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Analysis of the cranio-cervical curvatures in subjects with migraine with and without neck pain
Accepted Manuscript Title: ANALYSIS OF THE CRANIO-CERVICAL CURVATURES IN SUBJECTS WITH MIGRAINE WITH AND WITHOUT NECK PAIN Authors: Gabriela Nat´alia Ferracini, Thais Cristina Chaves, Fab´ıola Dach, D´ebora Bevilaqua-Grossi, C´esar Fern´andez-de-las-Pe˜nas, Jos´e Geraldo Speciali PII: DOI: Reference:
S0031-9406(17)30026-3 http://dx.doi.org/doi:10.1016/j.physio.2017.03.004 PHYST 961
To appear in:
Physiotherapy
Please cite this article as: Ferracini Gabriela Nat´alia, Chaves Thais Cristina, Dach Fab´ıola, Bevilaqua-Grossi D´ebora, Fern´andez-de-las-Pe˜nas C´esar, Speciali Jos´e Geraldo.ANALYSIS OF THE CRANIO-CERVICAL CURVATURES IN SUBJECTS WITH MIGRAINE WITH AND WITHOUT NECK PAIN.Physiotherapy http://dx.doi.org/10.1016/j.physio.2017.03.004 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
1
ANALYSIS
OF
THE
CRANIO-CERVICAL
CURVATURES
IN
SUBJECTS WITH MIGRAINE WITH AND WITHOUT NECK PAIN
Gabriela Natália Ferracinia* MD, Thais Cristina Chavesb PhD, Fabíola Dachc PhD, Débora Bevilaqua-Grossid PhD, César Fernández-de-las-Peñase PhD, José Geraldo Specialif PhD.
1. *Doctoral Student, Department of Neurosciences and Behavioral Sciences/Faculty of Medicine of RibeirãoPreto, University of São Paulo – FMRP-USP. Ribeirão Preto, São Paulo, Brazil.
2. Professor, Department of Neurosciences and Behavioral Sciences/Faculty of Medicine of Ribeirão Preto, University of São Paulo – FMRP-USP/Postgraduate Program of Rehabilitation and Functional Performance. Ribeirão Preto, São Paulo, Brazil.
3. Professor, Department of Neurosciences and Behavioral Sciences/Faculty of Medicine of RibeirãoPreto, University of São Paulo – FMRP-USP/Responsible for the Headache and Craniofacial Pain Outpatient Clinic, University Hospital, Faculty of Medicine of Ribeirão Preto, Ribeirão Preto, São Paulo, Brazil.
4. Professor, Department of Neurosciences and Behavioral Sciences/Faculty of Medicine of Ribeirão Preto, University of São Paulo – FMRP-USP/Postgraduate Program of Rehabilitation and Functional Performance. Ribeirão Preto, São Paulo, Brazil.
5. Professor, Department of Physical Therapy, Occupational Therapy, Physical Medicine and Rehabilitation of Rey Juan Carlos University, Alcorcón, Spain
6. Senior Professor, Department of Neurosciences and Behavioral Sciences/Faculty of
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Medicine of Ribeirão Preto, University of São Paulo – FMRP-USP. Ribeirão Preto, São Paulo, Brazil.
*Adress correspondece and reprint requests to: Gabriela Natália Ferracini. Department of Neurosciences and Behavioral Sciences. Faculty of Medicine of Ribeirão Preto, University of São Paulo. Avenida dos Bandeirantes, 3900 - 14048-900. Ribeirão Preto, SP, Brasil. Tel: +55 16 99750-8011
ABSTRACT Objective: To investigate the differences in head and cervical spine alignment between subjects with migraine and healthy people. Design: A cross-sectional, observational, study. Participants: Fifty subjects with migraine and 50 matched healthy controls participated. Main outcomes measures: The presence of neck pain and neck pain-related disability was assessed. Four angles (high cervical angle; low cervical angle; atlas plane angle, and cervical lordosis Cobb angle) as well as 4 distances (anterior translation distance; C0-C1 distance; C2-C7 posterior translation, and hyoid triangle) were calculated using digitalized radiographs and analyzed using the K-Pacs® software. Results: Subjects with migraine reported a longer history of neck pain symptoms, and higher pain intensity and neck painrelated disability than controls (P<0.01). Patients exhibited a smaller anterior translation distance (mean difference: 4.9mm, 95%CI 1.8-8.8; P<0.001) and hyoid triangle (difference: 3.0mm, 95% CI 1.0-5.0; P=0.02) than healthy controls. When the presence or the absence of neck pain was included in the analysis, the differences did not change. Differences in anterior translation and hyoid triangle distances were considered clinically relevant for subjects with migraine suffering from neck pain. Conclusion: Subjects with migraine
3
exhibited straightening of cervical lordosis curvature. The presence of neck pain did not influence head posture in subjects with and without migraine.
Keywords: Migraine. Neck. Radiograph. Posture.
INTRODUCTION Migraine is a common and chronic disabling disease. The prevalence ranges from 10 to 12% in the general population [1-3]. Approximately 90% of subjects with migraine report functional disability and about one third require rest during the head pain attacks [4]. Postural changes are commonly observed in subjects suffering from head pain, particularly those with primary headaches (migraine or tension-type headache). The most frequent cranio-cervical postural abnormality is the forward head posture (FHP) [5]. A FHP consists of a reduction of the cranio-cervical angle which is the degree of head extension in relation to the upper cervical spine, and implies that the head is anterior to a theoretical line passing through the center of gravity of the body [5]. However, there are other postural changes that could affect the cervical spine, e.g., a reduction or an increase of physiological cervical lordosis [6,7] which have not been investigated in primary headache populations. Postural changes can be evaluated by visual inspection and also documented photographically permitting a noninvasive and low-cost qualitative analysis method [8,9]. Different studies have investigated the presence of FHP with photographs in subjects with migraine [10,11] or tension type headache [12,13] and reported that subjects with headache exhibit greater FHP. Nevertheless, this qualitative evaluation
4
is not able to reproduce all curvatures of the cervical spine [7,14]. In such a scenario, radiographic examination is another method of postural evaluation which permits the assessment of cervical spine curvatures; take out however, although it is considered the gold standard to assess the spine curvatures [15], it also includes exposure to radiation [16]. A few studies have investigated the association of head and cervical spine posture and migraine, and the results are inconclusive. For instance, Fernández-delas-Peñas et al (2006) [10] and Ferreira et al (2014) [11] observed greater FHP in subjects with unilateral migraine. On the contrary, Zito et al (2006) and Ferracini et al (2015) [17,18] did not find such FHP in subjects with migraine in relation to healthy controls. To the best of the author’s knowledge, no study has previously investigated head/cervical spine posture by radiographic assessment in subjects with migraine. Therefore, the objective of our study was to investigate differences in the alignment of the head and the cervical spine between subjects with migraine and healthy people by using radiographic assessment. We hypothesized that subjects suffering from migraine will exhibit greater head and cervical spine postural misalignments than subjects without migraine.
