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Brazilian Oral Research

Print version ISSN 1806-8324On-line version ISSN 1807-3107

Braz. oral res. vol.32  São Paulo  2018  Epub July 23, 2018

http://dx.doi.org/10.1590/1807-3107bor-2018.vol32.0077 

Original Research

Temporomandibular Joint Dysfunction

Systemic diseases and other painful conditions in patients with temporomandibular disorders and migraine

Edwin Fernando Ruiz Contreras(a) 

Giovana Fernandes(b) 

Paula Cristina Jordani Ongaro(b) 

Leticia Bueno Campi(b) 

Daniela Aparecida Godoi Gonçalves(b) 

(a)Universidade Estadual de Londrina – UEL, Department of Restorative Dentistry, Londrina, PR, Brazil

(b)Universidade Estadual Paulista – UNESP, Araraquara Dental School, Department of Dental Materials and Prosthodontics, Araraquara, SP, Brazil


Abstract

Temporomandibular disorders (TMD) are a highly prevalent, painful musculoskeletal condition affecting the masticatory system, and are frequently associated with migraines (M) and other diseases. This study aimed to investigate the association between painful TMD and M with other painful conditions and systemic diseases, such as cervicalgia, body pain (BP), ear-nose-throat disorders, musculoskeletal disorders, diabetes, cardiopulmonary diseases and gastritis/peptic ulcer. Methods: This was a cross-sectional study conducted in a sample of 352 individuals. Participants were stratified into three groups according to the presence of painful TMD and M: controls [individuals free of TMD and any headache (HA)]; TMD only (presence of painful TMD, but free of any HA); and TMD+M (presence of painful TMD and M). TMD was classified according to the Research Diagnostic Criteria for Temporomandibular Disorders (RDC/TMD) - Axis I. Nonspecific physical symptoms (NSPS) were assessed by RDC/TMD - Axis II. The International Classification of Headache Disorders - II criteria, second edition, were applied to identify and classify primary HA. Other painful conditions and systemic diseases were assessed by volunteers’ self-report. The prevalence of all assessed conditions was higher in the TMD+M group. Multiple regression models showed that cervicalgia was associated with the TMD only group (p<0.05), whereas gender (p<0.05), cervicalgia (p<0.05), BP (p<0.05) and NSPS (p<0.05) were significantly associated with the TMD+M group. Our results suggest that individuals with a comorbidity (TMD associated with M) have a more severe condition than those presenting only painful TMD.

Keywords: Migraine Disorders; Temporomandibular Joint Disorders; Neck Pain; Headache; Comorbidity

Introduction

Temporomandibular disorders (TMD) are considered a type of functional pain syndrome (FPS) or idiopathic pain disorder (IPD), which also include conditions such as fibromyalgia, low back pain, irritable bowel syndrome, chronic headaches (HA), interstitial cystitis, chronic pelvic pain, chronic tinnitus, whiplash-associated disorders, and vulvar vestibulitis.1 Whereas TMD is defined as a group of disorders involving the masticatory muscles, the temporomandibular joint (TMJ) and associated structures,2 FPS, in general, is characterized by high levels of psychological distress (anxiety, health-seeking behavior and markers of somatization) and abnormalities in motor function, autonomic balance and sleep.1,3 Although these disorders frequently occur concomitantly, the relationship among them remains unclear.3 Moreover, FPS typically does not respond well to conventional therapies, indicating that a better understanding of its etiology and mechanism should be highly relevant to the medical field.1

A large proportion of patients with painful TMD also present a significant disability, with consequences that impact their lives. The simultaneous presence of pain in other body areas seems to increase the magnitude of the impact. Moreover, it has been demonstrated that painful TMD is strongly associated with other painful conditions,4 such as fibromyalgia,5,6 widespread pain,5,6 cervical spine dysfunction,7 neck pain, low back and joint pain8 and primary HA.9,10,11,12

Among the comorbid conditions, some primary HA are more frequently associated with painful TMD.9,10,13,14,15,16 The magnitude of the association is higher for migraine (M), followed by tension-type headaches (TTH).10,11,12,13,14,15,16,17 Previous evidence has indicated that TMD is comorbid with M and a risk factor for M chronification.9,11,12,13 Additionally, it has been demonstrated that the presence of a comorbidity negatively influences diagnostic tests for musculoskeletal pain.18

Although previous studies have shown an association between TMD and other painful conditions,18,19 somatization, depression5,18 and a reduced quality of life,20 there is still a lack of information regarding the relationship between painful TMD (isolated or associated with M) and systemic diseases. Therefore, this study aimed to investigate the association between painful TMD and M with other painful conditions [such as cervicalgia, body pain (BP), musculoskeletal disorders (MED)] and systemic diseases [such as ear-nose-throat disorders (ENT), diabetes, cardiopulmonary diseases and gastritis/peptic ulcer]. We hypothesized that painful TMD was significantly associated with systemic diseases, and that the magnitude of the association would be greater in the case of painful TMD and M comorbidity, thus resulting in a higher burden of the disease.

