**Increased Risk of Migraine in Patients with Temporomandibular Disorder: A Longitudinal Follow-Up Study Using a National Health Screening Cohort**

#### **Soo-Hwan Byun 1,2 , Chanyang Min 3 , Dae-Myoung Yoo 3 , Byoung-Eun Yang 1,2 and Hyo-Geun Choi 2,3,4, \***


Received: 11 August 2020; Accepted: 18 September 2020; Published: 20 September 2020

**Abstract:** Background: The aim of this study was to investigate the association between temporomandibular disorder (TMD) and migraine through a longitudinal follow-up study using population data from a national health screening cohort. Methods: This cohort study used data from the Korean National Health Insurance Service-Health Screening Cohort from 2002 to 2015. Of the 514,866 participants, 3884 TMD patients were matched at a 1:4 ratio with 15,536 control participants. Crude models and models adjusted for obesity, smoking, alcohol consumption, systolic blood pressure, diastolic blood pressure, fasting blood glucose, total cholesterol, and Charlson Comorbidity Index (CCI) scores were calculated. Chi-squared test, Kaplan–Meier analysis, and two-tailed log-rank test were used for statistical analysis. Stratified Cox proportional hazard models were used to assess hazard ratios (HR) and 95% confidence intervals (CIs) for migraine in both control groups. Results: The adjusted HR for migraine was 2.10 (95% CI: 1.81–2.44) in the TMD group compared to the control group, which was consistent in subgroup analyses according to age, sex, and Kaplan–Meier analysis. Conclusions: This study demonstrated that TMD patients have a higher risk of migraine. These results suggest that dentists can decrease the risk of migraine in TMD patients by managing TMD properly.

**Keywords:** migraine; TMD; Korean National Health Insurance Service; cohort; aura

### **1. Introduction**

Temporomandibular disorder (TMD) is a collective term for comprehensive clinical symptoms related to the dysfunction of the temporomandibular joint (TMJ), masticatory muscles, and adjacent anatomic structures [1]. The etiology of TMD is multifactorial, including parafunctional habit, posture, and neurologic factors [2,3]. Mastication and other functions aggravate the condition, and most patients suffer from limited or asymmetric mouth opening. Related symptoms of TMD are headache, joint sounds (clicking, popping, and crepitus), and craniomaxillofacial pain [4]. TMD affects between 5–70% of Caucasians, and several studies have reported that maxillofacial pain is the major complaint of

more than half of the consultations and up to 80% of dental appointments among adolescents [5,6]. Moreover, it was shown that clinicians feel incompetent in managing TMD, resulting in referrals to other clinicians [7].

Migraine usually occurs on one side of the head with throbbing pain or a pulsing sensation. The symptoms often occur with photosensitivity, vomiting, and nausea. Migraine can last for several hours, and it can interfere with normal activities. Medications could relieve some migraines and prevent them. Proper medications, combined with self-help solutions and healthier lifestyles, might help to manage this headache [8].

The International Classification of Headache Disorders (ICHD) has classified migraine into two types: with and without aura [9]. Based on the classification of ICHD-3, an aura must present with at least three of the following six symptoms: spreading gradually for more than 5 min, two or more symptoms occurring in succession, each individual aura symptom lasts 5–60 min, at least one aura symptom is unilateral, at least one aura symptom is positive, and the aura is accompanied or followed within 60 min by headache [9,10]. An aura is known as a warning sign prior to migraine for some patients. An aura can occur with visual disturbances, including blind spots, flashes of light, tingling on one side of the face, or difficulty speaking. Migraine with aura is considered to affect between one-fifth and one-third of those with migraine in the United States, an estimated 7.4–11.1 million people [11]. The pathophysiology of aura is widely known as cortical spreading depression (CSD) [12]. CSD is activated by slow depolarization in cortical neurons and glia, followed by hyperpolarization that moves across the cortex at a rate of 3–5 mm/min. It is accompanied by alterations in neurotransmitter release and ion homeostasis [13]. As greater energy is needed to restore homeostasis, this is accompanied by a rapid spike in cerebral blood flow [14].

A migraine without aura is the most common type of migraine, comprising approximately 75% of all migraines [9]. This type of migraine develops without aura, but it can present with various symptoms at its initial stages. According to ICHD-3, it lasts for 4–72 h and has at least two of the following headache characteristics: moderate-to-severe intensity, unilateral location, aggravation by physical activity, and pulsating quality [15]. One or more associated symptoms such as nausea/vomiting and photophobia/phonophobia would happen during the attack. In addition, attacks of a migraine without aura must not be attributable to another disorder.

