Abnormalities of masseter inhibitory reflex in patients with episodic tension-type headache

Abnormalities of masseter inhibitory reflex in patients with episodic tension-type headache 1 first-author †E-mail:tzvetanovplamen@hotmail.com †E-mail:tzvetanovplamen@hotmail.com tzvetanovplamen@hotmail.com 1 2 Department of Neurology and Neurosurgery, Medical University of Pleven, 5800 Pleven, Bulgaria Department of Neurology and Neurosurgery, Medical University of Pleven, 5800 Pleven, Bulgaria Department of Physiology, Medical University of Pleven, 5800 Pleven, Bulgaria Department of Physiology, Medical University of Pleven, 5800 Pleven, Bulgaria Objective: 2 To investigate the masseter inhibitory reflex (MIR) and its eventual changes in patients with episodic tension-type headache (TTH). Methods: 2 MIR was studied in 21 patients with episodic TTH and 30 healthy subjects, with age and sex matched to the study cohort. Median age of patients was 17.0 years (ranged 16~49 years), median duration of disease 12 months (1~5 years), and median frequency of headache 7.5 d per month. Results: 2 The second period of suppression (S2) of MIR was reduced in intensity and duration in 10% of controls and 66.7% (confidence interval ( CI )=45.3%~85%; P < 0.05) of patients with episodic TTH ( χ 2 =74.9; P < 0.001). In 3 (14.3%) of patients with episodic TTH, S2 was completely absent. No significant correlation between the duration of disease and headache frequency was found. Conclusion: 2 Our results confirm the link between episodic TTH and reduction or absence of S2. Teenage patients with episodic TTH may exhibit marked pathological changes in S2 in contrast to older individuals. Tension-type headache (TTH) Temporalis muscle exteroceptive suppression Masseter inhibitory reflex (MIR) INTRODUCTION 1 Masseter inhibitory reflex (MIR), also known as jaw-opening reflex (jaw jerk reflex), temporalis muscle exteroceptive suppression, and masseter silent period, manifests in reflex inhibition of the voluntary contraction of the muscles of mastication in response to intensive mechanical or electrical stimulation of the oral mucosa, and the teeth and skin in the area innervated by the maxillary and mandibular nerves. It is considered mainly as protective reflex, but participates in the coordination of the mandibular movements in mastication and articulation as well (Schoenen, 1993 1993 ). From a neurophysiologic point of view, the phenomenon of MIR becomes apparent in the appearance of two periods of muscle silence: early (S1), with latent period of 10~15 ms and minimum duration of 10 ms, and late (S2), with latent period of 40~60 ms and minimum duration of 20 ms. These periods are separated by a short period of activity (Wallasch et al., 1993 1993 ; Göbel and Dworschak, 1996 1996 ), which is considered to be a transcortical analogue of the long-loop reflex of the limbs (Ongerboer de Visser et al., 1990 1990 ). Many researches clarify MIR to a great extent to be the anatomical background and the functional importance of the reflex (Yemm, 1972 1972 ; Cruccu et al., 1989 1989 ; Ongerboer de Visser et al., 1990 1990 ). A commonly accepted opinion is that S1 represents oligosynaptic inhibitory reflex, mediated by A-beta afferent components of the trigeminal nerve, which complete a reflex arch via neurons exiting the rostral portion of the spinal trigeminal nucleus at the level of the middle third of the pons, and project bilaterally on the trigeminal motor nucleus. S2 causes greater contradictions and is considered as nociceptive reflex, proprioceptive period of silence, a pause evoked by the synchronization in the neuronal activity, and multisynaptic skin reflex (Ongerboer de Visser et al., 1990 1990 ). It has been clarified that S2 is also mediated by A-beta afferent fibers, which reach neurons of the spinal trigeminal nucleus located in the lowest caudal pons, from where projections extend polysynaptically via the lateral reticular formation and ascend to the motor nucleus bilaterally (Yemm, 1972 1972 ). S2 is suppressed by nicotine, as this effect in turn is blocked by naloxon. The reason for this is that the inhibitory neurons, responsible for S2, are cholinergic and are included in a wider cholinergic inhibitory system, passing through the whole brain stem. This system is under intensive limbic control and participates in the structures