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Cephalalgia 30(1) 7786 ! International Headache Society 2009 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1111/j.1468-2982.2009.01901.x cep.sagepub.com
Generalized neck-shoulder hyperalgesia in chronic tension-type headache and unilateral migraine assessed by pressure pain sensitivity topographical maps of the trapezius muscle
as1,2,3, P Madeleine2, AB Caminero4, ndez-de-las-Pen C Ferna ML Cuadrado3,5,6, L Arendt-Nielsen2 and JA Pareja3,5
Abstract Spatial changes in pressure pain hypersensitivity are present throughout the cephalic region (temporalis muscle) in both chronic tension-type headache (CTTH) and unilateral migraine. The aim of this study was to assess pressure pain sensitivity topographical maps on the trapezius muscle in 20 patients with CTTH and 20 with unilateral migraine in comparison with 20 healthy controls in a blind design. For this purpose, a pressure algometer was used to assess pressure pain thresholds (PPT) over 11 points of the trapezius muscle: four points in the upper part of the muscle, two over the levator scapulae muscle, two in the middle part, and the remaining three points in the lower part of the muscle. Pressure pain sensitivity maps of both sides (dominant/non-dominant; symptomatic/non-symptomatic) were depicted for patients and controls. CTTH patients showed generalized lower PPT levels compared with both migraine patients (P 0.03) and controls (P < 0.001). The migraine group had also lower PPT than healthy controls (P < 0.001). The most sensitive location for the assessment of PPT was the neck portion of the upper trapezius muscle in both patient groups and healthy controls (P < 0.001). PPT was negatively related to some clinical pain features in both CTTH and unilateral migraine patients (all P < 0.05). Side-to-side differences were found in strictly unilateral migraine, but not in those subjects with bilateral pain, i.e. CTTH. These data support the influence of muscle hyperalgesia in both CTTH and unilateral migraine patients and point towards a general pressure pain hyperalgesia of neck-shoulder muscles in headache patients, particularly in CTTH. Keywords Pressure pain sensitivity, trapezius muscle, chronic tension-type headache, unilateral migraine
Date received: 31 October 2008; accepted: 8 March 2009
Introduction
Headache is the most prevalent neurological disorder and experienced by almost everyone (1). Among headaches, tension-type headache represents the most common type with 1-year prevalence rates of 38.3% for the episodic form and 2.2% for the chronic form (2). In addition, the prevalence of tension-type headache has increased in recent years (3). The second most common headache, migraine, has a lifetime prevalence of 16% worldwide, and a last-year prevalence of 10% (4). Migraine and tension-type headache may cause substantial levels of disability not only to the individual patient and their family but also to the entire global society due to very high prevalence in the general
1 Department of Physical Therapy, Occupational Therapy, Physical n, Medicine and Rehabilitation of Universidad Rey Juan Carlos, Alcorco Madrid, Spain. 2 Centre for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University, Aalborg, Denmark. 3 n, Aesthesiology Laboratory of Universidad Rey Juan Carlos, Alcorco Madrid, Spain. 4 Neurology Department of Hospital Avila, Avila, Spain. 5 n Hospital Alcorco n and Departments of Neurology of Fundacio n, Madrid, Spain. Universidad Rey Juan Carlos, Alcorco 6 nico San Carlos and Universidad Neurology Department, Hospital Cl Complutense, Madrid, Spain.