Most painful symptoms are transient and are related to a specific lesion or disease that can be cured. Unfortunately, some types of pain are chronic, and chronic pain remains a public health issue [16]. Both TMD and migraine could be main causes of chronic pain in the orofacial area. Many patients with TMD have several comorbid conditions [17,18]. Moreover, previous studies of TMD patients have revealed that comorbid conditions are the reason for 50% of TMD patients requiring care for TMD symptoms, and for 20% of patients with long-term disability from their pain [19–21]. It is essential that any comorbid conditions and their influences on clinical outcomes are identified and evaluated by clinicians managing TMD patients [22].

Some studies have reported an association between TMD and migraine [8,23–26]. This association was thought to be induced by anatomic, neurologic, and emotional relationships. Previous studies reported that migraine is related to pain in the sinus, teeth, TMJ, and cervical areas [27–29]. However, most studies have been based on limited participants or subjective questionnaires [26,30].

The aim of this study was to investigate the association between TMD and migraine by conducting a longitudinal study using population data from a national health screening cohort. It was determined that patients with TMD have a greater risk of migraine than those without TMD.

#### **2. Materials and Methods**

#### *2.1. Study Population*

The ethics committee of Hallym University approved this study on 4 November 2019 (No. 2019-10-023). The need for written informed consent was waived by the Institutional Review Board. All analyses adhered to the guidelines and regulations of the ethics committee. The details of the Korean National Health Insurance Service-Health Screening Cohort data have been described elsewhere [31].

### *2.2. Definition of Temporomandibular Disorder*

TMD was defined if participants were diagnosed with the ICD (International Classification of Diseases)-10 code K07.6 (Temporomandibular joint disorders). For diagnostic accuracy, this study only selected participants who were treated ≥2 times for the diagnosis of TMD. ≥

#### *2.3. Definition of Migraine*

Migraine was defined if participants were diagnosed with the ICD-10 code G43 (Migraine). For diagnostic accuracy, this study only selected participants who were treated ≥2 times for the diagnosis of migraine. Among them, migraine with aura was defined if participants were diagnosed with the ICD-10 code G43.1 (Migraine with aura). ≥

#### *2.4. Participant Selection*

TMD patients were selected from 514,866 participants with 615,488,428 medical claim codes from 2002 to 2015 (*n* = 4627). The control group consisted of participants who were not diagnosed with TMD from 2002 to 2015 (*n* = 510,239). TMD patients were excluded if they had a 1-year washout period (*n* = 172). Control participants were excluded if they were diagnosed with the ICD-10 code K07.6 once (*n* = 6659). TMD patients were matched at a 1:4 ratio with control participants for age, sex, income, and region of residence; this was done randomly to prevent selection bias. In this study, we supposed that the matched participants were involved in the same date (index date). Participants who died before the index date and had a history of migraine before the index date were excluded. In the TMD group, 571 participants were excluded, and during matching, 488,044 control participants were excluded. As a result, 3884 TMD patients were matched at a 1:4 ratio with 15,536 control participants (Figure 1).

**Figure 1.** A schematic illustration of the participant selection process. Out of 514,866 participants, 3884 patients with temporomandibular disorder were matched at a 1:4 ratio with 15,536 control participants for age, sex, income, and region of residence. TMD, temporomandibular disorder; ICD-10, International Classification of Diseases, 10th edition.

#### *2.5. Covariates*

Age was categorized into ten groups ranging from 40–44 to 85+. Income groups were divided into five classes from lowest income (class 1) to highest (class 5) income. Regions of residence were grouped into urban and rural areas following our previous study [31].

Tobacco smoking, alcohol consumption, obesity based on body mass index (BMI, kg/m<sup>2</sup> ) [32,33], systolic blood pressure (BP), diastolic BP, fasting blood glucose, and total cholesterol were measured as described in our previous study [34]. The Charlson Comorbidity Index (CCI) was used to measure 17 comorbidities [35].

#### *2.6. Statistical Analyses*

Chi-squared tests were used to compare general characteristics between the TMD and control groups.

