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The influence of repetitive painful stimulation on peripheral and trigeminal pain thresholds
Journal of the Neurological Sciences 273 (2008) 108–111
Contents lists available at ScienceDirect
Journal of the Neurological Sciences j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / j n s
The influence of repetitive painful stimulation on peripheral and trigeminal pain thresholds Monika Dirkwinkel a, Ingrid Gralow b, Reyhan Colak-Ekici c, Anne Wolowski c, Martin Marziniak a, Stefan Evers a,⁎ a b c
Department of Neurology, University of Münster, Germany Department of Anaesthesiology, University of Münster, Germany Department of Dental Prosthetics, University of Münster, Germany
A R T I C L E
I N F O
Article history: Received 29 March 2008 Received in revised form 16 June 2008 Accepted 2 July 2008 Available online 8 August 2008 Keywords: Pain threshold Martial arts Kung Fu Facilitation Habituation Trigeminal Peripheral Hypalgesia
A B S T R A C T We were interested in how continuous painful stimulation which is performed as inurement exercises in some Asian martial arts influences sensory and pain perception. Therefore, we examined 15 Kung Fu disciples before and after a 14 day period with repetitive inurement exercises and measured sensory and pain thresholds and intensities in both the trigeminal and the peripheral (peroneal nerve) region. The results of the probands were compared to those of 15 healthy control subjects who were performing sports without painful stimulation during this period. The probands showed a significantly decreased trigeminal pain intensity after repetitive electrical stimulation whereas the control subjects did not show any changes of sensory or pain perception during the study period. This suggests a change of central sensitisation and inhibitory control mechanisms in the nociceptive spinal or cerebral pathways by inurement exercises. In addition, pain thresholds showed an (not significant) increase after the study period whereas the control subjects showed a significant decrease of pain thresholds. In summary, our pilot study suggests that inurement exercises, i.e. repetitive painful stimulation, over a period of 14 days might induce changes of pain perception resulting in trigeminal pain habituation and higher pain thresholds. © 2008 Elsevier B.V. All rights reserved.
1. Introduction In the last years, one of the main topics in trigeminal pain research was how pain facilitation and pain inhibition can influence each other and how one can measure these phenomena [1]. We were interested in how repetitive exogenous painful stimulation can influence trigeminal and peripheral pain thresholds and pain perception. Some Asian martial arts use repetitive painful exercises to subsequently decrease subjective pain perception. Especially in the traditional Chinese Shaolin Kung Fu, inurement exercises are exactly defined. The aim of these exercises is that the body of the martial arts disciple should be habituated to pain in order to be prepared for the fighting situation. The inurement exercises of the Mantis Kung Fu style can serve as a model to explore the impact of exogenous repetitive painful stimulation. In this study, we therefore examined if this training of exogenously induced pain with the aim of subjective hypalgesia is leading to changes of peripheral and trigeminal pain thresholds and, thus, can change pain facilitation and pain inhibition. Because of the anatomical differences of the peripheral and trigeminal nociceptive systems we ⁎ Corresponding author. Department of Neurology, University of Münster, AlbertSchweitzer-Str. 33, 48129 Münster, Germany. Fax: +49 251 8348181. E-mail address: [email protected] (S. Evers). 0022-510X/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.jns.2008.07.002
studied them separately. We chose the anterior tibial muscle region which is supplied by the peroneal nerve as a model for the peripheral nervous system and the masseter muscle region supplied by the trigeminal nerve as a model for the trigeminal system. 2. Methods 2.1. Subjects We included 30 healthy male and female subjects. Exclusion criteria were the presence of neurological or psychiatric diseases as well as regular intake of analgesics or other medication. The female subjects were not allowed to use oral contraceptives to avoid influence of this medication on pain perception. The age range of the subjects was between 18 and 40 years. They were excluded from participation in further pain studies. We only included right-handed subjects. All subjects gave informed consent to participate in the study. The study was approved by the Ethics Committee of the Faculty of Medicine, University of Münster. The probands (n = 15) were martial arts disciples recruited from the Kung Fu Training group of the exercises and sports club (TSC) Münster. These probands practise Kung Fu one to two times a week for a time of 1.5 to 2 h over a period of months to years. The control subjects (n = 15) performed any other sports excluding martial
M. Dirkwinkel et al. / Journal of the Neurological Sciences 273 (2008) 108–111 Table 1 Demographic data of the probands and control subjects
Sex Age in years Height in cm Weight in kg BMI in kg/m2 Duration of Kung Fu training in years
Probands (n = 15)
Controls (n = 15)
Significance
14 male 1 female 25.2 ± 7.7 (18.0–44.0) 184.3 ± 8.3 (170.0–201.0) 84.1 ± 12.2 (67.0–108.0) 24.7 ± 2.8 (20.7–32.2) 6.3 ± 4.8 (0.5–18.0)
11 male 4 female 27.6 ± 2.9 (24.0–34.0) 179.9 ± 10.5 (162.0–200.0) 77.9 ± 12.4 (56.0–95.0) 23.9 ± 2.0 (19.2–26.6) ./.