Corresponding author: sar Ferna ndez de las Pen as, Facultad de Ciencias de la Salud, Ce n, Universidad Rey Juan Carlos, Avenida de Atenas s/n, 28922 Alcorco Madrid, Spain. Email: [email protected]
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population (5). Globally, the percentage of the adult population with a headache disorder is 47% for headache in general, 10% for migraine, 38% for tension-type headache and 3% for chronic headache that lasts for > 15 days/month (6). Furthermore, there has been increasing interest in the pathogenic mechanisms of these disorders within recent decades, but knowledge is scant, despite some advances in aetiology. It seems clear that hyperexcitability of nociceptive pathways plays an important role in both headaches (7,8). The sensitization of these pathways causes increased muscle tenderness in tension-type headache (9,10) and cutaneous allodynia in migraine patients (1113). Furthermore, these manifestations of sensitization are corroborated by increased mechanical pain sensitivity. Previous studies have found a decrease in pressure pain thresholds (PPTs) in chronic tension-type headache (CTTH) (1416) However, the results on PPTs in migraine populations are contradictory, since some studies have reported lower values in patients compared with controls (17,18), whereas others have not (9,19,20). These conicting results in migraine may be related to the following aspects. First, previous studies have included patients with bilateral or side shifting migraine (9,1720). A recent study from our group has demonstrated side-to-side dierences in mechanical pain sensitivity in patients with strictly unilateral migraine (21), with signicant variations between sides that reveal that the side of stimulation can be highly relevant. Muscle tenderness was mostly related to hyperaesthesia of the following specic muscles, i.e. suboccipital, temporalis, sternocleidomastoid, rather than generalized muscle tenderness akin to that present in both tension-type headache forms (21). These ndings suggest that mechanical sensitivity in migraine can be a more complex clinical picture than expected, because of lateralization of pain sensitivity. A second aspect to explore is that previous studies investigating pain sensitivity in patients with migraine or tension-type headache have used a single standardized point in the anterior part of the temporalis muscle (9,1420). However, it is known that pressure pain sensitivity is not uniformly distributed over this muscle, since spatial changes in mechanical pain sensitivity are present throughout the cephalic region in both CTTH (22) and unilateral migraine patients (23). The anterior column of the temporalis muscle has been found to be the most sensitive part as depicted by pain sensitivity maps in strictly unilateral migraine and CTTH (22,23), but not in healthy matched controls. Work-related musculoskeletal disorders are often accompanied by pain in the neck-shoulder region (24) and headache (25). An overlap of trigeminal and upper cervical spinal aerent bres in the caudal components
Cephalalgia 30(1) (trigeminal nucleus caudalis) of the trigeminal brainstem complex and in the C1C3 segments has been described in animals (26). This has also been corroborated by electrophysiological ndings revealing convergence of trigeminal and cervical aerents onto both nociceptive and non-nociceptive neurons in trigeminal subnucleus caudalis in animals (27). Moreover, this is also supported by data reporting convergence between aerents from trapezius and temporalis muscles (28). Thus, there is a need for studies focusing on the relationship between headache and neck-shoulder muscles (29). Some studies have reported similarities between neck-shoulder pain and tension-type headache (30,31). Non-uniform distribution of pain sensitivity has also been reported in the shoulder region (32,33). Nevertheless, topographical distribution of pressure sensitivity maps over the trapezius muscle has not been previously investigated in primary headaches. The aim of this study was to investigate mechanical pain sensitivity distribution over the trapezius muscle in patients with CTTH and strictly unilateral migraine compared with matched controls.
ndez-de-las-Pen Ferna as et al. phonophobia, vomiting or nausea during attacks. Each patient fullled the criteria for CTTH, and there was no evidence of secondary headaches. Patients completed a headache diary for 4 weeks in order to complement the diagnosis (35). To be included in the migraine group, patients had to present the following features typical of migraine attacks: unilateral location, pulsating quality, moderate or severe pain intensity, photophobia, phonophobia, vomiting or nausea during headache and pain aggravation during physical activity. Furthermore, patients had to describe strictly unilateral headache attacks without side shift. Other primary headaches were excluded. A neuroimaging examination (magnetic resonance imaging or computed tomography) of the head was performed in all patients in order to exclude other disorders. Medication overuse headache as dened by the IHS (34) was ruled out. Patients whose headache was related to previous neck trauma were also excluded (34). All patients had received several prophylactic drugs, but none of them was taking any migraine preventive at the time the study was performed. Ethical approval was granted by the Local Ethics Committee (URJC/FHA 028). Informed consent was obtained from all participants, and procedures were conducted according to the Declaration of Helsinki.
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Within the migraine group, evaluation was held when all patients were headache free and when at least 1 week had elapsed since the last migraine attack to avoid migraine-related allodynia (11,12). CTTH patients were examined on days in which headache intensity was < 4 points on a 10-cm horizontal visual analogue scale. Subjects were asked to take a prone position on an examination bed. The following 11 points according to Nie et al. (32) over the upper, middle and lower trapezius muscle, in both dominant and non-dominant sides, were marked with a wax pencil: (1) occiput: at the suboccipital muscle insertions; (2) cervical muscle: transverse process of C5; (3) cervical myotendinous spot: transverse process of C7; (4) upper trapezius: middle point between the spinous process of C7 and the acromion; (5) levator scapulae: 2 cm superior to the superior angle of the scapulae; (6) superior angle of the scapulae; (7) 1 cm medial to the acromion-clavicular joint; (8) supraspinatus: 3 cm superior to the middle of spina of the scapulae; (9) supraspinatus: 2 cm distal to the middle of spina of the scapulae; (10) middle trapezius: middle point of spinous process of T4 and medial border of spina scapulae; and (11) lower trapezius: middle point of spinous process of T6 and medial border of spina scapulae (Fig. 1).