Stratified Cox proportional hazard models were used to assess the hazard ratios (HRs) and 95% confidence intervals (CIs) for migraine in the TMD group compared to the control group. In this analysis, crude (simple) and adjusted (for obesity, smoking, alcohol consumption, systolic BP, diastolic BP, fasting blood glucose, total cholesterol, and CCI scores) models were used. Age, sex, income, and region of residence were stratified. Additionally, this study calculated HRs with 95% CIs for migraine with and without aura in the TMD group compared to the control group.

A Kaplan–Meier analysis and the log-rank test were used to analyze the cumulative probability of migraine in the TMD group compared to the control group.

For subgroup analyses, this study divided participants by age and sex (<60 years old and ≥60 years old; males and females) and analyzed the crude and adjusted models. We additionally performed subgroup analyses of crude and adjusted HRs for migraine with and without aura in the TMD group compared to the control group (Tables S1 and S2).

Two-tailed analyses were performed, and significance was defined as *p*-values less than 0.05. SAS version 9.4 (SAS Institute, Cary, NC, USA) was used for statistical analyses.

#### **3. Results**

The general characteristics for age, sex, income, and region of residence were identical due to matching between the groups (Table 1), while those for obesity, smoking, alcohol consumption, BP, fasting blood glucose, total cholesterol, and CCI were different.


**Table 1.** General characteristics of participants.


**Table 1.** *Cont*.

CCI, Charlson Comorbidity Index; TMD, temporomandibular disorder. \* Chi-squared test, significance at *p* < 0.05. † Obesity (body mass index, kg/m<sup>2</sup> ) was categorized as underweight (<18.5), normal (≥18.5 to <23), overweight (≥23 to <25), obese I (≥25 to <30), or obese II (≥30).

The adjusted HR for migraine was 2.10 (95% CI: 1.81–2.44) in the TMD group compared to the control group (Table 2). The results were consistent in subgroup analyses according to age and sex. These were also exhibited in the Kaplan–Meier analysis (Figure 2).


**Table 2.** Crude and adjusted hazard ratios (95% confidence interval) for migraine in temporomandibular disorder and control groups.

CCI, Charlson Comorbidity Index; TMD, temporomandibular disorder. \* Stratified Cox proportional hazard regression model, significance at *p* < 0.05. † Models were stratified by age, sex, income, and region of residence. ‡ The model was adjusted for obesity, smoking, alcohol consumption, systolic blood pressure, diastolic blood pressure, fasting blood glucose, total cholesterol, and CCI scores.

This study additionally analyzed the HRs for migraine with and without aura. The adjusted HR for migraine with aura did not reach statistical significance (Figure S1, Table S1). However, the adjusted HR for migraine without aura was significant in every subgroup (Figure S2, Table S2).

#### **4. Discussion**

Marklund et al. reported that subjects with TMD had a three-fold greater risk of developing frequent headaches during the 2-year longitudinal study. However, this study did not include a large population [36]. Lim et al. showed that subjects who developed TMD had more headaches compared with those who did not develop TMD and collected data by using a questionnaire [37].

The present study evaluated the association between TMD and migraine by calculating the adjusted HR of migraine after a diagnosis of TMD and used a large population-based dataset which was collected by dentists and physicians who performed objective examinations. The adjusted, statistically significant HR for migraine was 2.10 in the TMD group compared to the control group (*p* < 0.001). The results were consistent in subgroup analyses according to age and sex. These were also shown in the Kaplan–Meier analysis. These results demonstrated that the presence of TMD could increase the risk of migraine. The adjusted HR for migraine with aura did not reach statistical significance (*p* > 0.05). However, the adjusted HR for migraine without aura was significant in every subgroup (*p* < 0.001). These supplementary results could be due to an inaccurate statistical analysis. The association between TMD and migraine is known as a bidirectional link. Both diseases could induce the development of craniomaxillofacial allodynia during painful aggravation. This symptom is associated with peripheral and central sensitization. TMD could activate central sensitization and reduce the pain threshold in migraine [38]. In addition, parafunctional habits and associated painful TMD also could increase the risk for chronic migraine [39,40].