Methods

Our sample was composed of 352 individuals. Of these, 305 were patients who sought care at the UNESP/Araraquara School of Dentistry, presenting with the chief complaint of orofacial pain, and 47 individuals (control group) were free of TMD, HA or any type of facial pain. The controls were selected among the patients seeking routine dental care treatment at the same university, or companions of patients. This group is relatively small, since finding individuals free of HA and TMD is not a simple task. We included individuals of both genders, aged between 18 and 65 years, presenting adequate bilateral occlusal contacts, and able to read and write. Exclusion criterion was the presence of any cognitive or communication impairment. The Research Ethics Committee of the Araraquara Dental School (UNESP - Universidade Estadual Paulista, Brazil), approved this study. Informed consent was obtained from each participant.

Assessments

Temporomandibular disorders and non-specific physical symptoms

Two trained researchers evaluated all the individuals, following a standardized orofacial pain clinic protocol, including an interview and a clinical exam. The chief complaint, characteristics of the pain (quality, duration, frequency, intensity, location, and exacerbating and alleviating factors), medical history and medication use were assessed. The TMD diagnosis and classification were made according to the diagnostic criteria of the American Academy of Orofacial Pain (AAOP)2 and the Research Diagnostic Criteria for Temporomandibular Disorders (RDC/TMD) - Axis I – Portuguese version, respectively.22 The RDC/TMD – Axis I allowed us to confirm the diagnosis of TMD and define its classification into muscle disorders (Group I), articular disorders (Group II and III), or both. Data analysis was performed by grouping the individuals according to the diagnosis of painful types of TMD, including those of muscular and/or articular origin. The nonspecific physical symptoms (NSPS) were assessed by the RDC/TMD - Axis II, item 2.3. According to this instrument, individuals were classified into two groups, those presenting or not presenting NSPS.

Painful conditions and systemic diseases

The presence of persistent painful conditions and systemic diseases in the last 6 months were assessed through the individuals’ report during the interview. We assessed the presence of cervicalgia, BP, musculoskeletal disorders (arthritis, fibromyalgia, back pain), ENT (otitis, sinusitis, rhinitis), diabetes, cardiorespiratory conditions (hypertension, heart disease, asthma, bronchitis), and gastritis/peptic ulcer.

Migraine

Migraine was clinically diagnosed by a researcher with specific training in HA medicine, using a structured questionnaire based on the International Classification for Headache Disorders, second edition (ICHD-II).23 The questions collected information regarding HA features (frequency and duration of episodes, laterality, characteristics of pain, exacerbation with movement), and associated symptoms (aura, nausea, photophobia, phonophobia, autonomic symptoms). This questionnaire has been used in performing epidemiological and clinical research in Brazil,9,10,11,12,13 and can identify the existence of M, TTH, or primary HA. Only individuals free of any HA or presenting M were included in the sample.

Data Analysis

The presence of painful TMD only or TMD associated with M comprised the outcome variables. Gender, self-reported diseases, other painful conditions and presence of NSPS were considered predictor variables. The sample was stratified into three groups, according to the presence of painful TMD and M: control (free of TMD and any HA); TMD only group (individuals presenting painful TMD but free of any HA); TMD+M group (individuals presenting painful TMD and M).

Descriptive statistics and frequency counts were used to characterize the sample. Two logistic regression models were performed to investigate the association between the outcome variables. The first model was built to study what predictor variables were associated with the TMD only group, compared with the control group. The second model was performed to analyze what predictor variables were associated with the simultaneous presence of painful TMD and M (TMD+M group), compared with the control group. In both models, the variables showing significant association (p < 0.05) with the univariate analyses were included in the multiple logistic models. In the logistic regression model, the predictor variables with the weakest association to the outcome variable were removed. This procedure was repeated using a backward stepwise approach until all the variables retained in the model yielded p < 0.05. The p-to-exit is reported for each predictor variable removed. The data were checked for multicollinearity, using a tolerance value < 0.10 and a variance inflation factor > 10. All analyses were performed with the Statistical Package for the Social Sciences (SPSS) software, version 21.0 for Mac.