MATERIALS AND METHODS Design A cross-sectional, observational study was conducted. All participants read and signed a consent form prior to enrollment. The study was approved by local ethics board of the XXXXXXXXX (Process15821-2011). Participants
5
Consecutive subjects with migraine attending a tertiary outpatient clinic were screened for eligibility criteria. Migraine was diagnosed according to the International Headache Society criteria by experienced neurologists (ICHD-II, 2004) [19]. Key element of headache history including family history, headache features, temporal profile, and current and past medications were considered. Participants were excluded if they exhibited; (1) other primary headache; (2) history of cervical injury; (3) cervical disc herniation; (4) medication overuse headache; (5) any systemic medical comorbidity, e.g. fibromyalgia or rheumatoid arthritis; (6) history who had not experienced any head pain; (7) those subjects who had received nerve blockade during the last 6 months; or, (8) subjects who had received physiotherapy for the neck/shoulder region in the previous 12 months. In addition, age- and sex-matched healthy subjects without headache history in the previous 6 months were also recruited. Clinical Outcomes In addition to demographic and anthropometric data, clinical headache outcomes including disease duration (years), frequency and duration of migraine, predominant head pain laterality, presence of self-reported neck pain, and intensity of migraine attacks during the last 3 months were assessed. Pain intensity at the time of evaluation was assessed using a numerical pain rate scale (NPRS where 0: absence of pain; 10: the worst pain experienced) [20]. Disability related to neck pain was determined with the Neck Disability Index (NDI) [21]. The NDI includes 10 questions related to the effects of neck pain on everyday activities, pain and concentration. The score corresponds to the sum of the points for each question (0-5), with 50 points as the maximum. Radiographic Outcomes
6
For the radiographic assessment, subjects were in a relaxed standing position, with both upper extremities along the body and both feet together. They were instructed to look at the horizon, and then take a comfortable neutral position of the head [22]. The distance between X-ray equipment and photographic film was standardized at 180 cm following international guidelines. The radiology technician was blinded to participant’s condition. Four cervical angles and four neck distances were measured in the digitalized radiographs and analyzed using the K-Pacs® software (Figure 1): 1. High cervical angle (HCA): This angle is formed by the McGregor plane (from the posterior nasal spine to the more inferior surface of the occipital line) and the plane of the odontoid process (line from C2 vertebrae axis to the most anteriorposterior point of C2). The intersection of these 2 tracings forms an angle that measures the degree of head extension in relation to the upper cervical spine (Fig. 1.6): the smaller the angle, the greater the head extension on the cervical spine [6]. 2. Low cervical angle (LCA): It is formed by a straight line tangent to the C3-C4 vertebral bodies through two distinct points, the highest point on the posterior C3 vertebral body and the most inferior point on the posterior surface of the C4 vertebral body (Fig. 1.5). The intersection on these 2 lines forms an angle that indicates the relationship between the high and low cervical spine: the greater the angle, the greater the cervical lordosis and the greater the extension of the upper cervical spine on the inferior part of the cervical spine [6]. 3. Atlas plane angle (APA): This angle represents the plane of the atlas vertebra (C1) with the tracing formed between a line parallel to horizontal and by another line traced in the inferior part of the posterior arc of the atlas (Fig. 1.2). An increase in
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this angle suggests an increased extension of the upper cervical spine, particularly atlas (C1) extension [23]. 4. Cervical lordosis Cobb angle (Cobb A): Formed by the intersection of the lines of the plane of the superior vertebral plateau of C7 vertebra and of the inferior plateau of C2 (Fig. 1.4). This angle is a measure of the lordosis of the cervical spine [8]. 5. Anterior translation distance (ATD): The tracing is formed by the distance between posterior-superior margin of the C2 body and a vertical line perpendicular to the inferior margin of C7 vertebra body (Fig. 1.7). This measurement is important in determining the anterior head transposition [8]. 6. C0-C1 distance (C0-C1D): Consists of the measurement from the most inferior point of the base of the occipital bone to the posterior arc of C1 [24] (Fig. 1.1). 7. C2-C7 posterior translation (C2-C7PT): It is formed by posterior vertebral body tangents from C2 to C7 vertebrae (Fig. 1.3). It measures the lordosis of the cervical spine [6]. 8. Hyoid triangle (HT): It is the distance between the most anterior-superior point of the hyoid bone and the H line (formed by the most anterior-inferior point of C3 vertebra and the most posterior-inferior point of the chin) [24] (Fig. 1.8). Three measurements of each angle were assessed in all radiographies and the mean was used for the analysis. Intra-examiner reliability was determined using 10 radiographs randomly selected. Two different measurements of each angle were conducted with 7 days of distance. Sample size calculation The sample size determination was conducted with an appropriate software (Tamaño de la Muestra 1.1©, Barcelona, Spain). The sample size was based on detecting between-groups difference of 10º in radiographic outcomes with an alpha
8
level of 0.05 and a desired power of 80%. This generated a sample size of at least 35 participants per group.
Data Analysis The statistical analysis was conducted using SPSS statistical software, version 18.0. Mean and standard deviation were calculated for each variable, whereas mean and 95% confidence intervals (95%CI) were calculated for between-group difference scores. Intra-examiner reliability was determined by calculating intra-class correlation coefficients [ICC], Bland and Altman mean bias and limits of agreement [25]. The Kolmogorov-Smirnov test revealed a normal distribution of quantitative outcomes (P>0.05), therefore parametric tests were applied. First, student t-test (2tailed) for independent samples was used to determine the differences in angles and planes between subjects with migraine and controls. Second, an analysis of variance (ANOVA) with Bonferroni as post hoc analysis was used to compare the values of the angles and planes between groups considering the presence or absence of neck pain (migraine and healthy controls with or without neck pain). Effect sizes (ES) were calculated and classified as small when 0.20 (0-0.39), moderate when 0.50 (0.4-0.79), and high when >0.80 (Cohen, 1988). Finally, the minimal important difference (MID) and standard error of measurement (SEM) were also calculated [25]. Clinical relevance was classified according to Armijo-Olivo et al (2011) [26]: (1) when ES was > 0.40 (moderate ES) and the mean difference between groups was higher than both MIDs; (2) potential clinical relevance (PCR): moderate ES and
9
a mean difference higher than one of the MIDs; or small/moderate E S and the mean difference was higher than both MIDs; and (3) not clinically relevant (NCR) where there was a small ES and a mean difference lower than one of the MID. The statistical analysis was conducted at a 95% confidence level, and a Pvalue less than 0.05 was considered statistically significant. RESULTS Six hundred and sixty-two potential participants were screened for inclusion criteria between December 2012 and January 2014. Six hundred and twelve (n=612) subjects were excluded for the following reasons: other primary headaches (n=360), refused to participate (n=24), systemic medical comorbidities (n= 226) and 2 were selected and participated but their radiology images were poor to obtain accurate readings. Finally, 50 subjects, 45 women and 5 men, aged from 18 to 55 years (mean: 34 years), with migraine satisfied all eligibility criteria, agreed to participate and signed the informed consent. Further, 50 age- and sex- matched controls were also recruited. No significant differences in demographic variables were observed between the groups (Table 1). A greater number of subjects with migraine compared with healthy controls reported neck pain (P<0.001). Subjects with migraine exhibited a higher intensity of neck pain and neck pain-related disability than healthy controls (P<0.01, Table 1). Intra-examiner reliability (ICC) ranged from good to excellent and is presented in the Table 2. The radiographic analyses of cranio-cervical posture of subjects with and without migraine are presented in Table 3. The student t-test revealed significant differences for ATD (P<0.001) and HT (P=0.02) distances between subjects with migraine and healthy people: distances were smaller in subjects with migraine than
10
in controls (Table 3). The size of differences could be considered potentially clinically relevant (Armijo et al., 2011) (Table 4). When the presence/absence of neck pain was included, the ANOVA revealed significant differences for HT distance (F=3.42; P=0.02) and ATD (F=4.67; P<0.001). Pos hoc analysis revealed that subjects with migraine suffering neck pain exhibited smaller ATD (P=0.005) and HT (P=0.01) distances than controls with or without neck pain (Table 5). Table 6 shows that differences in both ATD and HT distances were clinically relevant between subjects with migraine and neck pain compared to healthy controls without neck pain. Additionally, differences in HT distance between subjects with migraine with and without neck pain, and differences in ATD distance between migraine subjects with neck pain and controls with neck pain were also clinically relevant (Table 6).
DISCUSSION The current study found that subjects with migraine exhibited 2 major postural changes including smaller ATD and HT distances. These results were not associated with the presence of neck pain symptom. Current findings suggest that migraine may be associated with a straightening of the cervical lordosis curvature rather than changes in cranio-cervical extension. To the best of our knowledge this is the first study investigating cervical postural changes in subjects with migraine by means of radiographic examination. Previous studies using photographic assessments found that subjects with migraine [10,11] or chronic tension type headache [12,13} exhibited greater FHP, i.e., smaller cranio-vertebral angle. However, Zito et al (2006) [17] and Ferracini et al (2015) [18]
11
did not find differences in FHP between migraine and healthy controls. Our findings and previous finding suggest that FHP is not present in subjects with migraine compared to women with no history of headache in 2 postural analyses (radiographic and photographic) [18]. Our study revealed that subjects with migraine exhibited a straightening of the cervical lordosis instead of a FHP. Discrepancies in postural changes observed may be related to the use of different outcomes. Gadotti et al (2013) [27] suggested that the photographs can be used as a clinical method for assessing the cranio-vertebral angle, i.e., FHP, in clinical setting; however, for proper assessment of the cervical lordosis the use of radiographic assessment is highly recommended. To determine potential reasons why subjects with migraine exhibited a loss of the physiological cervical lordosis is beyond the scope of this study; however, the clinical implications of these findings should be considered. For instance, the loss of the physiological cervical lordosis may result in changes in biomechanical force distribution both at vertebral and soft tissue levels [13,28]. Changes can include an overload on cervical structures e.g., ligaments, joints and discs, and muscle imbalances, i.e., activation and strength deficits [29] or myofascial trigger points [10]. These muscle imbalances can stimulate nociceptors, mechanoreceptors and proprioceptors at the cervical spine possibly leading to an activation of the trigeminocervical nucleus caudalis [29]. This could potentially result in postural changes of the cervical spine which may perpetuate migraine attacks; or vice versa, migraine attacks could also promote the chronification of neck disturbances. An interesting finding was that the presence of neck pain in either subjects with migraine and healthy controls did not influence the results. It is possible that the small number of healthy subjects from our sample reporting neck pain symptoms
12
may explain the lack of association. On the contrary, the prevalence of neck pain in subjects with migraine and other primary headaches has frequently been reported [30-33]. Our results showed a prevalence of 78% of subjects reporting neck pain within our migraine group, which is similar to recent published data [33]. It is possible that increased tension of the cervical musculature during migraine attacks can increase the risk of subsequent occurrence of migraine as a predictive factor for its onset [34]; however, the design of the current study does not permit us to determine any potential predictive factor. Although strengths of our study include a careful analysis of postural changes in the cranio-cervical region by radiographic examination considering both statistical and clinical viewpoints; there are also some potential limitations. First, subjects were recruited from a tertiary care hospital; therefore, it is possible that they represent a specific group of the general population with migraine. In fact, the presence of neck pain in our sample of healthy people suggests that extrapolation of our results should be conducted with caution at this stage. Second, the cross-sectional nature of the study does not permit us to establish a cause and effect relationship. Third, we did not include other relevant clinical outcomes, e.g., disability-related to migraine with maybe also related to postural changes. Fourth, the clinical relevance of postural changes in the cervical spine remains to be elucidated. Future population studies including large sample size of subjects with migraine and other co-morbid conditions are needed to further determine the presence of postural changes in the cervical spine and their clinical relevance in subjects with migraine.