ns (p = 0.130)
Table 3 Results of the measurement of the control subjects at the anterior tibial muscle (peripheral region) and masseter muscle (trigeminal region) at day 1
Sensitive threshold (mA) p = 0.041 Pain threshold (mA) ns (p = 0.267) ns (p = 0.285)
Intensity of threefold pain threshold stimulation (cm VAS) Pain intensity (cm VAS) 1. train
ns (p = 0.744) Pain intensity (cm VAS) 2. train Difference 2. train–1. train (cm VAS)
Data are given as arithmetic mean and standard deviation (range in brackets).
arts and excluding exercises with painful stimulation. They practised their sports in an equal extent as the probands. We matched sex, age, and body mass index of the probands and the control subjects. We recorded the duration of martial arts training in the probands additionally. For all subjects, we defined a study period of 14 days with an experimental measurement on day 1 and day 14 of this period. The probands had to perform inurement exercises during this time, the control subjects continued their normal sports training. 2.2. Inurement exercises The probands applied a daily training of modified Kung Fu exercises which they could do at home without a partner. They received a wooden stick covered with foamed material to emulate an arm or a leg. The probands inured their forearms and lower legs daily for 2 min each by punching them with the wooden stick with moderate power to avoid injuries. We demonstrated the inurement exercises during the first measurement session. 2.3. Measurement of nociception For the experimental measurement of pain thresholds, we applied cutaneous electrical rectangular stimuli by a bipolar saline-soaked surface stimulation electrode. Electrical stimuli were generated by a constant current stimulator (Counterpoint Mk2, Dantec, Copenhagen, Denmark). A single stimulus lasted 1 ms. Repetitive stimuli, so-called trains, consisted of 10 single stimuli at 0.5 Hz. We defined the sensible threshold at the intensity when a subject specified any perception. We defined the pain threshold at the intensity when a subject specified a displeasing perception. The subjects evaluated the pain intensity by a
109
Peripheral stimulation
Trigeminal stimulation
Significance
1.7 ± 0.7 (0.7–3.4) 8.6 ± 4.7 (2.8–19.4) 2.2 ± 2.1 (0.1–6.9) 2.3 ± 1.9 (0.1–6.5) 2.5 ± 2.0 (0.1–7.3) 0.2 ± 0.7 (−1.0–1.5)
1.1 ± 0.9 (0.4–3.8) 4.0 ± 2.6 (0.9–9.0) 3.9 ± 2.2 (0.1–8.5) 3.2 ± 1.9 (0.2–7.3) 3.0 ± 1.9 (0.2–6.8) − 0.2 ± 0.6 (− 1.4–1.2)
p = 0.031
Sensitive threshold (mA) Pain threshold (mA) Intensity of threefold pain threshold stimulation (cm VAS) Pain intensity (cm VAS) 1. train Pain intensity (cm VAS) 2. train Difference 2. train–1. train (cm VAS)
Peripheral stimulation
Trigeminal stimulation
Significance
2.5 ± 2.3 (1.2–9.6) 12.0 ± 6.0 (4.4–26.5) 2.3 ± 1.2 (0.5–4.5) 2.9 ± 1.4 (0.4–5.7) 3.3 ± 1.6 (0.4–5.9) 0.4 ± 0.7 (−0.9–1.5)
1.2 ± 0.4 (0.4–2.0) 4.9 ± 1.9 (2.0–7.4) 4.4 ± 1.9 (1.4–7.8) 4.1 ± 1.9 (1.3–7.4) 3.9 ± 2.0 (1.5–7.8) −0.1 ± 1.3 (−4.0–1.7)
p = 0.002⁎ p = 0.001⁎ p = 0.002⁎ p = 0.015 p = 0.042 ns (p = 0.223)
Data are given as arithmetic mean and standard deviation (range in brackets). ⁎Denotes that the p value remains significant after Bonferroni correction.
p = 0.009⁎ p = 0.021 ns (p = 0.078) ns (p = 0.068)
Data are given as arithmetic mean and standard deviation (range in brackets). ⁎Denotes that the p value remains significant after Bonferroni correction.