Results

Sample characterization

Initially, 507 volunteers were screened according to the protocol mentioned above. Of these, we excluded 93 individuals presenting other types of HA (no M), 21 presenting non-painful TMD, and 41 because of missing data regarding other diseases. The final sample consisted of 352 individuals stratified into three groups according to the presence of painful TMD and M (Figure). The descriptive data of the predictor variables stratified according to the three groups are shown in Table 1.

Figure 1 Participants flow diagram. 

Table 1 Descriptive data of the predictor variables stratified according to the three groups. 

Variable Control TMD only TMD+M Total
47 (13.4) 41 (11.6) 264 (75) 352
Cervicalgia
no 42 (38.5) 17 (15.6) 50 (45.9) 109 (100)
yes 5 (2.1) 23 (9.6) 212 (88.3) 240 (100)
Body Pain
no 43 (23) 23 (12.3) 121 (64.7) 187 (100)
yes 4 (2.5) 17 (10.4) 142 (87.1) 163 (100)
MED
no 32 (16.8) 23 (12.1) 135 (71.7) 190 (100)
yes 15 (9.3) 18 (11.1) 129 (79.6) 162 (100)
ENT
no 31 (17.8) 20 (11.5) 123 (70.7) 174 (100)
yes 16 (9) 21 (11.8) 141 (79.2) 178 (100)
Diabetes
no 44 (13.1) 36 (10.7) 255 (76.1) 335 (100)
yes 3 (17.6) 5 (29.4) 9 (52.9) 17 (100)
Cardiopulmonary
no 39 (14.8) 31 (11.7) 194 (73.5) 264 (100)
yes 8 (9.1) 10 (11.4) 70 (79.5) 88 (100)
Gastritis/Peptic Ulcer
no 41 (16.4) 28 (11.2) 181 (72.5) 250 (100)
yes 6 (5.9) 13 (12.7) 83 (81.4) 102 (100)
NSPS
no 34 (43) 19 (24.1) 26 (32.9) 79 (100)
yes 13 (4.8) 22 (8.1) 238 (87.2) 273 (100)

TMD: Temporomandibular disorders; M: Migraine; MED: Musculoskeletal disorders; ENT: Ear, nose and throat disorders; NSPS: Non-specific physical symptoms.

The majority of the sample were women (83.8%) (p < 0.001). Overall, the mean age was 37.7 ± 12.7, with no statistical difference among the groups (p > 0.05); 47 (13.4%) participants had no TMD or HA, and 305 (86.6%) presented painful TMD. Among the individuals with painful TMD, 264 also presented M. The prevalence of each painful condition and systemic disease, according to the three groups, are presented in Table 2. The prevalence of painful conditions, systemic diseases and NSPS was higher among individuals with painful TMD associated with M (TMD + M group), compared with the controls and the individuals presenting only painful TMD (TMD only group).

Table 2 Single and multiple logistic regression models for prediction of TMD only group versus the control group. The number of cases (n) included in the analysis is shown for each factor included in the single regression. 

Predictor variables n Single regression p -to-exit Multiple regression
p-value OR 95%CI p-value OR 95%CI
Gender
Men 34
Women 54 0.036 2.6 1.07–6.41 0.163
Cervicalgia
No 59
Yes 28 0.000 11.3 3.71–34.81 0.000 10.0 3.24–31.30
Body Pain
No 66
Yes 21 0.001 7.9 2.39–26.41 0.340
MED
No 55
Yes 33 0.248 1.7 0.70–3.98
ENT
No 51
Yes 37 0.105 2.0 0.86–4.81
Diabetes
No 80
Yes 8 0.352 2.0 0.46–9.11
Cardiorespiratory conditions
No 70
Yes 18 0.395 1.6 0.55–4.46
Gastritis/Ulcer
No 69
Yes 19 0.036 3.2 1.08–9.34 0.312
NSPS
No 53
Yes 35 0.014 3.0 1.25–7.35 0.471

TMD: Temporomandibular disorders; M: Migraine; MED: Musculoskeletal disorders; ENT: Ear, nose and throat disorders; NSPS: Non-specific physical symptoms.

The univariate analysis of the first regression model (TMD only compared with the control) showed that gender (p = 0.036), cervicalgia (p < 0.001), BP (p = 0.001), gastritis/peptic ulcer (p < 0.05) and NSPS (p < 0.05) were associated with the presence of painful TMD (Table 3). The multivariate analysis showed that the strongest predictor variable associated with the presence of TMD only was cervicalgia [odds ratio (OR): 10.0, 95%CI = 3.2–31.30].

Table 3 Single and multiple logistic regression models for prediction of the TMD+M versus the control group. The number of cases (n) included in the analysis is shown for each factor included in the single regression. 