These diseases are related to the common nociceptive system. The preliminary neurons involved in migraine are linked to the first branch of the trigeminal nerve and to the trigeminocervical complex, and those involved in TMD are linked to the neurons of the third branches of the trigeminal nerve [24,41,42]. This nociceptive information converges toward the caudal nucleus of the trigeminal nerve, and from there the pathways of headache and TMD share specific central pathways involved in pain modulation, including the limbic system, brainstem nuclei, sensitive cortex, and thalamus [24]. Neurons in the trigeminal nucleus caudalis combine nociceptive input from intracranial and extracranial tissues and receive supraspinal facilitatory and inhibitory inputs [43]. The neurons integrate all these inputs, transmit the net results to the thalamus, and on to the cortex. Through this convergent point, migraine and TMD may influence each other [23].

Both conditions could share a similar genetic and hormonal basis. A previous study suggested that the association between TMD pain and migraine in women may be partially due to a modest shared genetic risk for both diseases [44]. Sex hormones, such as estrogen, may also control trigeminal nerve sensitization by modulating nociceptive mediators, such as calcitonin gene-related peptide (CGRP) [45]. The OPPERA (Orofacial Pain: Prospective Evaluation and Risk Assessment) study found a complex pattern of considerable changes in biopsychosocial function associated with changes in TMD status. Several biopsychosocial parameters improved among participants with chronic TMD despite pain persisting for years, suggesting considerable potential for ongoing coping and adaptation in response to persistent pain. These biopsychosocial factors could also influence the occurrence of migraine and mutual interaction between TMD and migraine [46].

Based on the results of the present study, clinicians could consider the possibility of improvement in migraine by the treatment of TMD. A few studies have suggested TMD treatment as a solution for migraine. Wright et al. reported that the headache disability score decreased by 17%, the consumption of analgesics was reduced by 18%, and headaches were reduced by 19%, with statistically significant differences, after TMD treatment [47]. Lim et al. showed that the treatment of TMD can improve frequent tension-type headaches associated with TMD secondary to problems of the TMJ [48].

This study had some advantages. First, the data were collected by trained and experienced dentists and physicians. Many previous studies were performed by researchers with questionnaires rather than clinicians [25,30,37,49]. Second, this study utilized a large population-based dataset, the Korean National Health Insurance Service-Health Screening Cohort, which was representative of the Korean population. There have been some studies about the association between TMD and migraine, but most of them were based on data from small populations [23,25,26,30,50]. Moreover, TMD participants were followed up for a maximum of 13 years. Third, various influential factors were adjusted to reduce surveillance bias. This study included multiple confounding factors, such as smoking, alcohol consumption, obesity, and hypertension. Lastly, both TMD and migraine are common conditions, so this study would have great clinical significance for clinicians.

This study also had some disadvantages. First, there were lower numbers of participants for subgroups through the matching procedure. Even though this study started with 514,866 participants, there were only 41 participants with migraine with aura. This may have led to inaccurate results in subgroup analyses. Second, we attempted to adjust for as many factors as possible. However, it was difficult to adjust for all factors, as not all factors were included in the dataset. Finally, the diagnosis of TMD was based on ICD-10. However, to provide the TMD phenotype of a patient population, more accurate criteria such as diagnostic criteria for temporomandibular disorders (DC/TMD) could be utilized. If the diagnosis was made by using standardized and validated criteria such as DC/TMD, the results of this study would be more trustworthy [51].

#### **5. Conclusions**

This study demonstrated that TMD patients have a higher risk of migraine. This suggests that dentists can decrease the risk of migraine in TMD patients by managing this condition properly.

However, this study did not show that all migraines could be prevented or treated by TMD treatment alone. This study simply showed that TMD could be an influential factor on migraine, so clinicians should be aware of the presence of TMD in migraine patients. If TMD symptoms are found in migraine patients, these symptoms must be managed. In addition, dentists should also determine the presence of migraine in TMD patients. If migraine is confirmed, patients should be referred to the neurology department for further evaluation and treatment.

**Supplementary Materials:** The following are available online at http://www.mdpi.com/2075-4418/10/9/724/s1, Figure S1: Subgroup analyses of crude and adjusted hazard ratios (95% confidence interval) for migraine with aura in temporomandibular disorder and control groups, Figure S2: Subgroup analyses of crude and adjusted hazard ratios (95% confidence interval) for migraine without aura in temporomandibular disorder and control groups, Table S1: Subgroup analyses of crude and adjusted hazard ratios (95% confidence interval) for migraine with aura in temporomandibular disorder and control groups, Table S2: Subgroup analyses of crude and adjusted hazard ratios (95% confidence interval) for migraine without aura in temporomandibular disorder and control groups.