2 4 8 7 9 6 5 10 11 3
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The examiner located the C7 spinous process by the following procedure. First, he palpated the most prominent spinous process (C6 or C7) at the base of the cervical spine. After it was identied, he passively exed and extended the lower cervical spine to verify which one moved rst: C6 vertebra should be more mobile, whereas C7 should demonstrate less motion.
Cephalalgia 30(1) 11 (55%) on the left. Headache attacks had typical features of migraine without aura, and were severe and incapacitating. Sixteen patients recalled a positive family history of migraine in rst-degree relatives. Migraine history was 12 years (95% CI 8.8, 15.3). All patients were classied as having episodic migriaine, since they reported two to three attacks per month (2.6 0.7 attacks/month).
Statistical analysis
Mean standard deviations (S.D.) or 95% condence interval (CI) are reported. A normal distribution of the data was assessed by means of the Kolmogorov Smirnov test. The intraclass correlation coecient (ICC) was used to assess intra-examiner reliability of PPT levels over each point. Multivariate analysis of variance (MANOVA) was applied to detect dierences in PPT levels with side (dominant or non-dominant, symptomatic or non-symptomatic) and assessed points (from 1 to 11) as within-subject variables and with group (CTTH, migraine, controls) as between-subject variable. StudentNewmanKeuls (SNK) test was used for pair-wise comparisons. Finally, the Pearson correlation test (r) test was used to analyse the association between PPT data and the clinical variables relating to pain (frequency, intensity, duration). Statistical analysis was conducted at a 95% condence level, and a P-value < 0.05 was considered to be statistically signicant.
ndez-de-las-Pen Ferna as et al. PPT levels over the lower part of the trapezius muscle (points 6, 911) were higher on the symptomatic side. Table 1 summarizes PPT values of each point for both sides (dominant or non-dominant, symptomatic or non-symptomatic) in all groups.
81 Pressure sensitivity and pain features in CTTH and unilateral migraine patients
Finally, signicant negative correlations between PPT data and several pain features were found: (i) within the migraine group between the frequency of attacks and PPT over point 1 (r 0.7; P < 0.001), point 5 (r 0.5; P 0.02) and point 8 (r 0.47; P 0.03) on the aected side; (ii) within the CTTH group between the duration of the headache and PPT levels over point 3 (r 0.6; P 0.01), point 6 (r 0.46; P 0.04), point 7 (r 0.48; P 0.04), point 9 (r 0.8; P < 0.001), point 10 (r 0.59; P 0.01), point 11 (r 0.72; P < 0.001) in both sides, and between headache intensity and PPT over point 2 (r 0.5; P 0.02). Thus, the greater the frequency of headache or the longer the headache duration, the lower was the PPT.
500 450 400 350 PPT (kPa) 300 250 200 150 100 50 0 0 1 2 3 4 # #
Discussion
5 6 7 8 Point number 9 10 11
Figure 2. Pressure pain thresholds (PPT) (average of both sides) for each point in both patient groups and healthy controls (data are expressed as mean and standard deviation). *Significantly lower PPT levels in both headache groups compared with healthy controls (P < 0.001). #Significantly lower PPT levels in points 1, 2 and 4 within the chronic tension-type headache (CTTH) group compared with both migraine and healthy controls (P < 0.001).
Our study has shown that the upper part of the trapezius muscle is the most pressure pain sensitive part in both headache patients and controls. Generalized lower PPT was found over the whole trapezius muscle in CTTH patients compared with both migraine and healthy controls. Furthermore, patients with strictly unilateral migraine had lower pain thresholds in the trapezius muscle than healthy controls. Finally, side-to-side dierences were also found in patients with strictly unilateral symptoms,
DOMINANT SIDE
NON-DOMINANT SIDE 380 360 340 320 300 280 260 240 220 200 180
Figure 3. Average pressure pain threshold maps for chronic tension-type headache patients. X represents the measured points.
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DOMINANT SIDE NON-DOMINANT SIDE 380 360 340 320 300 280 260 240 220 200 180
Cephalalgia 30(1)
Figure 4. Average pressure pain threshold maps for healthy controls. X represents the measured points.