visual analogue scala (VAS) with an adjustment from 0 (no pain) to 10 (strongest pain). 2.4. Procedures All subjects were examined in a lying position in the same room with equal temperature and lightning conditions after a rest period. After looking for the anterior tibial muscle and the masseter muscle, the skin over these muscles was cleaned with alcohol and the electrode pads were placed over the muscle. All measures were performed at the right (i.e., dominant) side. The first measurement was at the anterior tibial muscle (i.e., area supplied by the peroneal nerve, further called peripheral stimulation). The amperage was escalated by steps of 0.1 mA until the subjects communicated a perception. After reaching the sensitive threshold, we continued escalating the amperage until the subjects communicated an unpleasant painful feeling. This was noted as the pain threshold in mA. Hereafter, we set a single stimulus with threefold pain threshold strength which the probands had to evaluate on the VAS. Afterwards, we applied a so-called train in an intensity of one and a half times of the pain threshold. After a break of 30 s, we applied a second train. The subjects had to evaluate the last of the ten impulses of each train on the VAS. All measures were done thrice and the mean value was considered as the respective threshold
Table 4 Results of the measurement of probands at the peripheral and trigeminal region at day 1 and day 14 Day 1
Table 2 Results of the measurement of the probands at the anterior tibial muscle (peripheral region) and masseter muscle (trigeminal region) at day 1
p = 0.001⁎
Sensitive threshold (mA) Peripheral Trigeminal Pain threshold (mA) Peripheral Trigeminal Intensity of threefold pain threshold stimulation (cm VAS) Peripheral Trigeminal Pain intensity (cm VAS) 1. train Peripheral Trigeminal Pain intensity (cm VAS) 2. train Peripheral Trigeminal Difference 2. train–1. train (cm VAS) Peripheral Trigeminal
Day 14
Significance
2.5 ± 2.3 1.2 ± 0.4
1.6 ± 0.5 1.1 ± 0.5
p = 0.047 ns (p = 0.819)
12.0 ± 6.0 4.9 ± 1.9
12.0 ± 5.2 6.2 ± 3.5
ns (p = 1.000) ns (p = 0.132)
2.3 ± 1.2 4.4 ± 1.9
2.9 ± 2.0 3.8 ± 1.9
ns (p = 0.625) ns (p = 0.069)
2.9 ± 1.4 4.1 ± 1.9
2.7 ± 1.5 3.0 ± 1.6
ns (p = 0.279) p = 0.006⁎
3.3 ± 1.6 3.9 ± 2.0
2.5 ± 1.5 2.9 ± 1.6
p = 0.023 p = 0.011
0.4 ± 0.7 −0.1 ± 1.3
−0.1 ± 0.6 0.1 ± 0.8
p = 0.016 ns (p = 0.925)
Data are given as arithmetic mean and standard deviation. ⁎Denotes that the p value remains significant after Bonferroni correction.
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M. Dirkwinkel et al. / Journal of the Neurological Sciences 273 (2008) 108–111
Table 5 Results of the measurement of the control subjects at the peripheral and trigeminal region at day 1 and day 14 Day 1 Sensitive threshold (mA) Peripheral Trigeminal Pain threshold (mA) Peripheral Trigeminal Intensity of threefold pain threshold stimulation (cm VAS) Peripheral Trigeminal Pain intensity (cm VAS) 1. train Peripheral Trigeminal Pain intensity (cm VAS) 2. train Peripheral Trigeminal Difference 2. train–1. train (cm VAS) Peripheral Trigeminal
Day 14
thresholds and intensities were not significantly changed after 14 days of routine sport exercises.
Significance
4. Discussion Our data do not demonstrate a general impact of exogenous, repetitive nociceptive stimulation on pain thresholds neither in the peripheral not in the trigeminal innervation region. This finding suggests that inurement exercises in Asian martial arts do not induce a general hypalgesia via impairment of nociceptive mechanisms. Since many disciples report a habituation to pain after long training including inurement exercises (and even without), other mechanisms than nociceptive pathways such as cognitive or affective changes in the attitude towards pain must be responsible for this phenomenon. However, there were some interesting findings. The major significant finding is that the probands but not the control subjects showed a significantly lower pain intensity after train stimulation in the trigeminal (but not in the peripheral) region. The specific examination of the so-called trains, in our study defined as a sequence of 10 painful stimuli with a frequency of 0.5 Hz, was proven in previous studies to be appropriate for the examination of pain thresholds and assessment of pain habituation [1,2]. A lowered pain intensity after repetitive stimuli as applied in our train stimulation points to a change of central sensitisation and central inhibitory control mechanisms [3]. It is possible that the inurement exercises stimulate pain habituation on the spinal level. Interestingly, this could only be observed in the trigeminal region which might be more sensitive to pain habituation (or induces a higher cerebral plasticity) than the peripheral nociceptive system [4,5]. Another interesting finding is that the probands showed an (not significant) increase of pain thresholds at the trigeminal system whereas the control subjects showed a significant decrease. This finding corresponds to the phenomenon in trigeminal pain habituation as described first. Maybe, inurement exercises lead to changes of pain processing resulting in higher pain sensitivity (i.e., lower pain perception) even in regions of the body not directly affected by the exercises. We did not find this phenomenon in the peripheral pain perception. Another aspect of this study is the difference between the peripheral and the trigeminal nerve system in reference to pain thresholds and pain habituation. In other studies, there