CONCLUSIONS
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Our results revealed that subjects with migraine exhibited straightening of the cervical lordosis curvature, that is, reduced ATD and HT distances, when assessed with radiographs. The presence of neck pain did not influence the results for people without migraine. Current results should be considered with caution at this stage due to the limitation in generalizability of the results.
Funding: This study was funded by Fundação de Amparo à pesquisa do estado de São Paulo (FAPESP).
Disclosure of interests: All authors have no conflicts of interest to declare.
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24. Headache Classification Subcommittee of the Inter- national Headache Society. The International Classifications of Headache Disorders, 2nd ed. Cephalalgia. 2004;24:9-160. 25. Bolton JE, Wilkinson CR. Responsiveness of pain scales: A comparison of three pain intensity measures in chiropractic patients. J Manipulative Physiol Ther 1988; 21:1-7. 26. Cook C, Richardson JK, Braga L, et al. Cross-cultural adaptation and validation of the Brazilian Portuguese version of the Neck Disability Index and Neck Pain and Disability Scale. Spine 2006; 31: 1621-7. 27. Garrett TR, Youdas JW, Madson TJ. Reliability of measuring forward head posture in a clinical setting. J Orthop Sports Phys Ther 1993; 17: 155-60. 28. Huggare JAV, Rautia A. Head posture and cervicovertebral and craniofacial morphology in patients with craniomandibular dysfunction. J Craniomand Pract 1992; 10: 435-40. 29. Rocabado M, Tapia V. Estúdio radiográfico de relación craneocervical em pacientes bajo tratamiento ortodóncio y su incidencia com sintomas referidos. Ortodonxia 1994; 8: 59-63. 30. Cohen J. The concepts of power analysis. In: Cohen J, editor. Statistical power analysis for the behavioral sciences. Hillsdale, New Jersey: Academic Press, Inc; 1988. p. 1-17. 31. Armijo-Olivo S, Warren S, Fuentes J, et al. Clinical relevance vs. statistical significance: Using neck outcomes in patients with temporomandibular disorders as an example. Man Ther 2011; 16: 563-72.
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32. Gadotti I, Armijo-Olivo S, Silveira A, et al. Reliability of the cranio-cervical posture assessment: visual and angular measurements using photographs and radiographs. J Manipulative Physiol Ther 2013; 36: 619-25. 33. Harrison DE, Jones WE, Janik TJ, et al. Evaluation of axial and flexural stresses in the vertebral body cortex and trabecular bone in lordosis and two sagittal cervical translation configurations with an elliptical shell model. J Manipulative Physiol Ther 2002; 26: 391-401. 34. Jull G, Amiri M, Bullock-Saxton J, et al. Cervical musculoskeletal impairment in frequent intermittent headache. Part 1: Subjects with single headaches. Cephalalgia 2007; 27: 793-802. 35. Wober C, Brannath W, Schmidt K, et al. Prospective analysis of factors related to migraine attacks: The PAMINA study. Cephalalgia. 2007; 27: 304314. 36. Calhoun AH, Ford S, Millen C, et al. The prevalence of neck pain in migraine. Headache 2010; 50: 1273-1277. 37. Plesh O, Adams SH, Gansky SA. Self-reported comorbid pains in severe headaches or migraines in a US national sample. Headache 2012; 52: 946956. 38. Ashina S, Bendtsen L, Lyngberg AC, et al. Prevalence of neck pain in migraine and tension-type headache: A population study. Cephalalgia. 2014 May 22. ii: 0333102414535110. [Epub ahead of print]. 39. Ferracini GN, Chaves TC, Dach F, Bevilaqua-Grossi D, Fernández-de-lasPeñas C, Speciali JG. Cervico-occipital posture in women with migraine: A case control study. J Orthop Sports Phys Ther 2015 (in press).
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40. Blaschek A, Decke S, Albers L. Self-reported neck pain is associated with migraine but not with tension-type headache in adolescents. Cephalalgia 2014;34: 895-903.
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Figure 1: Illustrative diagram of the radiographic measurements.
Legend: C0-C1 distance; (2) atlas plane angle; (3) C2-C7 posterior translation; (4) Cobb cervical spine angle; (5) low cervical angle; (6) high cervical angle; (7) anterior translation distance; (8) hyoid
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Table 1: Clinical and demographic characteristics of patients with migraine and healthy controls Migraine (n=50)
Controls (n=50)
P
Sex (F/M)
45/5
45/5
0.99
Age (years)
34.1 (10.8)
33.7 (11.8)
0.85
Disease duration (years)
17.4 (12.3)
-
-
Headache Intensity - last 3 months
7.5 (1.7)
-
-
Headache intensity - time of evaluation (n=27)
5.4 (2.6)
-
-
Frequency of headache (days/month)
12.0 (9.7)
-
-
Duration of headache (hours per crisis)
18.1 (11.2)
-
-
Cervical Pain
78%
18%
<0.001*
Sex (F/M)
38/1
8/1
<0.002*
Duration of pain (years)
6.9 (1.2)
4.8 (1.4)
<0.001*
Intensity
4.9 (0.5)
1.4 (0.4)
<0.001*
Disability scores (NDI)
11.8 (1.0)
4.5 (1.4)
<0.001*
Data are expressed as mean (standard deviation) otherwise is advised F: female; M: male; BMI: body mass index; NPRS: numeric pain rate scale; NDI: neck disability index * Significant differences between patients and controls (Student t-test).
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Table 2: Intra-examiner reliability for radiographic angles and distances Angles and distances
ICC (95%CI)
Bland and Altman mean bias (limits of agreement)
HCA (°)
0.88 (0.52 - 0.97)
0.5 (-1.2, 2.4)
LCA (°)
0.97 (0.91 - 0.99)
0.1 (-0.3, 0.5)
APA (°)
0.90 (0.61 - 0.97)
0.3 (-0.2, 0.8)
C2-C7 PT (°)
0.96 (0.84 - 0.99)
0.5 (-2.1, 3.1)
Cobb A (°)
0.93 (0.73 - 0.98)
1.3 (-0.2, 2.8)
C0-C1D (mm)
0.97 (0.90 - 0.99)
0.05 (-0.8, 0.9)
ATD (mm)
0.97 (0.88 - 0.99)
0.7 (-1.3, 2.7)
HT (mm)
0.94 (0.92 - 0.99)
0.03 (-0.3, 0.4)
HCA: high cervical angle; LCA: low cervical angle; APA: atlas plane angle; C2-C7 PT: posterior tangent C2-C7; Cobb A: Cobb angle for the cervical spine; C0-C1D: C0-C1 distance; ATD: anterior translation distance; HT: hyoid triangle. ICC: intra-class correlation coefficient; CI: confidence interval.