NON-SYMPTOMATIC SIDE
SYMPTOMATIC SIDE 380 360 340 320 300 280 260 240 220 200 180
Figure 5. Average pressure pain threshold maps for unilateral migraine patients. X represents the measured points.
but not in patients with bilateral pain symptoms (CTTH). PPT recordings are recommended by the IHS classication (34) However, the classication of headache patients into subgroups is still not clearly related to possible pathophysiological mechanisms. PPT levels are considered a valuable clinical test for the evaluation of pericranial muscle sensitivity. Furthermore, we have demonstrated the utility of multiple site recordings for
PPT mapping, leading to a new imaging modality of muscle sensitivity to pain (22,23,33). The technique enables the detection and visualization of non-uniformity in muscle pain sensitivity as reported in headache and musculoskeletal pain (22,23,40). Our results support the relevance of assessing pressure pain sensitivity at multiple sites in the trapezius muscle in both CTTH and migraine patients. The existing neurophysiological and
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Table 1. Pressure pain thresholds of each point in either dominant (right) or non-dominant (left) sides within chronic tension-type headache, migraine and healthy controls Chronic tension-type headache Point 1* Point 2* Point 3* Point 4* Point 5* Point 6* Point 7* Point 8* Point 9* Point 10* Point 11* Left side Right side Left side Right side Left side Right side Left side Right side Left side Right side Left side Right side Left side Right side Left side Right side Left side Right side Left side Right side Left side Right side 164.6 33.1 172.3 38.5 172.4 33.3 183.1 45.5 297.6 62.7 298.9 59.7 246.3 58.5 257.5 56.9 286.8 55.7 293.6 62.1 313.3 53.8 319.3 42.3 303.9 57.5 310.2 41.5 290.8 51.7 297.1 56.8 333.7 48.9 338.3 55.1 322.3 43.1 326.8 31.6 338.8 58.9 355.6 49.7 Strictly unilateral migraine Symptomatic side Non-symptomatic Symptomatic side Non-symptomatic Symptomatic side Non-symptomatic Symptomatic side Non-symptomatic Symptomatic side Non-symptomatic Symptomatic side Non-symptomatic Symptomatic side Non-symptomatic Symptomatic side Non-symptomatic Symptomatic side Non-symptomatic Symptomatic side Non-symptomatic Symptomatic side Non-symptomatic 240.3 50.5 253.5 54.1 210.2 36.1 228.8 57.4 265.1 55.5 290.5 50.9 276.1 53.4 287.1 84.3 289.3 40.7 295.2 58.9 324.5 34.3 306.8 68.5 291.6 58.1 316.7 65.6 271.7 49.2 301.9 63.2 332.8 52.4 315.2 52.8 332.9 44.9 316.4 43.7 334.7 25.8 318.9 37.4 Control group Left side Right side Left side Right side Left side Right side Left side Right side Left side Right side Left side Right side Left side Right side Left side Right side Left side Right side Left side Right side Left side Right side 333.2 42.8 344.3 41.4 332.2 38.5 338.4 41.2 358.6 29.3 382.1 37.1 337.3 31.1 338.3 29.9 333.1 19.3 357.1 27.7 343.1 22.8 357.3 36.7 350.3 23.4 370.8 30.7 343.7 33.1 350.7 28.1 358.6 30.9 362.5 17.2 339.7 27.9 328.6 19.7 353.1 38.1 350.5 30.4
side side side side side side side side side side side
Pressure pain thresholds are expressed as means standard deviation (kPa). *Significant differences between patients and controls.
morphological evidence of convergence from cervical sensory and muscle aerent inputs onto trigeminal sub-nucleus caudalis nociceptive and non-nociceptive neurons is considered an explanation for the phenomenon of cervical-to-trigeminal and trigeminal-tocervical pain referral commonly seen clinically. Therefore, our data support the relevance of cervical aerence in both CTTH and unilateral migraine patients and point towards a general hyperalgesia of neck-shoulder muscles in headache patients, particularly in CTTH. The fact that work-related neckshoulder pain is accompanied by headache (25,41) underlines these convergence mechanisms, making muscle pain one possible cause or eect of headache (42). Nevertheless, our results can also be explained in the opposite way, i.e. trigeminal aerence may be also relevant for the sensitization of cervical muscles. Nie et al. found increased mechanical pain sensitivity of muscle belly locations of the trapezius muscle compared with the pressure pain sensitivity of musculo-tendinous junctions after the induction of delayed onset muscle soreness (32), indicating that changes of mechanical pain sensitivity are not
uniform over this trapezius region, in line with our ndings in headache patients. This could be due to a dierent distribution of muscle nociceptors between the dierent subdivisions of the trapezius muscle. In addition, we also found bilateral topographical maps of the trapezius muscle in both CTTH and healthy controls, but only side-to-side dierences in unilateral migraine. These results agree with those previously reported for the temporalis muscle in CTTH (22), but not in strictly unilateral migraine (23). In our previous study we found bilateral pressure hyperalgesia in the temporalis muscle in patients with strictly unilateral pain symptoms (23). However, pressure maps in the trapezius muscle were not symmetrical in unilateral migraine. It may be that sensitization of central pathways (7) accounts for bilateral hyperalgesia (43) in the trigeminal-related region (temporalis muscle), but not in the cervical-related region (upper trapezius) in unilateral pain headache. In agreement with that, side-to-side dierences in pain sensitivity and tenderness over the upper trapezius, but not the temporalis, muscle were found in a cohort of 25 patients with unilateral migraine (21). Further