were distinct threshold differences between the peripheral nerve system and the trigeminal nerve system [1,2,6]. We could confirm the phenomenon that sensitive and pain thresholds are lower and pain intensity ratings are higher in the trigeminal region. This has been explained by the different morphologic structure and the different transmitter systems in both regions [7]. Other individual factors which might have influenced our results but are impossible to control in such a study are the kind of myelination, synaptic networks (increased sensitivity against stimuli on the level of the posterior horn of the spinal cord or decreased inhibition from supraspinal structures), and nerve potentials of facilitating neurons. Our study has several limitations which are related to its character as a pilot study. First, we cannot exclude other factors than the inurement exercises which could have influenced the pain processing during the 14 days of the study period. Second, pain was only elicited by electrical stimulation. This stimulation mainly affects the Aδ-fibres and not other nerve fibres involved in pain perception [8]. Therefore, we cannot conclude on possible pain habituation by inurement exercises via other fibre systems. Third, we applied the painful electrical stimulation at the site of the third branch of the trigeminal nerve. This makes it difficult to transfer our findings to other trigeminal pain mechanisms such as idiopathic headache since these mechanisms are related to the first branch of the trigeminal nerve. Fourth, we examined young and healthy subjects used to routine sports. It might be that in older or untrained patients the mechanisms of pain habituation as observed in
1.7 ± 0.7 1.1 ± 0.9
1.3 ± 0.7 0.9 ± 0.4
ns (p = 0.064) ns (p = 0.732)
8.6 ± 4.7 4.0 ± 2.6
6.1 ± 4.2 3.5 ± 1.8
p = 0.033 ns (p = 0.451)
2.2 ± 2.1 3.9 ± 2.2
2.4 ± 2.2 3.3 ± 1.9
ns (p = 0.409) ns (p = 0.065)
2.3 ± 1.9 3.2 ± 1.9
2.0 ± 1.6 2.4 ± 1.9
ns (p = 0.157) p = 0.038
2.5 ± 2.0 3.0 ± 1.9
2.0 ± 1.7 2.4 ± 1.9
ns (p = 0.068) p = 0.044
0.2 ± 0.7 −0.2 ± 0.6
0.0 ± 0.6 −0.1 ± 0.3
ns (p = 0.068) ns (p = 0.219)
Data are given as arithmetic mean and standard deviation.
or intensity. After the first pass at the anterior tibial muscle region, we repeated all measures at the masseter muscle region (further called trigeminal region). 2.5. Statistics We applied non-parametric testing for statistical analysis. For comparisons within one subject group, we used the Wilcoxon-test. For comparison between the proband and the subject group, we used the Mann–Whitney-U-test. Significance level was set at p = 0.05. Bonferroni correction was applied for multiple testing. 3. Results The demographic data of the probands and subjects are shown in Table 1. The two groups differed only significantly with respect to age (p = 0.041). 3.1. Measurement at day 1 In the probands, the measurement of the trigeminal region showed significantly lower sensitive and pain thresholds than the measurement of the peripheral region (Table 2). The pain intensity after threefold stimulation was also significantly lower for the peripheral than for the trigeminal region. The results of the control subjects were similar to those of the probands (Table 3). The evaluation of the pain intensity of the 1. train as compared to the 2. train (an indicator for a possible pain habituation) did not show a significant difference in both regions and for both subject groups. 3.2. Measurement at day 14 The data of the measurement at day 14 as compared to day 1 are given in Table 4 for the probands and in Table 5 for the control subjects. There were some significant differences for the probands between day 1 and day 14 which however did not remain statistically significant after Bonferroni correction for multiple testing except the difference in pain intensity at train 2 with a lower pain intensity in the trigeminal region after inurement exercises. This means that pain thresholds and pain intensities are not significantly changed after 14 days of inurement exercise except the train stimulation in the trigeminal region. In the control subjects, the differences of the several pain parameters did not remain significant after Bonferroni correction. This means that pain
M. Dirkwinkel et al. / Journal of the Neurological Sciences 273 (2008) 108–111
our study are not the same and that inurement exercises under other circumstances and in other subjects could even increase pain perception. Further, we only examined the right side stimulation and are thus not able to demonstrate differences between the dominant and non-dominant side. Since our female proband group was rather small, we are also not able to demonstrate differences by gender. Some studies reported nociceptive threshold to be higher on the dominant hand of dextral subject and also report gender differences [9]. In summary, our preliminary data suggest that inurement exercises with painful stimulation of the arms and legs have only minor impact on pain processing as measured by our methods and might only influence pain processing in the trigeminal region as measured by the pain intensity after repetitive electrical stimuli. This finding could however be one of the underlying mechanisms responsible for the subjective hypalgesia which is trained by disciples of Asian martial arts. Furthermore, this finding warrants studies with a more sophisticated assessment of pain thresholds and intensities in order to evaluate the possible role of inurement exercises in the treatment of chronic pain.