Predictor variables n Single regression p-to-exit Multiple regression
p-value OR 95%CI p-value OR 95%CI
Gender
Men 46
Women 265 0.000 10.0 4.92–20.51 0.000 6.4 2.38–16.99
Cervicalgia
No 92
Yes 217 0.000 35.6 13.41–94.62 0.000 10.3 3.37–31.44
Body pain
No 164 --
Yes 146 0.000 12.6 4.40–36.15 0.041 3.8 1.06–13.53
MED
No 167
Yes 144 0.034 2.0 1.06–3.94 0.156 --
ENT
No 154
Yes 157 0.016 2.0 1.16–4.25 0.064
Diabetes
No 299
Yes 12 0.337 2.0 0.50–7.42
Cardiorespiratory conditions
No 233
Yes 78 0.171 1.8 0.78–3.94
Gastritis/Ulcer
No 222
Yes 89 0.012 3.1 1.28–7.67 0.274
NSPS
No 60
Yes 251 0.000 24.0 11.24–51.02 0.000 7.1 2.81–18.06

TMD: Temporomandibular disorders; M: Migraine; MED: Musculoskeletal disorders; ENT: Ear, nose and throat disorders; NSPS: Non-specific physical symptoms.

In the second model (Table 4) (TMD+M vs. control), the univariate analyses indicated that gender (p < 0.001), cervicalgia (p < 0.001), BP (p < 0.001), MED (p = 0.034), ENT (p = 0.016), gastritis/peptic ulcer (p = 0.012) and NSPS (p < 0.001) were significantly associated with the presence of concomitant painful TMD and M. Multivariate analyses, in turn, showed that comorbidity (TMD+M group) was significantly associated with a wide variety of predictor variables, including gender [OR: 6.4 (95%CI = 2.38–16.99)], cervicalgia [OR: 10.0 (95%CI = 3.24–31.30)], BP [OR: 3.8 (95%CI = 1.06–13.53)], and NSPS [OR: 7.1 (95%CI = 2.81–18.06)].

Table 4 Single and multiple logistic regression models for prediction of TMD+M group versus TMD only group. The number of cases (n) included in the analysis is shown for each factor included in the single regression. 

Predictor variables n Single regression p-to-exit Multiple regression
p value OR 95%CI p-value OR 95%CI
Gender
Men 34
Women 271 0.001 3.8 1.7–8.65 0.026 2.8 1.13–6.86
Cervicalgia
No 67
Yes 235 0.001 3.1 1.55–6.30 0.232
Body pain
No 144
Yes 159 0.178 1.6 0.81–3.11
MED
No 158
Yes 147 0.555 1.2 0.63–2.36
ENT
No 143
Yes 162 0.794 1.1 0.56–2.10
Diabetes
No 291
Yes 14 0.019 3.9 1.24–12.39 0.019 4.5 1.23–15.55
Cardiorespiratory conditions
No 225
Yes 80 0.774 1.1 0.52–2.40
Gastritis/Ulcer
No 209
Yes 96 0.973 1.01 0.49–2.05
NSPS
No 45
Yes 260 < 0.001 7.9 3.79–16.49 < 0.001 6.8 3.16–14.64

Finally, the last model compared the TMD only group with the TMD+M group (Table 5). According to the univariate analyses, gender (p = 0.001), cervicalgia (p = 0.001), diabetes (p = 0.019) and NSPS (p < 0.001) were significantly associated with individuals presenting the concomitant presence of painful TMD and M, compared with those presenting only painful TMD. Multivariate analysis indicated that gender [OR = 2.8 (CI = 1.13–6.86)], diabetes [OR = 4.5 (CI = 1.23–15.55)] and NSPS [OR = 6.8 (CI = 3.16–14.64)] were significantly associated with the presence of painful TMD and M. There were no signs of multicollinearity among the predictor variables.

Table 5 Single and multiple logistic regression models for prediction of TMD+M group versus TMD only group. The number of cases (n) included in the analysis is shown for each factor included in the single regression. 