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Table 3: Mean values and between-groups differences of angles (°) and distances (mm) for migraine and control groups
Angles and distances
Migraine
Healthy control
Mean Difference
HCA (°)
66.8 (5.3)
67.3 (5.5)
-0.5 (-2.5, 1.5)
LCA (°)
9.4 (5.2)
10.2 (6.6)
-0.8 (-3.1, 1.5)
APA (°)
16.7 (6.8)
15.5 (7.1)
1.2 (-1.5, 3.9)
C2-C7 PT (°)
14.8 (7.2)
12.0 (6.3)
2.8 (-0.5, 6.1)
Cobb A (°)
32.4 (9.2)
31.8 (8.3)
0.6 (-2.6, 3.8)
C0-C1D (mm)
8.5 (3.4)
8.5 (3.7)
0.0 (-1.2, 1.2)
ATD (mm)
14.4 (6.8)*
19.3 (6.4)
-4.9 (-8.8, -1.8)*
HT (mm)
3.1 (2.3)*
6.1 (3.8)
-3.0 (-1.0, -5.0)*
HCA: high cervical angle; LCA: low cervical angle; APA: atlas plane angle; C2-C7 PT: posterior tangent C2-C7; Cobb A: Cobb angle for the cervical spine; C0-C1D: C0-C1 distance; ATD: anterior translation distance; HT: hyoid triangle. Data are expressed as means (standard deviation) for group data and as means (95% confidence interval) for between-groups differences * Significant differences between patients and controls (student t-test, P<0.05)
23
Table 4: Mean between-groups difference score, standard error of the mean (SEM), effect size and minimum important difference (MID) of angles (°) and distances (mm) between patients with migraine and healthy controls Angles
Mean difference
Effect size
MID (0.2)
MID (0.5)
SEM
HCA (°)
-0.5
-0.09
1.10
2.77
1.91
LCA (°)
-0.8
-0.14
1.22
3.07
1.06
APA (°)
1.2
0.14
1.69
4.23
2.25
C2-C7 PT (°)
2.8
0.33(SES)
1.65 (PCR)
3.33
2.80
Cobb A (°)
0.6
0.04
2.45
6.14
2.00
C0-C1D (mm)
0.0
0.00
0.74
1.87
0.65
ATD (mm)
-4.9*
-0.41(MES)
2.32 (PCR)
5.82
1.59
HT (mm)
-3.0*
-0.48(MES)
1.28 (PCR)
3.20
0.93
distances
MID: minimal important difference; SEM: standard error of the mean; HCA: high cervical angle; LCA: low cervical angle; APA: atlas plane angle; Cobb A: Cobb angle for the cervical spine; C2-C7 PT: posterior tangent C2-C7; C0-C1D: C0-C1 distance; ATD: anterior translation distance; HT: hyoid triangle; MES: moderate effect size; PCR: potentially clinically relevant
24
Table 5: Mean and standard deviation (SD) of angles (°) and distances (mm) for patients with migraine and healthy controls by the presence or absence of neck pain Angles
MGNP
CGNP
CGWONP
(n=10)
(n=40)
MGWONP (n=11) and distances
(n=39)
HCA (°)
67.3 (5.4)
65.0 (5.2)
67.0 (5.9)
67.4 (5.4)
LCA (°)
9.5 (5.2)
8.7 (5.3)
9.7 (6.0)
10.4 (6.5)
APA (°)
16.7 (6.8)
17.4 (7.2)
15.0 (5.8)
15.6 (6.2)
C2-C7 PT (°)
14.3 (7.4)
16.5 (7.5)
12.9 (8.6)
12.6 (7.9)
Cobb A (°)
32.3 (8.0)
32.3 (7.9)
35.0 (8.2)
31.0 (8.4)
C0-C1D (mm)
8.8 (3.6)
7.6 (3.7)
7.4 (4.7)
8.8 (3.4)
ATD (mm)
12.0 (7.3)
13.5 (7.8)
19.9 (8.9)*
19.1 (8.5)*
HT (mm)
2.4 (2.3)
5.6 (4.6)
3.4 (4.4)
6.8 (4.7)*
MGNP: migraine group with neck pain, MGWONP: migraine group without neck pain; CGNP: control group with neck pain; CGWONP: control group without neck pain; HCA: high cervical angle, LCA: low cervical angle, APA: atlas plane angle; C2-C7 PT: posterior tangent C2C7; Cobb A: Cobb angle for the cervical spine; C0 - C1D: C0- C1 distance; ATD: anterior translation distance; HT: hyoid triangle.
* Significant difference between migraine patients with neck pain and control group (ANOVA, P<0.05 Bonferroni post hoc)
25
Table 6: Mean (95% confidence interval) of between-groups difference and minimum important difference of angles (°) and distances (mm) for patients with migraine and healthy controls by the presence/absence of neck pain
Mean difference Angles/distances
MID (0.2)
MID (0.5)
(MGNP- MGWONP) HCA (°)
2.3 (-1.6, 6.2)
1.08 (PCR)
2.70 (NCR)
LCA (°)
0.8 (-3.1, 4.7)
1.11 (NCR)
2.77
APA (°)
-0.7 (-2.0, 0.6)
1.41 (NCR)
3.53
C2-C7 PT (°)
-2.2 (-5.1, 0.7)
1.70 (NCR)
4.25
Cobb A (°)
0.0 (-5.1, 5.1)
1.57 (NCR)
5.93
C0-C1D (mm)
1.2 (-1.5, 3.9)
0.68 (PCR)
1.70 (NCR)
ATD (mm)
-1.5 (-3.1, 0.1)
1.72 (NCR)
4.29
HT (mm)
-3.2 (-5.2, -1.2)*
1.21
3.02 (CR)*
MID (0.2)
MID (0.5)
Mean difference Angles/distances (MGNP - CGWONP) HCA (°)
-0.1 (-2.6, 2.4)
1.14 (NCR)
2.84
LCA (°)
-0.9 (-4.1, 2.3)
1.26 (NCR)
3.14
APA (°)
1.2 (-1.2, 3.6)
1.42 (NCR)
3.54
C2-C7 PT (°)
1.7 (-1.5, 4.9)
1.56 (PCR)
3.90 (NCR)
Cobb A (°)
1.3 (-2.2, 4.8)
1.39 (NCR)
3.46
C0-C1D (mm)
0.0 (-1.6, 1.6)
0.79 (NCR)
1.97
ATD (mm)
-7.1 (-9.7, -4.5)*
1.79
4.48 (CR)*
HT (mm)
-4.4 (-6.3, -2.5)*
1.30
3.25 (CR)*
MID (0.2)
MID (0.5)
Angles/distances Mean difference (MGNP-CGNP) HCA (°)
0.3 (-3.4, 4.0)
1.02 (NCR)
2.54
LCA (°)
-0.2 (-1.8, 1.4)
1.08 (NCR)
2.70
APA (°)
1.7 (-2.0, 5.4)
1.38 (PCR)
3.46 (NCR)
C2-C7 PT (°)
1.4 (-2.1, 4.9)
1.53 (NCR)
3.84
Cobb A (°)
-2.7 (-7.6, 2.2)
1.44 (PCR)
3.59 (NCR)
C0-C1D (mm)
1.4 (-1.2, 4.0)
0.69 (PCR)
1.71 (NCR)
26
ATD (mm)
-7.9 (-9.1, -6.7)*
1.77
4.42 (CR)*
HT (mm)
-1.0 (-3.5, 1.5)
1.18 (NCR)
2.95
MID (0.2)
MID (0.5)
Mean difference Angles/distances (MGWONP-CGNP) HCA (°)
-2.0 (-5.1, 1.1)
1.15 (PCR)
2.88 (NCR)
LCA (°)
-1.0 (-3.0, 1.0)
1.33 (NCR)
3.32
APA (°)
2.4 (-5.8, 1.0)
1.44 (PCR)
3.60 (NCR)
C2-C7 PT (°)
3.6 (-0.2, 7.5)
1.99 (PCR)
4.99 (NCR)
Cobb A (°)
-2.7 (-8.7, 3.3)
1.53 (PCR)
3.84 (NCR)
C0-C1D (mm)
0.2 (-1.2, 1.6)
0.78 (NCR)
1.95
ATD (mm)
-6.4 (-9.5, -3.3)*
1.85
4.63 (CR)*
HT (mm)
2.2 (-1.1, 5.5)
1.30 (PCR)
3.26 (NCR)
HCA: high cervical angle; LCA: low cervical angle; APA: atlas plane angle; Cobb A: Cobb angle for the cervical spine; C2-C7 PT: posterior tangent C2-C7; C0-C1D: C0-C1 distance; ATD: anterior translation distance; HT: hyoid triangle; MID: minimal important difference; NCR: not clinically relevant; PCR: potentially clinically relevant; *CR: clinically relevant.