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References [1] Ashina S, Jensen R, Bendtsen L. Pain sensitivity in pericranial and extracranial regions. Cephalalgia 2003;23:456–62. [2] Ashina S, Bendtsen L, Ashina M, Magerl W, Jensen R. Generalized hyperalgesia in patients with chronic tension-type headache. Cephalalgia 2006;26:940–8. [3] Li J, Simone DA, Larson AA. Windup leads to characteristics of central sensitization. Pain 1999;79:75–82. [4] Katz DB, Simon SA, Moody A, Nicolelis MA. Simultaneous reorganization in thalamocortical ensembles evolves over several hours after perioral capsaicin injections. J Neurophysiol 1999;82:963–77. [5] Ferretti A, Del Gratta C, Babiloni C, Caulo M, Arienzo D, Tartaro A, et al. Functional topography of the secondary somatosensory cortex for nonpainful and painful stimulation of median and tibial nerve: an fMRI study. NeuroImage 2004;23:1217–25. [6] Rhudy JL, Williams AE, McCabe KM, Nguyen MA, Rambo P. Affective modulation of nociception at spinal and supraspinal levels. Psychophysiology 2005;42:579–87. [7] Takemura M, Sugiyo S, Moritani M, Kobayashi M, Yonehara N. Mechanisms of orofacial pain control in the central nervous system. Arch Histol Cytol 2006;69:79–100. [8] Sang CN, Max MB, Gracely RH. Stability and reliability of detection thresholds for human A-beta and A-delta sensory afferents determined by cutaneous electrical stimulation. J Pain Symptom Manage 2003;25:64–73. [9] Sarlani E, Farooq N, Greenspan JD. Gender and laterality differences in thermosensation throughout the perceptible range. Pain 2003;106:9–18.
Contents lists available at ScienceDirect
Journal of the Neurological Sciences j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / j n s
The influence of repetitive painful stimulation on peripheral and trigeminal pain thresholds Monika Dirkwinkel a, Ingrid Gralow b, Reyhan Colak-Ekici c, Anne Wolowski c, Martin Marziniak a, Stefan Evers a,⁎ a b c
Department of Neurology, University of Münster, Germany Department of Anaesthesiology, University of Münster, Germany Department of Dental Prosthetics, University of Münster, Germany
A R T I C L E
I N F O
Article history: Received 29 March 2008 Received in revised form 16 June 2008 Accepted 2 July 2008 Available online 8 August 2008 Keywords: Pain threshold Martial arts Kung Fu Facilitation Habituation Trigeminal Peripheral Hypalgesia
A B S T R A C T We were interested in how continuous painful stimulation which is performed as inurement exercises in some Asian martial arts influences sensory and pain perception. Therefore, we examined 15 Kung Fu disciples before and after a 14 day period with repetitive inurement exercises and measured sensory and pain thresholds and intensities in both the trigeminal and the peripheral (peroneal nerve) region. The results of the probands were compared to those of 15 healthy control subjects who were performing sports without painful stimulation during this period. The probands showed a significantly decreased trigeminal pain intensity after repetitive electrical stimulation whereas the control subjects did not show any changes of sensory or pain perception during the study period. This suggests a change of central sensitisation and inhibitory control mechanisms in the nociceptive spinal or cerebral pathways by inurement exercises. In addition, pain thresholds showed an (not significant) increase after the study period whereas the control subjects showed a significant decrease of pain thresholds. In summary, our pilot study suggests that inurement exercises, i.e. repetitive painful stimulation, over a period of 14 days might induce changes of pain perception resulting in trigeminal pain habituation and higher pain thresholds. © 2008 Elsevier B.V. All rights reserved.
1. Introduction In the last years, one of the main topics in trigeminal pain research was how pain facilitation and pain inhibition can influence each other and how one can measure these phenomena [1]. We were interested in how repetitive exogenous painful stimulation can influence trigeminal and peripheral pain thresholds and pain perception. Some Asian martial arts use repetitive painful exercises to subsequently decrease subjective pain perception. Especially in the traditional Chinese Shaolin Kung Fu, inurement exercises are exactly defined. The aim of these exercises is that the body of the martial arts disciple should be habituated to pain in order to be prepared for the fighting situation. The inurement exercises of the Mantis Kung Fu style can serve as a model to explore the impact of exogenous repetitive painful stimulation. In this study, we therefore examined if this training of exogenously induced pain with the aim of subjective hypalgesia is leading to changes of peripheral and trigeminal pain thresholds and, thus, can change pain facilitation and pain inhibition. Because of the anatomical differences of the peripheral and trigeminal nociceptive systems we ⁎ Corresponding author. Department of Neurology, University of Münster, AlbertSchweitzer-Str. 33, 48129 Münster, Germany. Fax: +49 251 8348181. E-mail address: [email protected] (S. Evers). 0022-510X/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.jns.2008.07.002
studied them separately. We chose the anterior tibial muscle region which is supplied by the peroneal nerve as a model for the peripheral nervous system and the masseter muscle region supplied by the trigeminal nerve as a model for the trigeminal system. 2. Methods 2.1. Subjects We included 30 healthy male and female subjects. Exclusion criteria were the presence of neurological or psychiatric diseases as well as regular intake of analgesics or other medication. The female subjects were not allowed to use oral contraceptives to avoid influence of this medication on pain perception. The age range of the subjects was between 18 and 40 years. They were excluded from participation in further pain studies. We only included right-handed subjects. All subjects gave informed consent to participate in the study. The study was approved by the Ethics Committee of the Faculty of Medicine, University of Münster. The probands (n = 15) were martial arts disciples recruited from the Kung Fu Training group of the exercises and sports club (TSC) Münster. These probands practise Kung Fu one to two times a week for a time of 1.5 to 2 h over a period of months to years. The control subjects (n = 15) performed any other sports excluding martial
M. Dirkwinkel et al. / Journal of the Neurological Sciences 273 (2008) 108–111 Table 1 Demographic data of the probands and control subjects
Sex Age in years Height in cm Weight in kg BMI in kg/m2 Duration of Kung Fu training in years
Probands (n = 15)
Controls (n = 15)
Significance
14 male 1 female 25.2 ± 7.7 (18.0–44.0) 184.3 ± 8.3 (170.0–201.0) 84.1 ± 12.2 (67.0–108.0) 24.7 ± 2.8 (20.7–32.2) 6.3 ± 4.8 (0.5–18.0)
11 male 4 female 27.6 ± 2.9 (24.0–34.0) 179.9 ± 10.5 (162.0–200.0) 77.9 ± 12.4 (56.0–95.0) 23.9 ± 2.0 (19.2–26.6) ./.