connected with pain modulation (Yu et al., 1973 1973 ; Woolf, 1991 1991 ; Schoenen et al., 1991 1991 ). It has been reported that in patients with chronic tension-type headache (TTH) S2 of MIR is reduced in duration and intensity (Miles et al., 1987 1987 ; Cruccu et al., 1989 1989 ; Wang and Schoenen, 1994 1994 ; Wang et al., 1995 1995 ; Lipchik et al., 2000 2000 ; Aktekin et al., 2001 2001 ). The aim of the present study is to investigate the reflex and its eventual changes in patients with episodic TTH. MATERIALS AND METHODS 1 Twenty-one patients (median age 17.0 years, ranged 16~49 years) with episodic TTH (median duration of disease 12 months (1~5 years), and median frequency of headache 7.5 d per month), who met the criteria of Headache Classification Subcommittee of the International Headache Society ( 2004 2004 ), were studied in the period without headache after informed consent. Young patients, who are non-smokers, without personal and family history of migraine, any somatic diseases, or systematic acceptance of medication, were deliberately chosen. History and physical examination data are presented in Table 1 1 . M: male; F: female; b: bilateral; f: frontal; t: temporal; o: occipital Patient No. Sex Age (year) Duration of disease Incidence (day per month) Duration of attacks (h) Site Clinical characteristics of the headache 1 M 16 2 years 4~8 1~2 b, f, t Pressure, tightness 2 M 18 18 moths 4~8 1~2 b, f, t Pressure, tightness 3 F 16 2 years 2~4 2~6 b, t Tightness 4 F 39 6 months 10~15 1~4 b, f, t Pressure 5 F 35 6 months 10 6~12 b, t Tight band around head 6 F 46 1 year 5~10 4~6 f, b, t Tightness 7 F 35 18 years 10~15 2~6 b, f, t Pressure 8 M 49 5 months 5~10 4~6 b, f Tightness 9 M 28 1 month 10 4~6 b, f, t Tightness, pressure 10 F 18 1 year 5 ≤24 b, f, t Tightness 11 F 17 1 year 1~2 6~12 b, f, o Tightness 12 F 17 6 month 10 2 b, t Pressure, tightness 13 F 17 4 years 15 12 b, f, t Tightness 14 M 17 6 months 10~15 1~2 b, t Tightness 15 F 17 1 year 15 12 b, f, t Pressure 16 F 17 1 year 15 2~4 b, f Tightness 17 F 17 5 years 5~10 2~6 b, t Tightness 18 F 17 3 years 5~10 6~12 b, t Tightness, pressure 19 M 17 2 years 5 2~6 b, f, t Tightness 20 F 38 18 months 12~15 2~24 b, f, o Pressure 21 M 17 1 year 5~10 2~4 b, f, t Tightness To investigate the episode frequency, the patients were examined a month after the primary check up. The equipment used was “Medicor” with a computer system for electromyography “Pulse-Art” and “Toennies-Multilinear” (Jaeger/Toennies, Germany) machine. MIR was investigated according to the standard method as follows: the activity of both head side temporal muscles was registered with surface electrodes, as the active electrode was placed over the muscle belly, and the referent on the cheekbone arch. Nervus mentalis (n. mentalis) was stimulated with electrical stimuli with duration of 0.1 ms in the projection of foramen mentale in maximum voluntary contraction of masticatory muscles. To avoid reflex habituation, the frequency of stimulation used was about 1 min −1 . The stimulus intensity was 3 to 5 times the sensory threshold (ranged from 12 to 24 mA), which corresponds to the subject’s sensation of light pain radiating to the teeth. First the right n. mentalis and second the left n. mentalis were stimulated consecutively, as the activity was registered in two channels from both temporal muscles. Ten traces with duration of 250 ms and predelay of 50 ms were superimposed. The curves obtained were subjected to full-wave rectification in some of the patients. The curves were evaluated visually after recording on a paper, and the following conditional classification was accepted: Type 1—normal S2 (Fig. 1a 1a ); Type 2—S2 suppression with reduction of its duration and presence of action potentials in the suppression period with summation amplitudes ranging from 20% to 80% of the initial total sum amplitude (Fig. 1b 1b ); Type 3—complete absence of S2 (Fig. 1c 1c ). Results were compared with normative values of the laboratory obtained from 30 healthy persons with age and sex matched to the study cohort. The Statgraphics Plus Version 2.1 statistical system was used. For data analysis, the χ 2 test and confidence interval ( CI ) were applied. A level of P < 0.05 was considered statistically significant. RESULTS 1 The second period of suppression (S2) was reduced in intensity