**Author Contributions:** Conceptualization, S.-H.B. and H.-G.C.; data curation, C.M. and H.-G.C.; formal analysis, C.M. and H.-G.C.; funding acquisition, H.-G.C.; investigation, S.-H.B. and H.-G.C; methodology, C.M. and H.-G.C.; project administration, H.-G.C.; resources, D.-M.Y. and B.-E.Y.; software, S.-H.B. and D.-M.Y.; supervision, S.-H.B., B.-E.Y., and H.-G.C.; validation, S.-H.B. and H.-G.C.; writing—original draft, S.-H.B.; writing—review and editing, S.-H.B. All authors have read and agreed to the published version of the manuscript.

**Funding:** This work was supported in part by a research grant (NRF-2018-R1D1A1A0-2085328) from the National Research Foundation (NRF) of Korea and the Hallym University Research Fund (HURF). This work was supported by the Korea Medical Device Development Fund grant funded by the Korea government (the Ministry of Science and ICT; the Ministry of Trade, Industry, and Energy; the Ministry of Health & Welfare, Republic of Korea; and the Ministry of Food and Drug Safety).

**Conflicts of Interest:** The authors declare no conflict of interest.

#### **References**


© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).

### *Article* **Electromyography-Guided Adjustment of an Occlusal Appliance: Effect on Pain Perceptions Related with Temporomandibular Disorders. A Controlled Clinical Study**

**Simona Tecco 1, \* , Vincenzo Quinzi 2 , Alessandro Nota 1 , Alessandro Giovannozzi 3 , Maria Rosaria Abed 3 and Giuseppe Marzo 2**


**Abstract:** Background: The purpose of this study is to evaluate the effect of an electromyographyguided adjustment of an occlusal appliance on the management of Temporomandibular disorderrelated pain. Methods: Data from 40 adult patients (20 males and 20 females), who underwent treatment with occlusal appliances, were recorded. A total of 20 appliances were adjusted according to electromyographic data (group 1), while the others were adjusted by a clinical conventional procedure (group 2). Muscle pain to palpation, pain during articular movements and headache were recorded by a VAS score (from 0 to 100) before the beginning of treatment (T0), at T1 (4 weeks) and T2 (8 weeks). Results: Results showed a reduction of pain in both groups, with a better trend for group 1, where better results were achieved at T1 and maintained stability at T2, with an improved mean value regarding all parameters studied. After 8 weeks, only small recurrences started to occur in muscle pain to palpation in group 2. Conclusions: An occlusal appliance seems to be able to achieve a clinical improvement of Temporomandibular disorder (TMD)-related pain and headache, independently from the adjustment procedure adopted. However, the use of a surface electromyographic activity of masticatory muscles (sEMG) device as an aid in the calibration procedure seems to allow a better trend because the improvement of symptoms was obtained before, after the first four weeks, with an improvement in percentages of all the variables investigated. While the conventional procedure obtained later the improvement.

**Keywords:** occlusal appliance; electromyography; temporomandibular joint disorders; muscle pain; removable appliance

#### **1. Introduction**

Temporomandibular disorders (TMDs) are a heterogeneous group of clinical dysfunctions involving the masticatory muscles and/or temporomandibular joints (TMJ) and associated structures (American Association of Dental research. Policy Statement on TDM. March 2010—reaffirmed 2015—http://www.iadr.org/AADR/About-Us/Policy-Steatments/Science-Policy/Temporomandibular-Disorders-TMD, accessed on 1 February 2021). TMDs are the most prevalent orofacial pain condition, among inflammation (e.g., sinusitis), vascular compression (e.g., vascular migraines), other disorders of the musculoskeletal, neurological and/or neuropathic involvement (e.g., trigeminal neuralgia), and idiopathic trigeminal pain [1].

In general, TMD is believed to affect anywhere between 5 and 15% of adults in the population [2]. Interestingly, there is evidence that the prevalence of TMD appears to be increased in recent years [2].

**Citation:** Tecco, S.; Quinzi, V.; Nota, A.; Giovannozzi, A.; Abed, M.R.; Marzo, G. Electromyography-Guided Adjustment of an Occlusal Appliance: Effect on Pain Perceptions Related with Temporomandibular Disorders. A Controlled Clinical Study. *Diagnostics* **2021**, *11*, 667. https://doi.org/10.3390/ diagnostics11040667

Academic Editor: Timo Sorsa

Received: 15 March 2021 Accepted: 6 April 2021 Published: 8 April 2021

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

TMDs are diffused in males and females with a prevalence of female gender, and are also observed in the pediatric and adolescent population (about 11% was reported) [2].