ns (p = 0.130)
Table 3 Results of the measurement of the control subjects at the anterior tibial muscle (peripheral region) and masseter muscle (trigeminal region) at day 1
Sensitive threshold (mA) p = 0.041 Pain threshold (mA) ns (p = 0.267) ns (p = 0.285)
Intensity of threefold pain threshold stimulation (cm VAS) Pain intensity (cm VAS) 1. train
ns (p = 0.744) Pain intensity (cm VAS) 2. train Difference 2. train–1. train (cm VAS)
Data are given as arithmetic mean and standard deviation (range in brackets).
arts and excluding exercises with painful stimulation. They practised their sports in an equal extent as the probands. We matched sex, age, and body mass index of the probands and the control subjects. We recorded the duration of martial arts training in the probands additionally. For all subjects, we defined a study period of 14 days with an experimental measurement on day 1 and day 14 of this period. The probands had to perform inurement exercises during this time, the control subjects continued their normal sports training. 2.2. Inurement exercises The probands applied a daily training of modified Kung Fu exercises which they could do at home without a partner. They received a wooden stick covered with foamed material to emulate an arm or a leg. The probands inured their forearms and lower legs daily for 2 min each by punching them with the wooden stick with moderate power to avoid injuries. We demonstrated the inurement exercises during the first measurement session. 2.3. Measurement of nociception For the experimental measurement of pain thresholds, we applied cutaneous electrical rectangular stimuli by a bipolar saline-soaked surface stimulation electrode. Electrical stimuli were generated by a constant current stimulator (Counterpoint Mk2, Dantec, Copenhagen, Denmark). A single stimulus lasted 1 ms. Repetitive stimuli, so-called trains, consisted of 10 single stimuli at 0.5 Hz. We defined the sensible threshold at the intensity when a subject specified any perception. We defined the pain threshold at the intensity when a subject specified a displeasing perception. The subjects evaluated the pain intensity by a
109
Peripheral stimulation
Trigeminal stimulation
Significance
1.7 ± 0.7 (0.7–3.4) 8.6 ± 4.7 (2.8–19.4) 2.2 ± 2.1 (0.1–6.9) 2.3 ± 1.9 (0.1–6.5) 2.5 ± 2.0 (0.1–7.3) 0.2 ± 0.7 (−1.0–1.5)
1.1 ± 0.9 (0.4–3.8) 4.0 ± 2.6 (0.9–9.0) 3.9 ± 2.2 (0.1–8.5) 3.2 ± 1.9 (0.2–7.3) 3.0 ± 1.9 (0.2–6.8) − 0.2 ± 0.6 (− 1.4–1.2)
p = 0.031
Sensitive threshold (mA) Pain threshold (mA) Intensity of threefold pain threshold stimulation (cm VAS) Pain intensity (cm VAS) 1. train Pain intensity (cm VAS) 2. train Difference 2. train–1. train (cm VAS)
Peripheral stimulation
Trigeminal stimulation
Significance
2.5 ± 2.3 (1.2–9.6) 12.0 ± 6.0 (4.4–26.5) 2.3 ± 1.2 (0.5–4.5) 2.9 ± 1.4 (0.4–5.7) 3.3 ± 1.6 (0.4–5.9) 0.4 ± 0.7 (−0.9–1.5)
1.2 ± 0.4 (0.4–2.0) 4.9 ± 1.9 (2.0–7.4) 4.4 ± 1.9 (1.4–7.8) 4.1 ± 1.9 (1.3–7.4) 3.9 ± 2.0 (1.5–7.8) −0.1 ± 1.3 (−4.0–1.7)
p = 0.002⁎ p = 0.001⁎ p = 0.002⁎ p = 0.015 p = 0.042 ns (p = 0.223)
Data are given as arithmetic mean and standard deviation (range in brackets). ⁎Denotes that the p value remains significant after Bonferroni correction.
p = 0.009⁎ p = 0.021 ns (p = 0.078) ns (p = 0.068)
Data are given as arithmetic mean and standard deviation (range in brackets). ⁎Denotes that the p value remains significant after Bonferroni correction.