and duration in 10% of controls and 66.7% ( CI =45.3%~85%; P < 0.05) of patients with episodic TTH ( χ 2 =74.9; P < 0.001). Type 1, normal S2, was recorded in 7 (33.3%) patients (Fig. 1a 1a ). Type 2, changed but available S2, was found in 11 patients (52.4%) (Fig. 1b 1b ). Three patients (14.3%) demonstrated Type 3 recording, corresponding to the most marked change (Fig. 1c 1c ). The distribution of the three types of recordings in accordance with the age, duration of disease, and frequency and duration of attacks is shown in Table 2 2 . Certain teenage patients with episodic TTH exhibited marked pathological changes of S2 in contrast to older individuals. No significant correlation between the duration of disease and headache frequency was found. 3 Type of S2 suppression 15 Patient number 4 Age (year) 4 Duration of disease (month) 4 Duration of attacks (h) 3 Frequency of attacks (day per month) ≤20 21~30 31~40 41~50 ≤6 7~12 13~24 >24 2~4 5~6 7~12 >12 ≤5 6~10 11~15 1 4 1 1 1 − 4 1 2 2 2 2 1 4 1 2 2 7 − 3 1 5 − 3 3 3 5 2 1 1 5 5 3 3 − − − 1 1 3 − 1 − 1 1 1 − 2 DISCUSSION 1 We reported the significant changes of S2 in the patients with episodic TTH. Patients with personal or family history of migraine were not included to avoid the reduction of habituation of the nociception-specific blink reflex (Di Clemente et al., 2007 2007 ). The comparatively limited number of patients included in the present study does not allow a strong conclusion to be drawn but several tendencies emerged. Firstly, the abnormalities in S2 were demonstrated in 66.7% of the patients with episodic TTH, whereas they were presented in 16.3% of the total number of patients. These results are in concert with the findings of Wang and Schoenen ( 1994 1994 ), suggesting that the genesis of the chronic and episodic TTH is similar. Exteroceptive suppression of temporalis muscle activity has been reported to be reduced mainly in chronic TTH (Miles et al., 1987 1987 ; Cruccu et al., 1989 1989 ; Wallasch, 1991 1991 ; Schoenen and Agrégé, 1993 1993 ; Wang et al., 1995 1995 ; Lipchik et al., 2000 2000 ; Aktekin et al., 2001 2001 ). The correlation is specific, because in patients with migraine, post-lumbar puncture headache, headache in inflammatory diseases, and mass lesions, similar changes were not found (Miles et al., 1987 1987 ; Paulus et al., 1992 1992 ; Raudino, 1994 1994 ; Zwart and Sand, 1995 1995 ). The explanation of this fact could be searched in a wider cholinergic dysfunction that might lie in the background of the reduced pain thresholds and the reduction of S2 as epiphenomenona. The changes observed in TTH are also due to hyperexcitability of the reticular nuclei, which inhibit the medullary inhibitory interneurons mediating S2 (Göbel et al., 1993 1993 ; Wallasch and Göbel, 1993 1993 ; Neufeld et al., 2000 2000 ). To some extent, our results are in contrast to the findings of Wallasch et al.( 1991 1991 ). They reported shortened duration of S2 in patients suffering from chronic TTH compared to migraineurs and controls. However, patients with episodic TTH exhibited late suppression periods of temporal muscle activity of differing durations. The discrepancy might be explained by the age of our patients, and future investigations could be useful to verify such a correlation. It is impressive that more marked changes in S2 were observed in the youngest group of patients. Furthermore, the duration of disease and episode frequency do not form any significant correlation towards the types of S2. Younger patients with more marked changes in S2 represent a group of predisposed individuals, which would most likely develop chronic TTH in the future, while in older patients the genesis is not that closely linked with dysfunction of the cholinergic inhibitory systems. However, more studies need to be done with more patients with episodic TTH, as well as their prospective studies. In conclusion, the second period of suppression (S2) in MIR was reduced in intensity and duration, or was absent in 66.7% of the patients with episodic TTH. A tendency for differentiation of the group of patients with TTH at young age and with marked changes in S2, has been formed. They might most likely differ in prognosis from other episodic TTH patients. References B Aktekin , K Yaltkaya , S Ozkaynak , Y Oguz . 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