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studies investigating dierent pressure pain sensitivity topographical maps between muscles with trigeminal or cervical innervations should be conducted. Moreover, these investigations on muscle pain hyperalgesia should not be limited to a particular point, since the topographical distribution of pressure maps diers throughout the same muscle in headache and musculoskeletal pain (22,23,32,40). Olesen has proposed that perceived headache intensity could be the sum of the nociceptive barrage from cranial and extracranial peripheral tissues converging on the neurons of the trigeminal nucleus caudalis (44). Burstein suggested that hyperalgesic and allodynic responses in migraine are due to the development of central sensitization involving second-order neurons in the trigeminal nucleus and at least third-order neurons in the thalamus (45). The existence of central sensitization mechanisms in local pain syndromes may suggest that sustained peripheral noxious input to the central nervous system plays a role in the initiation and maintenance of central sensitization. In the current study, PPT levels over the trapezius muscle were negatively associated with some clinical pain features. These results support a role of muscle peripheral sensitization mechanisms in the initiation and maintenance of central sensitization (8). In fact, increased recruitment of central neurons by peripheral nociceptive stimulus (46), enhanced spatial summation (47) and spatial referral (i.e. tonic nociceptive input from local tissue can result in pain in remote areas and increase pain intensity (48)) have been suggested to be the potential peripheral mechanisms. Furthermore, it seems that hyperexcitability of the central nervous system is a dynamic condition and inuenced by the activity and location of peripheral nociceptive inputs (49). Therefore, prolonged nociceptive inputs from nontrigeminal, but cervical, innervated tissues (upper trapezius muscle) may result in spatial summation (50), increasing pain perception, mechanical pain hypersensitivity and the intensity of headache. In the present study we found a generalized increased hypersensitivity expressed by lower PPT in the trapezius muscle (including the asymptomatic lower part of the muscle) in both CTTH and migraine. Our ndings support the role of central sensitization mechanism in CTTH. Nevertheless, our patients with strictly unilateral migraine were classied as episodic, so current ndings in episodic migraine may result from a general putative dysfunction in sensory processing and pain control system, i.e. abnormal habituation in multimodal cortical evoked potential and cutaneous allodynia during attacks (51). Moreover, the observed spatial dierences in PPT levels provide some evidence of dierent pathogenic factors underlying CTTH and unilateral migraine. Nevertheless, CTTH and migraine
Cephalalgia 30(1) patients reported neck-shoulder pain, but the pain intensity and spreading was not assessed in the present study. Thus, pain in the neck-shoulder region could be the sole factor responsible for the general hyperalgesia in the trapezius muscle. However, it is most likely that convergence mechanisms from trigeminal and cervical aerents play a role in hyperalgesia observed in the temporalis muscle and trapezius muscles in CTTH and migraine patients (22,23). Population-based epidemiological studies with larger samples are needed for a more generalized interpretation of these results. Furthermore, during face-to-face interview none of the included patients seemed to have psychiatric or depression symptoms; however, since pressure pain sensitivity can be inuenced by depression or anxiety, specic questionnaires could have been used. Finally, we have described the spatial distribution of pressure pain sensitivity only in patients with unilateral migraine or CTTH. Assessment of pressure pain sensitivity maps in other headache disorders, e.g. trigeminal autonomic cephalalgias, and in both genders, may expand current knowledge about the state of nociception in headaches.
Conclusions
CTTH and migraine patients have generalized lower PPT levels in the trapezius muscle region compared with controls. CTTH patients also have lower PPTs in the trapezius muscle than migraine subjects. The topographical pressure pain map revealed that the upper part of the trapezius muscle is the most sensitive part of the muscle in both patients and controls. Finally, side-to-side dierences were also found in patients with strictly unilateral migraine, but not in patients with CTTH. The present study supports the implication of cervical aerences in headache conditions.
Acknowledgements
This study received funds from a grand conceded by the Universidad Rey Juan Carlos and Comunidad de Madrid (reference CCG07-URJC/BIO-1420).
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