visual analogue scala (VAS) with an adjustment from 0 (no pain) to 10 (strongest pain). 2.4. Procedures All subjects were examined in a lying position in the same room with equal temperature and lightning conditions after a rest period. After looking for the anterior tibial muscle and the masseter muscle, the skin over these muscles was cleaned with alcohol and the electrode pads were placed over the muscle. All measures were performed at the right (i.e., dominant) side. The first measurement was at the anterior tibial muscle (i.e., area supplied by the peroneal nerve, further called peripheral stimulation). The amperage was escalated by steps of 0.1 mA until the subjects communicated a perception. After reaching the sensitive threshold, we continued escalating the amperage until the subjects communicated an unpleasant painful feeling. This was noted as the pain threshold in mA. Hereafter, we set a single stimulus with threefold pain threshold strength which the probands had to evaluate on the VAS. Afterwards, we applied a so-called train in an intensity of one and a half times of the pain threshold. After a break of 30 s, we applied a second train. The subjects had to evaluate the last of the ten impulses of each train on the VAS. All measures were done thrice and the mean value was considered as the respective threshold
Table 4 Results of the measurement of probands at the peripheral and trigeminal region at day 1 and day 14 Day 1
Table 2 Results of the measurement of the probands at the anterior tibial muscle (peripheral region) and masseter muscle (trigeminal region) at day 1
p = 0.001⁎
Sensitive threshold (mA) Peripheral Trigeminal Pain threshold (mA) Peripheral Trigeminal Intensity of threefold pain threshold stimulation (cm VAS) Peripheral Trigeminal Pain intensity (cm VAS) 1. train Peripheral Trigeminal Pain intensity (cm VAS) 2. train Peripheral Trigeminal Difference 2. train–1. train (cm VAS) Peripheral Trigeminal
Day 14
Significance
2.5 ± 2.3 1.2 ± 0.4
1.6 ± 0.5 1.1 ± 0.5
p = 0.047 ns (p = 0.819)
12.0 ± 6.0 4.9 ± 1.9
12.0 ± 5.2 6.2 ± 3.5
ns (p = 1.000) ns (p = 0.132)
2.3 ± 1.2 4.4 ± 1.9
2.9 ± 2.0 3.8 ± 1.9
ns (p = 0.625) ns (p = 0.069)
2.9 ± 1.4 4.1 ± 1.9
2.7 ± 1.5 3.0 ± 1.6
ns (p = 0.279) p = 0.006⁎
3.3 ± 1.6 3.9 ± 2.0
2.5 ± 1.5 2.9 ± 1.6
p = 0.023 p = 0.011
0.4 ± 0.7 −0.1 ± 1.3
−0.1 ± 0.6 0.1 ± 0.8
p = 0.016 ns (p = 0.925)
Data are given as arithmetic mean and standard deviation. ⁎Denotes that the p value remains significant after Bonferroni correction.
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Table 5 Results of the measurement of the control subjects at the peripheral and trigeminal region at day 1 and day 14 Day 1 Sensitive threshold (mA) Peripheral Trigeminal Pain threshold (mA) Peripheral Trigeminal Intensity of threefold pain threshold stimulation (cm VAS) Peripheral Trigeminal Pain intensity (cm VAS) 1. train Peripheral Trigeminal Pain intensity (cm VAS) 2. train Peripheral Trigeminal Difference 2. train–1. train (cm VAS) Peripheral Trigeminal
Day 14
thresholds and intensities were not significantly changed after 14 days of routine sport exercises.
Significance
4. Discussion Our data do not demonstrate a general impact of exogenous, repetitive nociceptive stimulation on pain thresholds neither in the peripheral not in the trigeminal innervation region. This finding suggests that inurement exercises in Asian martial arts do not induce a general hypalgesia via impairment of nociceptive mechanisms. Since many disciples report a habituation to pain after long training including inurement exercises (and even without), other mechanisms than nociceptive pathways such as cognitive or affective changes in the attitude towards pain must be responsible for this phenomenon. However, there were some interesting findings. The major significant finding is that the probands but not the control subjects showed a significantly lower pain intensity after train stimulation in the trigeminal (but not in the peripheral) region. The specific examination of the so-called trains, in our study defined as a sequence of 10 painful stimuli with a frequency of 0.5 Hz, was proven in previous studies to be appropriate for the examination of pain thresholds and assessment of pain habituation [1,2]. A lowered pain intensity after repetitive stimuli as applied in our train stimulation points to a change of central sensitisation and central inhibitory control mechanisms [3]. It is possible that the inurement exercises stimulate pain habituation on the spinal level. Interestingly, this could only be observed in the trigeminal region which might be more sensitive to pain habituation (or induces a higher cerebral plasticity) than the peripheral nociceptive system [4,5]. Another interesting finding is that the probands showed an (not significant) increase of pain thresholds at the trigeminal system whereas the control subjects showed a significant decrease. This finding corresponds to the phenomenon in trigeminal pain habituation as described first. Maybe, inurement exercises lead to changes of pain processing resulting in higher pain sensitivity (i.e., lower pain perception) even in regions of the body not directly affected by the exercises. We did not find this phenomenon in the peripheral pain perception. Another aspect of this study is the difference between the peripheral and the trigeminal nerve system in reference to pain thresholds and pain habituation. In other studies, there were distinct threshold differences between the