protocols were so similar and the study group were using the term "tension". Holte et al.  investigated the larger in the present study (44 subjects in the present concept of tension in Norwegian subjects with question- study, 36 subjects in the previous study), we believe the naires and qualitative interviews and found that subjects different finding in the present study indicate that the ear- described tension in terms of both stress-related auto- lier reported correlation may have been a chance finding. nomic symptoms and musculoskeletal activation (the In the previous study increased muscular activity during Norwegian word for tension ("anspenthet") conveys the stressful task was found for the frontalis muscle and almost the same meaning as the word stress). Further- for the trapezius muscles (significant for the frontalis and more, different perception of the stressor may partly a trend for the trapezius muscles), whereas no response to explain the large inter-subject variation in physiological the stressful task was found for the splenius and tempora- responses [35,36]. Moreover, the lack of association lis muscles. The present study confirms the earlier findings between pain and tension responses may indicate that the of the frontalis and trapezius muscles as more responsive pain is linked to physiological factors and not to cognitive to a stressful task than the splenius and temporalis mus- factors alone. cles. The feedback period was necessary in order to ensure that In the present study most cardiovascular vs. EMG correla- all subjects had the same low level of muscle activity tions were not significant. However, we found correla- before the stressful task. The feedback was given solely on tions between the heart rate response and trapezius and muscular activity. The feedback was introduced after the temporalis muscle responses. The correlations were strong baseline period in order to get a true baseline period with- (p < 0.005), and we cannot exclude that it is relevant. The out influence from the feedback procedure. It is possible electrical activity from the heart was filtered out of the that the feedback procedure influenced the measured electromyographic signals, and a correlation with heart muscle activity during the stressful task by teaching the rate was not observed for the splenius muscles, hence it is subjects how to relax their muscles. However, this effect probably not related to an ECG-artefact. Increased muscu- was supposedly similar for all subjects. Furthermore, sub- lar activity in a rather large muscle like trapezius is reason- jects did not receive any feedback on the measured varia- ably paralleled by increased HR if the increased muscular bles during the stressful task. activity demands a higher cardiac output to satisfy the metabolic needs. In the correlation analysis we have used summary varia- bles in order to minimize the number of calculated corre- The low-grade stress response in the present experiments lations. While the subjective variables were steadily is shown by the heart rate only being elevated by 4 beats increasing through the task, most physiological responses Page 10 of 12 (page number not for citation purposes) BMC Musculoskeletal Disorders 2007, 8:81 http://www.biomedcentral.com/1471-2474/8/81 were more stable (although not without exceptions). The Conclusion physiological variables were measured continuously and In the present study of healthy subjects exposed to mental we did not want to place emphasis on any (possible ran- stress in 60 minutes the blood pressure and acral finger dom) peak value. Instead, the average value was consid- skin blood flow response did not recover to baseline even ered a summary variable reflecting the total physiological after 30 minutes rest. This was in clear contrast to other "burden" of the stressful task. However, the average pain physiological stress response variables (heart rate, respira- score will in our opinion not reflect the subjective "bur- tion frequency and muscle activity) which recovered to den" of the stressful task. An average pain score would baseline values early in the rest period. The protracted underestimate the pain-inducing effect of the stressful task blood pressure response was correlated to fatigue devel- in case the subject's pain pathways would have been sen- opment, but not to pain development, possibly implicat- sitised in any way, thus potentially neglecting the effect of ing psychological mechanisms. However, because of the any temporal summation of pain. We have chosen to use large number of correlations performed in the present the maximal value during the task as an approximation of study, one must keep in mind that this correlation may be this "burden", and this is in line with others [37-39]. a chance finding. The results imply that a long recovery period is necessary when the physiological recovery to Our subgroup analysis did not reveal any differences mental stress is studied. Moreover, a thorough exploration between groups regarding the recovery variables, and the of different aspects of the subjective complaints that present study thus confirms the findings of Steptoe  develops during and after low-grade stress of long dura- who reported no relationship between prolonged cardio- tion is needed. Examplewise, a valid and reliable way to vascular stress responses and sedentary lifestyle. We have distinguish between mild fatigue and unpleasantness in not found any other studies related to our findings of contrast to pain should be established in later studies of lower respiration frequency and higher frontalis muscle the relation between stress and development of subjective activity in women. Considering that smoking is well- complaints. Furthermore, the duration of stress period known risk factor for cardiovascular disease  our find- may be of importance and should be addressed in future ing of increased blood pressure among smokers is not sur- studies of physiological recovery after mental stress. prising. The higher pain response found for those living Finally, further studies should in a prospective design alone is very difficult to explain and we are not aware of investigate whether healthy subjects with a slow vascular any other study who has investigated this. However, as recovery after mental stress is at risk for developing already noted, subgroup sizes were partly asymmetric and chronic stress-related disorders later in life. not optimally sensitive for subgroup factor effect analysis. Competing interests We are not aware of other studies investigating the rela- The authors declare that they have no competing interests. tion between development of fatigue during stress and degree of physiological recovery and thus our finding of a Authors' contributions correlation between lack of blood pressure recovery and KBN participated in study design, in collecting the data, fatigue development during stress should be further inves- carried out the analysis and drafted the manuscript. TS tigated. It must be emphasized that the correlation was participated in the design, advised and assisted in the sta weak and may be a chance finding because of the large number of correlations performed. Nevertheless, the cor- tistical analysis and in the progress and drafting of the relation may indicate that psychological mechanisms are manuscript. LJS participated in the study design and in the important when considering the mechanisms for the pro- progress of the manuscript. RBL participated in the statis- tracted vascular response. Moreover, the correlation tical analysis and in the progress of the manuscript. RHW between the blood pressure and finger skin blood flow participated in the design, and in the progress and drafting recovery variables may point to a common mechanism of the manuscript. All authors read and approved the final responsible for the lack of recovery in these two variables. manuscript Steptoe (2003) proposed sustained changes in centrally Acknowledgements This work has been supported by the Norwegian Research Council. We mediated neurogenic vasoconstriction, or disturbance of are grateful to Grethe Helde for her invaluable technical assistance. nitric-oxide-dependent endothelial function, as explana- tions for lack of recovery of blood pressure after mental References stress . However, theories for mechanisms underlying 1. 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