S0031-9406(17)30026-3 http://dx.doi.org/doi:10.1016/j.physio.2017.03.004 PHYST 961
To appear in:
Physiotherapy
Please cite this article as: Ferracini Gabriela Nat´alia, Chaves Thais Cristina, Dach Fab´ıola, Bevilaqua-Grossi D´ebora, Fern´andez-de-las-Pe˜nas C´esar, Speciali Jos´e Geraldo.ANALYSIS OF THE CRANIO-CERVICAL CURVATURES IN SUBJECTS WITH MIGRAINE WITH AND WITHOUT NECK PAIN.Physiotherapy http://dx.doi.org/10.1016/j.physio.2017.03.004 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
1
ANALYSIS
OF
THE
CRANIO-CERVICAL
CURVATURES
IN
SUBJECTS WITH MIGRAINE WITH AND WITHOUT NECK PAIN
Gabriela Natália Ferracinia* MD, Thais Cristina Chavesb PhD, Fabíola Dachc PhD, Débora Bevilaqua-Grossid PhD, César Fernández-de-las-Peñase PhD, José Geraldo Specialif PhD.
1. *Doctoral Student, Department of Neurosciences and Behavioral Sciences/Faculty of Medicine of RibeirãoPreto, University of São Paulo – FMRP-USP. Ribeirão Preto, São Paulo, Brazil.
2. Professor, Department of Neurosciences and Behavioral Sciences/Faculty of Medicine of Ribeirão Preto, University of São Paulo – FMRP-USP/Postgraduate Program of Rehabilitation and Functional Performance. Ribeirão Preto, São Paulo, Brazil.
3. Professor, Department of Neurosciences and Behavioral Sciences/Faculty of Medicine of RibeirãoPreto, University of São Paulo – FMRP-USP/Responsible for the Headache and Craniofacial Pain Outpatient Clinic, University Hospital, Faculty of Medicine of Ribeirão Preto, Ribeirão Preto, São Paulo, Brazil.
4. Professor, Department of Neurosciences and Behavioral Sciences/Faculty of Medicine of Ribeirão Preto, University of São Paulo – FMRP-USP/Postgraduate Program of Rehabilitation and Functional Performance. Ribeirão Preto, São Paulo, Brazil.
5. Professor, Department of Physical Therapy, Occupational Therapy, Physical Medicine and Rehabilitation of Rey Juan Carlos University, Alcorcón, Spain
6. Senior Professor, Department of Neurosciences and Behavioral Sciences/Faculty of
2
Medicine of Ribeirão Preto, University of São Paulo – FMRP-USP. Ribeirão Preto, São Paulo, Brazil.
*Adress correspondece and reprint requests to: Gabriela Natália Ferracini. Department of Neurosciences and Behavioral Sciences. Faculty of Medicine of Ribeirão Preto, University of São Paulo. Avenida dos Bandeirantes, 3900 - 14048-900. Ribeirão Preto, SP, Brasil. Tel: +55 16 99750-8011
ABSTRACT Objective: To investigate the differences in head and cervical spine alignment between subjects with migraine and healthy people. Design: A cross-sectional, observational, study. Participants: Fifty subjects with migraine and 50 matched healthy controls participated. Main outcomes measures: The presence of neck pain and neck pain-related disability was assessed. Four angles (high cervical angle; low cervical angle; atlas plane angle, and cervical lordosis Cobb angle) as well as 4 distances (anterior translation distance; C0-C1 distance; C2-C7 posterior translation, and hyoid triangle) were calculated using digitalized radiographs and analyzed using the K-Pacs® software. Results: Subjects with migraine reported a longer history of neck pain symptoms, and higher pain intensity and neck painrelated disability than controls (P<0.01). Patients exhibited a smaller anterior translation distance (mean difference: 4.9mm, 95%CI 1.8-8.8; P<0.001) and hyoid triangle (difference: 3.0mm, 95% CI 1.0-5.0; P=0.02) than healthy controls. When the presence or the absence of neck pain was included in the analysis, the differences did not change. Differences in anterior translation and hyoid triangle distances were considered clinically relevant for subjects with migraine suffering from neck pain. Conclusion: Subjects with migraine
3
exhibited straightening of cervical lordosis curvature. The presence of neck pain did not influence head posture in subjects with and without migraine.
Keywords: Migraine. Neck. Radiograph. Posture.
INTRODUCTION Migraine is a common and chronic disabling disease. The prevalence ranges from 10 to 12% in the general population [1-3]. Approximately 90% of subjects with migraine report functional disability and about one third require rest during the head pain attacks [4]. Postural changes are commonly observed in subjects suffering from head pain, particularly those with primary headaches (migraine or tension-type headache). The most frequent cranio-cervical postural abnormality is the forward head posture (FHP) [5]. A FHP consists of a reduction of the cranio-cervical angle which is the degree of head extension in relation to the upper cervical spine, and implies that the head is anterior to a theoretical line passing through the center of gravity of the body [5]. However, there are other postural changes that could affect the cervical spine, e.g., a reduction or an increase of physiological cervical lordosis [6,7] which have not been investigated in primary headache populations. Postural changes can be evaluated by visual inspection and also documented photographically permitting a noninvasive and low-cost qualitative analysis method [8,9]. Different studies have investigated the presence of FHP with photographs in subjects with migraine [10,11] or tension type headache [12,13] and reported that subjects with headache exhibit greater FHP. Nevertheless, this qualitative evaluation
4
is not able to reproduce all curvatures of the cervical spine [7,14]. In such a scenario, radiographic examination is another method of postural evaluation which permits the assessment of cervical spine curvatures; take out however, although it is considered the gold standard to assess the spine curvatures [15], it also includes exposure to radiation [16]. A few studies have investigated the association of head and cervical spine posture and migraine, and the results are inconclusive. For instance, Fernández-delas-Peñas et al (2006) [10] and Ferreira et al (2014) [11] observed greater FHP in subjects with unilateral migraine. On the contrary, Zito et al (2006) and Ferracini et al (2015) [17,18] did not find such FHP in subjects with migraine in relation to healthy controls. To the best of the author’s knowledge, no study has previously investigated head/cervical spine posture by radiographic assessment in subjects with migraine. Therefore, the objective of our study was to investigate differences in the alignment of the head and the cervical spine between subjects with migraine and healthy people by using radiographic assessment. We hypothesized that subjects suffering from migraine will exhibit greater head and cervical spine postural misalignments than subjects without migraine.