peripheral nerve system and the trigeminal nerve system [1,2,6]. We could confirm the phenomenon that sensitive and pain thresholds are lower and pain intensity ratings are higher in the trigeminal region. This has been explained by the different morphologic structure and the different transmitter systems in both regions [7]. Other individual factors which might have influenced our results but are impossible to control in such a study are the kind of myelination, synaptic networks (increased sensitivity against stimuli on the level of the posterior horn of the spinal cord or decreased inhibition from supraspinal structures), and nerve potentials of facilitating neurons. Our study has several limitations which are related to its character as a pilot study. First, we cannot exclude other factors than the inurement exercises which could have influenced the pain processing during the 14 days of the study period. Second, pain was only elicited by electrical stimulation. This stimulation mainly affects the Aδ-fibres and not other nerve fibres involved in pain perception [8]. Therefore, we cannot conclude on possible pain habituation by inurement exercises via other fibre systems. Third, we applied the painful electrical stimulation at the site of the third branch of the trigeminal nerve. This makes it difficult to transfer our findings to other trigeminal pain mechanisms such as idiopathic headache since these mechanisms are related to the first branch of the trigeminal nerve. Fourth, we examined young and healthy subjects used to routine sports. It might be that in older or untrained patients the mechanisms of pain habituation as observed in
1.7 ± 0.7 1.1 ± 0.9
1.3 ± 0.7 0.9 ± 0.4
ns (p = 0.064) ns (p = 0.732)
8.6 ± 4.7 4.0 ± 2.6
6.1 ± 4.2 3.5 ± 1.8
p = 0.033 ns (p = 0.451)
2.2 ± 2.1 3.9 ± 2.2
2.4 ± 2.2 3.3 ± 1.9
ns (p = 0.409) ns (p = 0.065)
2.3 ± 1.9 3.2 ± 1.9
2.0 ± 1.6 2.4 ± 1.9
ns (p = 0.157) p = 0.038
2.5 ± 2.0 3.0 ± 1.9
2.0 ± 1.7 2.4 ± 1.9
ns (p = 0.068) p = 0.044
0.2 ± 0.7 −0.2 ± 0.6
0.0 ± 0.6 −0.1 ± 0.3
ns (p = 0.068) ns (p = 0.219)
Data are given as arithmetic mean and standard deviation.
or intensity. After the first pass at the anterior tibial muscle region, we repeated all measures at the masseter muscle region (further called trigeminal region). 2.5. Statistics We applied non-parametric testing for statistical analysis. For comparisons within one subject group, we used the Wilcoxon-test. For comparison between the proband and the subject group, we used the Mann–Whitney-U-test. Significance level was set at p = 0.05. Bonferroni correction was applied for multiple testing. 3. Results The demographic data of the probands and subjects are shown in Table 1. The two groups differed only significantly with respect to age (p = 0.041). 3.1. Measurement at day 1 In the probands, the measurement of the trigeminal region showed significantly lower sensitive and pain thresholds than the measurement of the peripheral region (Table 2). The pain intensity after threefold stimulation was also significantly lower for the peripheral than for the trigeminal region. The results of the control subjects were similar to those of the probands (Table 3). The evaluation of the pain intensity of the 1. train as compared to the 2. train (an indicator for a possible pain habituation) did not show a significant difference in both regions and for both subject groups. 3.2. Measurement at day 14 The data of the measurement at day 14 as compared to day 1 are given in Table 4 for the probands and in Table 5 for the control subjects. There were some significant differences for the probands between day 1 and day 14 which however did not remain statistically significant after Bonferroni correction for multiple testing except the difference in pain intensity at train 2 with a lower pain intensity in the trigeminal region after inurement exercises. This means that pain thresholds and pain intensities are not significantly changed after 14 days of inurement exercise except the train stimulation in the trigeminal region. In the control subjects, the differences of the several pain parameters did not remain significant after Bonferroni correction. This means that pain
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our study are not the same and that inurement exercises under other circumstances and in other subjects could even increase pain perception. Further, we only examined the right side stimulation and are thus not able to demonstrate differences between the dominant and non-dominant side. Since our female proband group was rather small, we are also not able to demonstrate differences by gender. Some studies reported nociceptive threshold to be higher on the dominant hand of dextral subject and also report gender differences [9]. In summary, our preliminary data suggest that inurement exercises with painful stimulation of the arms and legs have only minor impact on pain processing as measured by our methods and might only influence pain processing in the trigeminal region as measured by the pain intensity after repetitive electrical stimuli. This finding could however be one of the underlying mechanisms responsible for the subjective hypalgesia which is trained by disciples of Asian martial arts. Furthermore, this finding warrants studies with a more sophisticated assessment of pain thresholds and intensities in order to evaluate the possible role of inurement exercises in the treatment of chronic pain.
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