Predictor variables n Single regression p-to-exit Multiple regression
p-value OR 95%CI p-value OR 95%CI
Gender
Men 34
Women 271 0.001 3.8 1.7–8.65 0.026 2.8 1.13–6.86
Cervicalgia
No 67
Yes 235 0.001 3.1 1.55–6.30 0.232
BP
No 144
Yes 159 0.178 1.6 0.81–3.11
MED
No 158
Yes 147 0.555 1.2 0.63–2.36
ENT
No 143
Yes 162 0.794 1.1 0.56–2.10
Diabetes
No 291
Yes 14 0.019 3.9 1.24–12.39 0.019 4.5 1.23–15.55
Cardiorespiratory conditions
No 225
Yes 80 0.774 1.1 0.52–2.40
Gastritis/Ulcer
No 209 --
Yes 96 0.973 1.01 0.49–2.05
NSPS
No 45
Yes 260 < 0.001 7.9 3.79–16.49 < 0.001 6.8 3.16–14.64

TMD: Temporomandibular disorders; M: Migraine; MED: Musculoskeletal disorders; ENT: Ear, nose and throat disorders; NSPS: Non-specific physical symptoms.

Discussion

TMD has been included in a group of painful conditions named functional pain syndromes, or idiopathic pain disorders.1 These conditions are associated with neurobiological, physiological and anatomical changes in the central nervous system.24 It is also well established that there is a comorbid relationship between painful TMD and M.10,13 Previous studies have demonstrated that TMD patients, as well as migraineurs, are more sensitive to pain and present multiple BP areas more frequently.4,19,25 These characteristics point to a generalized dysfunction of the nociceptive system, and an upregulation of the nociceptive process.26 Herein, we hypothesized that the presence of a comorbidity (painful TMD associated with M) could be associated with a higher prevalence of other painful conditions and systemic diseases.

Our most important findings were: a) individuals with painful TMD and M presented higher prevalence of all the painful conditions and systemic diseases investigated; b) cervicalgia was significantly associated with the presence of painful TMD, compared with the condition of the controls; c) gender, cervicalgia, BP and NSPS were significantly associated with the presence of a comorbidity (painful TMD+M), compared with the condition of the controls; d) when comparing individuals with TMD, the presence of M (comorbid group) was associated with gender, diabetes and NSPS.

In our results, the report of persistent cervicalgia figured as an important factor associated with TMD only or TMD+M. Previous studies have shown that cervicalgia is both associated with and a predictor of TMD,8,27 as is M.28 Among the hypotheses about the mechanisms related to these associations, the anatomical aspects seem to be particularly relevant. Muscles and ligaments of the cranial area are connected in the cervical region, possibly resulting in an interaction among such factors as neck muscle activity, head position, and mandibular function.29 Moreover, there is a convergence of cervical and trigeminal inputs with the spinal trigeminal nucleus, resulting in referred pain.2

In the present study, both TMD and M were more prevalent among adult women than men. In the univariate regression, gender was significantly associated with both groups (TMD only and TMD+M), whereas in the multiple regressions, it figured as a significant predictor only for the comorbid group. Similar results were found by other authors with a higher prevalence in women10,30 aged 20 to 40 years.30 These differences may be attributed to the different activation of the endogenous analgesia system and the central processing of nociceptive stimuli between genders. Moreover, sexual hormones, especially estrogen, have been pointed out as playing an important role in sensitivity to pain, altering the pain threshold and tolerance according to the menstrual cycle phase. TMD onset tends to occur after puberty, and the increase in the severity of signs and symptoms generally reaches its peak during the reproductive age, with higher prevalence in young adult women.30

In our sample, the presence of diffuse BP was significantly associated with comorbidity. It has been reported that multiple pain conditions elsewhere in the body could predict TMD onset,31 and influence its maintenance.32 Migraineurs are also more likely to report BP.25 It is plausible to hypothesize that this association could be related to central sensitization and functional changes in genetically susceptible individuals.33 Previous evidence supports the theory that the activation and sensitization of the trigeminovascular system may result in the impairment of diffuse noxious inhibitory control,34 predisposing to a progressive development of cephalic and whole-body cutaneous allodynia.35 This evidence is consistent with our findings, considering that the association between M and TMD may reflect a more severe state of sensitization.

Although more studies are needed to improve the understanding of the mechanisms involved in comorbid conditions, our results are aligned with the evidence pointing to the relevant role of the central and peripheral nervous systems. Structural and functional aspects have to be considered, in addition to the influence of other aspects, such as genetics and psychosocial alterations.1,28,37

We can conclude that individuals with a comorbidity (M associated with painful TMD) show a more severe condition, as evidenced by the higher number of predictor variables, compared with individuals with only painful TMD. This finding strongly entails impairment of the endogenous mechanisms of pain control, which should be considered in all processes, from diagnosis to treatment plan.

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Received: October 07, 2017; Accepted: February 21, 2018; Revised: June 04, 2018

Corresponding Author: Edwin Fernando Ruiz Contreras, E-mail: edwinfrc@gmail.com

Declaration of Interests: The authors certify that they have no commercial or associative interest that represents a conflict of interest in connection with the manuscript.

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