MATERIALS AND METHODS Design A cross-sectional, observational study was conducted. All participants read and signed a consent form prior to enrollment. The study was approved by local ethics board of the XXXXXXXXX (Process15821-2011). Participants
5
Consecutive subjects with migraine attending a tertiary outpatient clinic were screened for eligibility criteria. Migraine was diagnosed according to the International Headache Society criteria by experienced neurologists (ICHD-II, 2004) [19]. Key element of headache history including family history, headache features, temporal profile, and current and past medications were considered. Participants were excluded if they exhibited; (1) other primary headache; (2) history of cervical injury; (3) cervical disc herniation; (4) medication overuse headache; (5) any systemic medical comorbidity, e.g. fibromyalgia or rheumatoid arthritis; (6) history who had not experienced any head pain; (7) those subjects who had received nerve blockade during the last 6 months; or, (8) subjects who had received physiotherapy for the neck/shoulder region in the previous 12 months. In addition, age- and sex-matched healthy subjects without headache history in the previous 6 months were also recruited. Clinical Outcomes In addition to demographic and anthropometric data, clinical headache outcomes including disease duration (years), frequency and duration of migraine, predominant head pain laterality, presence of self-reported neck pain, and intensity of migraine attacks during the last 3 months were assessed. Pain intensity at the time of evaluation was assessed using a numerical pain rate scale (NPRS where 0: absence of pain; 10: the worst pain experienced) [20]. Disability related to neck pain was determined with the Neck Disability Index (NDI) [21]. The NDI includes 10 questions related to the effects of neck pain on everyday activities, pain and concentration. The score corresponds to the sum of the points for each question (0-5), with 50 points as the maximum. Radiographic Outcomes
6
For the radiographic assessment, subjects were in a relaxed standing position, with both upper extremities along the body and both feet together. They were instructed to look at the horizon, and then take a comfortable neutral position of the head [22]. The distance between X-ray equipment and photographic film was standardized at 180 cm following international guidelines. The radiology technician was blinded to participant’s condition. Four cervical angles and four neck distances were measured in the digitalized radiographs and analyzed using the K-Pacs® software (Figure 1): 1. High cervical angle (HCA): This angle is formed by the McGregor plane (from the posterior nasal spine to the more inferior surface of the occipital line) and the plane of the odontoid process (line from C2 vertebrae axis to the most anteriorposterior point of C2). The intersection of these 2 tracings forms an angle that measures the degree of head extension in relation to the upper cervical spine (Fig. 1.6): the smaller the angle, the greater the head extension on the cervical spine [6]. 2. Low cervical angle (LCA): It is formed by a straight line tangent to the C3-C4 vertebral bodies through two distinct points, the highest point on the posterior C3 vertebral body and the most inferior point on the posterior surface of the C4 vertebral body (Fig. 1.5). The intersection on these 2 lines forms an angle that indicates the relationship between the high and low cervical spine: the greater the angle, the greater the cervical lordosis and the greater the extension of the upper cervical spine on the inferior part of the cervical spine [6]. 3. Atlas plane angle (APA): This angle represents the plane of the atlas vertebra (C1) with the tracing formed between a line parallel to horizontal and by another line traced in the inferior part of the posterior arc of the atlas (Fig. 1.2). An increase in
7
this angle suggests an increased extension of the upper cervical spine, particularly atlas (C1) extension [23]. 4. Cervical lordosis Cobb angle (Cobb A): Formed by the intersection of the lines of the plane of the superior vertebral plateau of C7 vertebra and of the inferior plateau of C2 (Fig. 1.4). This angle is a measure of the lordosis of the cervical spine [8]. 5. Anterior translation distance (ATD): The tracing is formed by the distance between posterior-superior margin of the C2 body and a vertical line perpendicular to the inferior margin of C7 vertebra body (Fig. 1.7). This measurement is important in determining the anterior head transposition [8]. 6. C0-C1 distance (C0-C1D): Consists of the measurement from the most inferior point of the base of the occipital bone to the posterior arc of C1 [24] (Fig. 1.1). 7. C2-C7 posterior translation (C2-C7PT): It is formed by posterior vertebral body tangents from C2 to C7 vertebrae (Fig. 1.3). It measures the lordosis of the cervical spine [6]. 8. Hyoid triangle (HT): It is the distance between the most anterior-superior point of the hyoid bone and the H line (formed by the most anterior-inferior point of C3 vertebra and the most posterior-inferior point of the chin) [24] (Fig. 1.8). Three measurements of each angle were assessed in all radiographies and the mean was used for the analysis. Intra-examiner reliability was determined using 10 radiographs randomly selected. Two different measurements of each angle were conducted with 7 days of distance. Sample size calculation The sample size determination was conducted with an appropriate software (Tamaño de la Muestra 1.1©, Barcelona, Spain). The sample size was based on detecting between-groups difference of 10º in radiographic outcomes with an alpha
8
level of 0.05 and a desired power of 80%. This generated a sample size of at least 35 participants per group.
Data Analysis The statistical analysis was conducted using SPSS statistical software, version 18.0. Mean and standard deviation were calculated for each variable, whereas mean and 95% confidence intervals (95%CI) were calculated for between-group difference scores. Intra-examiner reliability was determined by calculating intra-class correlation coefficients [ICC], Bland and Altman mean bias and limits of agreement [25]. The Kolmogorov-Smirnov test revealed a normal distribution of quantitative outcomes (P>0.05), therefore parametric tests were applied. First, student t-test (2tailed) for independent samples was used to determine the differences in angles and planes between subjects with migraine and controls. Second, an analysis of variance (ANOVA) with Bonferroni as post hoc analysis was used to compare the values of the angles and planes between groups considering the presence or absence of neck pain (migraine and healthy controls with or without neck pain). Effect sizes (ES) were calculated and classified as small when 0.20 (0-0.39), moderate when 0.50 (0.4-0.79), and high when >0.80 (Cohen, 1988). Finally, the minimal important difference (MID) and standard error of measurement (SEM) were also calculated [25]. Clinical relevance was classified according to Armijo-Olivo et al (2011) [26]: (1) when ES was > 0.40 (moderate ES) and the mean difference between groups was higher than both MIDs; (2) potential clinical relevance (PCR): moderate ES and
9
a mean difference higher than one of the MIDs; or small/moderate E S and the mean difference was higher than both MIDs; and (3) not clinically relevant (NCR) where there was a small ES and a mean difference lower than one of the MID. The statistical analysis was conducted at a 95% confidence level, and a Pvalue less than 0.05 was considered statistically significant. RESULTS Six hundred and sixty-two potential participants were screened for inclusion criteria between December 2012 and January 2014. Six hundred and twelve (n=612) subjects were excluded for the following reasons: other primary headaches (n=360), refused to participate (n=24), systemic medical comorbidities (n= 226) and 2 were selected and participated but their radiology images were poor to obtain accurate readings. Finally, 50 subjects, 45 women and 5 men, aged from 18 to 55 years (mean: 34 years), with migraine satisfied all eligibility criteria, agreed to participate and signed the informed consent. Further, 50 age- and sex- matched controls were also recruited. No significant differences in demographic variables were observed between the groups (Table 1). A greater number of subjects with migraine compared with healthy controls reported neck pain (P<0.001). Subjects with migraine exhibited a higher intensity of neck pain and neck pain-related disability than healthy controls (P<0.01, Table 1). Intra-examiner reliability (ICC) ranged from good to excellent and is presented in the Table 2. The radiographic analyses of cranio-cervical posture of subjects with and without migraine are presented in Table 3. The student t-test revealed significant differences for ATD (P<0.001) and HT (P=0.02) distances between subjects with migraine and healthy people: distances were smaller in subjects with migraine than
10
in controls (Table 3). The size of differences could be considered potentially clinically relevant (Armijo et al., 2011) (Table 4). When the presence/absence of neck pain was included, the ANOVA revealed significant differences for HT distance (F=3.42; P=0.02) and ATD (F=4.67; P<0.001). Pos hoc analysis revealed that subjects with migraine suffering neck pain exhibited smaller ATD (P=0.005) and HT (P=0.01) distances than controls with or without neck pain (Table 5). Table 6 shows that differences in both ATD and HT distances were clinically relevant between subjects with migraine and neck pain compared to healthy controls without neck pain. Additionally, differences in HT distance between subjects with migraine with and without neck pain, and differences in ATD distance between migraine subjects with neck pain and controls with neck pain were also clinically relevant (Table 6).
DISCUSSION The current study found that subjects with migraine exhibited 2 major postural changes including smaller ATD and HT distances. These results were not associated with the presence of neck pain symptom. Current findings suggest that migraine may be associated with a straightening of the cervical lordosis curvature rather than changes in cranio-cervical extension. To the best of our knowledge this is the first study investigating cervical postural changes in subjects with migraine by means of radiographic examination. Previous studies using photographic assessments found that subjects with migraine [10,11] or chronic tension type headache [12,13} exhibited greater FHP, i.e., smaller cranio-vertebral angle. However, Zito et al (2006) [17] and Ferracini et al (2015) [18]
11
did not find differences in FHP between migraine and healthy controls. Our findings and previous finding suggest that FHP is not present in subjects with migraine compared to women with no history of headache in 2 postural analyses (radiographic and photographic) [18]. Our study revealed that subjects with migraine exhibited a straightening of the cervical lordosis instead of a FHP. Discrepancies in postural changes observed may be related to the use of different outcomes. Gadotti et al (2013) [27] suggested that the photographs can be used as a clinical method for assessing the cranio-vertebral angle, i.e., FHP, in clinical setting; however, for proper assessment of the cervical lordosis the use of radiographic assessment is highly recommended. To determine potential reasons why subjects with migraine exhibited a loss of the physiological cervical lordosis is beyond the scope of this study; however, the clinical implications of these findings should be considered. For instance, the loss of the physiological cervical lordosis may result in changes in biomechanical force distribution both at vertebral and soft tissue levels [13,28]. Changes can include an overload on cervical structures e.g., ligaments, joints and discs, and muscle imbalances, i.e., activation and strength deficits [29] or myofascial trigger points [10]. These muscle imbalances can stimulate nociceptors, mechanoreceptors and proprioceptors at the cervical spine possibly leading to an activation of the trigeminocervical nucleus caudalis [29]. This could potentially result in postural changes of the cervical spine which may perpetuate migraine attacks; or vice versa, migraine attacks could also promote the chronification of neck disturbances. An interesting finding was that the presence of neck pain in either subjects with migraine and healthy controls did not influence the results. It is possible that the small number of healthy subjects from our sample reporting neck pain symptoms
12
may explain the lack of association. On the contrary, the prevalence of neck pain in subjects with migraine and other primary headaches has frequently been reported [30-33]. Our results showed a prevalence of 78% of subjects reporting neck pain within our migraine group, which is similar to recent published data [33]. It is possible that increased tension of the cervical musculature during migraine attacks can increase the risk of subsequent occurrence of migraine as a predictive factor for its onset [34]; however, the design of the current study does not permit us to determine any potential predictive factor. Although strengths of our study include a careful analysis of postural changes in the cranio-cervical region by radiographic examination considering both statistical and clinical viewpoints; there are also some potential limitations. First, subjects were recruited from a tertiary care hospital; therefore, it is possible that they represent a specific group of the general population with migraine. In fact, the presence of neck pain in our sample of healthy people suggests that extrapolation of our results should be conducted with caution at this stage. Second, the cross-sectional nature of the study does not permit us to establish a cause and effect relationship. Third, we did not include other relevant clinical outcomes, e.g., disability-related to migraine with maybe also related to postural changes. Fourth, the clinical relevance of postural changes in the cervical spine remains to be elucidated. Future population studies including large sample size of subjects with migraine and other co-morbid conditions are needed to further determine the presence of postural changes in the cervical spine and their clinical relevance in subjects with migraine.
CONCLUSIONS
13
Our results revealed that subjects with migraine exhibited straightening of the cervical lordosis curvature, that is, reduced ATD and HT distances, when assessed with radiographs. The presence of neck pain did not influence the results for people without migraine. Current results should be considered with caution at this stage due to the limitation in generalizability of the results.
Funding: This study was funded by Fundação de Amparo à pesquisa do estado de São Paulo (FAPESP).
Disclosure of interests: All authors have no conflicts of interest to declare.
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15. Gadotti I, Magee D. Radiographic craniocervical posture of asymtomatic female subjects. J Manipulative Physiol Ther 2013; 36: 27-32. 16. Fernández-de-las-Peñas C, Cuadrado ML, Pareja JA. Myofascial trigger points, neck mobility and forward head posture in unilateral migraine. Cephalalgia 2006; 26: 10611070. 17. Ferreira MC, Bevilaqua-Grossi D, Dach FE, et al. Body posture changes in women with migraine with or without temporomandibular disorders. Brazilian J Phys Ther 2014; 18: 19-29. 18. Fernández-de-las-Peñas C, Alonso-Blanco C, Cuadrado ML, et al. Triggers points in the suboccipital muscles and forward head posture in tension-type headache. Headache 2006; 46: 454-460. 19. Sohn JH, Choi HC, Lee SM, et al. Differences in cervical musculoskeletal impairment
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24. Headache Classification Subcommittee of the Inter- national Headache Society. The International Classifications of Headache Disorders, 2nd ed. Cephalalgia. 2004;24:9-160. 25. Bolton JE, Wilkinson CR. Responsiveness of pain scales: A comparison of three pain intensity measures in chiropractic patients. J Manipulative Physiol Ther 1988; 21:1-7. 26. Cook C, Richardson JK, Braga L, et al. Cross-cultural adaptation and validation of the Brazilian Portuguese version of the Neck Disability Index and Neck Pain and Disability Scale. Spine 2006; 31: 1621-7. 27. Garrett TR, Youdas JW, Madson TJ. Reliability of measuring forward head posture in a clinical setting. J Orthop Sports Phys Ther 1993; 17: 155-60. 28. Huggare JAV, Rautia A. Head posture and cervicovertebral and craniofacial morphology in patients with craniomandibular dysfunction. J Craniomand Pract 1992; 10: 435-40. 29. Rocabado M, Tapia V. Estúdio radiográfico de relación craneocervical em pacientes bajo tratamiento ortodóncio y su incidencia com sintomas referidos. Ortodonxia 1994; 8: 59-63. 30. Cohen J. The concepts of power analysis. In: Cohen J, editor. Statistical power analysis for the behavioral sciences. Hillsdale, New Jersey: Academic Press, Inc; 1988. p. 1-17. 31. Armijo-Olivo S, Warren S, Fuentes J, et al. Clinical relevance vs. statistical significance: Using neck outcomes in patients with temporomandibular disorders as an example. Man Ther 2011; 16: 563-72.
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32. Gadotti I, Armijo-Olivo S, Silveira A, et al. Reliability of the cranio-cervical posture assessment: visual and angular measurements using photographs and radiographs. J Manipulative Physiol Ther 2013; 36: 619-25. 33. Harrison DE, Jones WE, Janik TJ, et al. Evaluation of axial and flexural stresses in the vertebral body cortex and trabecular bone in lordosis and two sagittal cervical translation configurations with an elliptical shell model. J Manipulative Physiol Ther 2002; 26: 391-401. 34. Jull G, Amiri M, Bullock-Saxton J, et al. Cervical musculoskeletal impairment in frequent intermittent headache. Part 1: Subjects with single headaches. Cephalalgia 2007; 27: 793-802. 35. Wober C, Brannath W, Schmidt K, et al. Prospective analysis of factors related to migraine attacks: The PAMINA study. Cephalalgia. 2007; 27: 304314. 36. Calhoun AH, Ford S, Millen C, et al. The prevalence of neck pain in migraine. Headache 2010; 50: 1273-1277. 37. Plesh O, Adams SH, Gansky SA. Self-reported comorbid pains in severe headaches or migraines in a US national sample. Headache 2012; 52: 946956. 38. Ashina S, Bendtsen L, Lyngberg AC, et al. Prevalence of neck pain in migraine and tension-type headache: A population study. Cephalalgia. 2014 May 22. ii: 0333102414535110. [Epub ahead of print]. 39. Ferracini GN, Chaves TC, Dach F, Bevilaqua-Grossi D, Fernández-de-lasPeñas C, Speciali JG. Cervico-occipital posture in women with migraine: A case control study. J Orthop Sports Phys Ther 2015 (in press).
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40. Blaschek A, Decke S, Albers L. Self-reported neck pain is associated with migraine but not with tension-type headache in adolescents. Cephalalgia 2014;34: 895-903.
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Figure 1: Illustrative diagram of the radiographic measurements.
Legend: C0-C1 distance; (2) atlas plane angle; (3) C2-C7 posterior translation; (4) Cobb cervical spine angle; (5) low cervical angle; (6) high cervical angle; (7) anterior translation distance; (8) hyoid
20
Table 1: Clinical and demographic characteristics of patients with migraine and healthy controls Migraine (n=50)
Controls (n=50)
P
Sex (F/M)
45/5
45/5
0.99
Age (years)
34.1 (10.8)
33.7 (11.8)
0.85
Disease duration (years)
17.4 (12.3)
-
-
Headache Intensity - last 3 months
7.5 (1.7)
-
-
Headache intensity - time of evaluation (n=27)
5.4 (2.6)
-
-
Frequency of headache (days/month)
12.0 (9.7)
-
-
Duration of headache (hours per crisis)
18.1 (11.2)
-
-
Cervical Pain
78%
18%
<0.001*
Sex (F/M)
38/1
8/1
<0.002*
Duration of pain (years)
6.9 (1.2)
4.8 (1.4)
<0.001*
Intensity
4.9 (0.5)
1.4 (0.4)
<0.001*
Disability scores (NDI)
11.8 (1.0)
4.5 (1.4)
<0.001*
Data are expressed as mean (standard deviation) otherwise is advised F: female; M: male; BMI: body mass index; NPRS: numeric pain rate scale; NDI: neck disability index * Significant differences between patients and controls (Student t-test).
21
Table 2: Intra-examiner reliability for radiographic angles and distances Angles and distances
ICC (95%CI)
Bland and Altman mean bias (limits of agreement)
HCA (°)
0.88 (0.52 - 0.97)
0.5 (-1.2, 2.4)
LCA (°)
0.97 (0.91 - 0.99)
0.1 (-0.3, 0.5)
APA (°)
0.90 (0.61 - 0.97)
0.3 (-0.2, 0.8)
C2-C7 PT (°)
0.96 (0.84 - 0.99)
0.5 (-2.1, 3.1)
Cobb A (°)
0.93 (0.73 - 0.98)
1.3 (-0.2, 2.8)
C0-C1D (mm)
0.97 (0.90 - 0.99)
0.05 (-0.8, 0.9)
ATD (mm)
0.97 (0.88 - 0.99)
0.7 (-1.3, 2.7)
HT (mm)
0.94 (0.92 - 0.99)
0.03 (-0.3, 0.4)
HCA: high cervical angle; LCA: low cervical angle; APA: atlas plane angle; C2-C7 PT: posterior tangent C2-C7; Cobb A: Cobb angle for the cervical spine; C0-C1D: C0-C1 distance; ATD: anterior translation distance; HT: hyoid triangle. ICC: intra-class correlation coefficient; CI: confidence interval.
22
Table 3: Mean values and between-groups differences of angles (°) and distances (mm) for migraine and control groups
Angles and distances
Migraine
Healthy control
Mean Difference
HCA (°)
66.8 (5.3)
67.3 (5.5)
-0.5 (-2.5, 1.5)
LCA (°)
9.4 (5.2)
10.2 (6.6)
-0.8 (-3.1, 1.5)
APA (°)
16.7 (6.8)
15.5 (7.1)
1.2 (-1.5, 3.9)
C2-C7 PT (°)
14.8 (7.2)
12.0 (6.3)
2.8 (-0.5, 6.1)
Cobb A (°)
32.4 (9.2)
31.8 (8.3)
0.6 (-2.6, 3.8)
C0-C1D (mm)
8.5 (3.4)
8.5 (3.7)
0.0 (-1.2, 1.2)
ATD (mm)
14.4 (6.8)*
19.3 (6.4)
-4.9 (-8.8, -1.8)*
HT (mm)
3.1 (2.3)*
6.1 (3.8)
-3.0 (-1.0, -5.0)*
HCA: high cervical angle; LCA: low cervical angle; APA: atlas plane angle; C2-C7 PT: posterior tangent C2-C7; Cobb A: Cobb angle for the cervical spine; C0-C1D: C0-C1 distance; ATD: anterior translation distance; HT: hyoid triangle. Data are expressed as means (standard deviation) for group data and as means (95% confidence interval) for between-groups differences * Significant differences between patients and controls (student t-test, P<0.05)
23
Table 4: Mean between-groups difference score, standard error of the mean (SEM), effect size and minimum important difference (MID) of angles (°) and distances (mm) between patients with migraine and healthy controls Angles
Mean difference
Effect size
MID (0.2)
MID (0.5)
SEM
HCA (°)
-0.5
-0.09
1.10
2.77
1.91
LCA (°)
-0.8
-0.14
1.22
3.07
1.06
APA (°)
1.2
0.14
1.69
4.23
2.25
C2-C7 PT (°)
2.8
0.33(SES)
1.65 (PCR)
3.33
2.80
Cobb A (°)
0.6
0.04
2.45
6.14
2.00
C0-C1D (mm)
0.0
0.00
0.74
1.87
0.65
ATD (mm)
-4.9*
-0.41(MES)
2.32 (PCR)
5.82
1.59
HT (mm)
-3.0*
-0.48(MES)
1.28 (PCR)
3.20
0.93
distances
MID: minimal important difference; SEM: standard error of the mean; HCA: high cervical angle; LCA: low cervical angle; APA: atlas plane angle; Cobb A: Cobb angle for the cervical spine; C2-C7 PT: posterior tangent C2-C7; C0-C1D: C0-C1 distance; ATD: anterior translation distance; HT: hyoid triangle; MES: moderate effect size; PCR: potentially clinically relevant
24
Table 5: Mean and standard deviation (SD) of angles (°) and distances (mm) for patients with migraine and healthy controls by the presence or absence of neck pain Angles
MGNP
CGNP
CGWONP
(n=10)
(n=40)
MGWONP (n=11) and distances
(n=39)
HCA (°)
67.3 (5.4)
65.0 (5.2)
67.0 (5.9)
67.4 (5.4)
LCA (°)
9.5 (5.2)
8.7 (5.3)
9.7 (6.0)
10.4 (6.5)
APA (°)
16.7 (6.8)
17.4 (7.2)
15.0 (5.8)
15.6 (6.2)
C2-C7 PT (°)
14.3 (7.4)
16.5 (7.5)
12.9 (8.6)
12.6 (7.9)
Cobb A (°)
32.3 (8.0)
32.3 (7.9)
35.0 (8.2)
31.0 (8.4)
C0-C1D (mm)
8.8 (3.6)
7.6 (3.7)
7.4 (4.7)
8.8 (3.4)
ATD (mm)
12.0 (7.3)
13.5 (7.8)
19.9 (8.9)*
19.1 (8.5)*
HT (mm)
2.4 (2.3)
5.6 (4.6)
3.4 (4.4)
6.8 (4.7)*
MGNP: migraine group with neck pain, MGWONP: migraine group without neck pain; CGNP: control group with neck pain; CGWONP: control group without neck pain; HCA: high cervical angle, LCA: low cervical angle, APA: atlas plane angle; C2-C7 PT: posterior tangent C2C7; Cobb A: Cobb angle for the cervical spine; C0 - C1D: C0- C1 distance; ATD: anterior translation distance; HT: hyoid triangle.
* Significant difference between migraine patients with neck pain and control group (ANOVA, P<0.05 Bonferroni post hoc)
25
Table 6: Mean (95% confidence interval) of between-groups difference and minimum important difference of angles (°) and distances (mm) for patients with migraine and healthy controls by the presence/absence of neck pain
Mean difference Angles/distances
MID (0.2)
MID (0.5)
(MGNP- MGWONP) HCA (°)
2.3 (-1.6, 6.2)
1.08 (PCR)
2.70 (NCR)
LCA (°)
0.8 (-3.1, 4.7)
1.11 (NCR)
2.77
APA (°)
-0.7 (-2.0, 0.6)
1.41 (NCR)
3.53
C2-C7 PT (°)
-2.2 (-5.1, 0.7)
1.70 (NCR)
4.25
Cobb A (°)
0.0 (-5.1, 5.1)
1.57 (NCR)
5.93
C0-C1D (mm)
1.2 (-1.5, 3.9)
0.68 (PCR)
1.70 (NCR)
ATD (mm)
-1.5 (-3.1, 0.1)
1.72 (NCR)
4.29
HT (mm)
-3.2 (-5.2, -1.2)*
1.21
3.02 (CR)*
MID (0.2)
MID (0.5)
Mean difference Angles/distances (MGNP - CGWONP) HCA (°)
-0.1 (-2.6, 2.4)
1.14 (NCR)
2.84
LCA (°)
-0.9 (-4.1, 2.3)
1.26 (NCR)
3.14
APA (°)
1.2 (-1.2, 3.6)
1.42 (NCR)
3.54
C2-C7 PT (°)
1.7 (-1.5, 4.9)
1.56 (PCR)
3.90 (NCR)
Cobb A (°)
1.3 (-2.2, 4.8)
1.39 (NCR)
3.46
C0-C1D (mm)
0.0 (-1.6, 1.6)
0.79 (NCR)
1.97
ATD (mm)
-7.1 (-9.7, -4.5)*
1.79
4.48 (CR)*
HT (mm)
-4.4 (-6.3, -2.5)*
1.30
3.25 (CR)*
MID (0.2)
MID (0.5)
Angles/distances Mean difference (MGNP-CGNP) HCA (°)
0.3 (-3.4, 4.0)
1.02 (NCR)
2.54
LCA (°)
-0.2 (-1.8, 1.4)
1.08 (NCR)
2.70
APA (°)
1.7 (-2.0, 5.4)
1.38 (PCR)
3.46 (NCR)
C2-C7 PT (°)
1.4 (-2.1, 4.9)
1.53 (NCR)
3.84
Cobb A (°)
-2.7 (-7.6, 2.2)
1.44 (PCR)
3.59 (NCR)
C0-C1D (mm)
1.4 (-1.2, 4.0)
0.69 (PCR)
1.71 (NCR)
26
ATD (mm)
-7.9 (-9.1, -6.7)*
1.77
4.42 (CR)*
HT (mm)
-1.0 (-3.5, 1.5)
1.18 (NCR)
2.95
MID (0.2)
MID (0.5)
Mean difference Angles/distances (MGWONP-CGNP) HCA (°)
-2.0 (-5.1, 1.1)
1.15 (PCR)
2.88 (NCR)
LCA (°)
-1.0 (-3.0, 1.0)
1.33 (NCR)
3.32
APA (°)
2.4 (-5.8, 1.0)
1.44 (PCR)
3.60 (NCR)
C2-C7 PT (°)
3.6 (-0.2, 7.5)
1.99 (PCR)
4.99 (NCR)
Cobb A (°)
-2.7 (-8.7, 3.3)
1.53 (PCR)
3.84 (NCR)
C0-C1D (mm)
0.2 (-1.2, 1.6)
0.78 (NCR)
1.95
ATD (mm)
-6.4 (-9.5, -3.3)*
1.85
4.63 (CR)*
HT (mm)
2.2 (-1.1, 5.5)
1.30 (PCR)
3.26 (NCR)
HCA: high cervical angle; LCA: low cervical angle; APA: atlas plane angle; Cobb A: Cobb angle for the cervical spine; C2-C7 PT: posterior tangent C2-C7; C0-C1D: C0-C1 distance; ATD: anterior translation distance; HT: hyoid triangle; MID: minimal important difference; NCR: not clinically relevant; PCR: potentially clinically relevant; *CR: clinically relevant.