To date, the main guidelines on TMDs management are provided by the American Association of Dental Research (AADR), which read verbatim as follows: "The signs and symptoms associated with these disorders are diverse, and may include difficulties with chewing, speaking, and other orofacial functions. They also are frequently associated with acute or persistent pain, and the patients often suffer from other painful disorders (comorbidities)".

TMDs are classified from painless clicking of the joint (Stage I) to severe degenerative bony changes (Stage V) [2]. In some cases, a patient is diagnosed with multiple diagnoses, and often those diagnoses may change as the disease progresses or resolves.

Chewing problems include intra-articular sounds, reduced range of motion of the lower jaw, pain and discomfort pressing the area around TMJ, or masticatory muscles.

Some signs and symptoms resolve spontaneously even without treatment, whereas others persist for years despite all treatment options having been exhausted [2].

Treatments include the use of occlusal appliances, sometimes surgical procedures as arthrocentesis, cognitive behavioral therapy for muscle parafunction, and other various treatments involving other specialists (physiotherapy, for example) [2].

Again, today, occlusal appliances are the most widely used intraoral devices for the management of pain, due to the reversibility of the procedure [3]. The desired outcomes of reversible therapy with occlusal appliances are essentially a reduction in the Algic component, masticatory muscle relaxation and, hopefully, reduction of headache [4]. Therefore, TMDs are also associated with the presence of intra-articular sounds (clicks) and occlusal splint often reduces their frequency because of its capability to re-establish immediately the normal condyle/disk relationship [2,5].

Therefore, the success of reversible therapy on pain appears to be paramount for long-term rehabilitation [6]. According to the literature, however, there is a lack of clarity regarding the management of occlusal appliances by the clinicians, due to different existing protocols for their adjustment. For example, Wiens (2016) has shown the technical advances over time, but did not reflect a desired clinical outcome [7]. An optimum adjustment should include point-like homogeneous contact points on the appliance, all distributed on the dental arch. The clinical effect of the occlusal appliance should be an improvement of signs and symptoms.

Undoubtedly, it is worth mentioning that the clinical effects of occlusal appliances for the different types of disorders may suffer from the role played by the practitioner itself during the clinical conventional procedure of its adjustment [7,8].

One of the emerging digital procedures for the adjustment of intraoral appliances or prostheses is based on the analysis of surface electromyographic activity of masticatory muscles (sEMG), which monitor the synergistic action of muscles in order to evaluate their balanced function [8,9]. This approach is based on data that highlight how symmetry in the electromyographic activity of the masticatory muscles is necessary for oral [9,10] as well as functional rehabilitation [11]. However, on these digitized procedures, there are no studies that have evaluated the results from a clinical and symptomatological point of view (on pain).

Thus, the purpose of this observational study was to analyze the effects of an electromyography-guided adjustment of an occlusal appliance on muscular pain comparing it with a standard procedure in a control group.

#### **2. Materials and Methods**

The present observational protocol was approved by the Ethics Committee of the University of L'Aquila, Italy (Document DR206/2013, dated 10 January 2014). Data from a sample of 40 subjects, 20 males and 20 females, aged between 20 and 30 years old (average 25 years), who were going to receive an occlusal appliance for the management of TMD at George Eastman Dental Hospital in Rome (Italy) were selected for the present study. All the patients complained of muscle tension headache, associated with masticatory muscle pain to palpation, as well as pain during mandibular movements. None of them was affected by disc displacement, or degenerative joint disease. All patients were treated with an individualized 1.5 mm thick occlusal appliance, made of a heat-cured acrylic resin (Duran®, Scheu-Dental Technology, Iserlohn, Germany), applied in their lower jaw (Figure 1).

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**Figure 1.** Individualized 1.5 mm thick occlusal appliance, made of a heat-cured acrylic resin (Duran®, Scheu-Dental Technology, Iserlohn, Germany).

In the study group (the study group) (20 patients) the calibration was performed by achieving a condition of muscular balance and relaxation according to sEMG data, whereas in the control group (the control group) (20 patients) it was performed by a standard procedure aimed to achieve homogeneous point-shaped dental contacts on the appliance [12]. The patients were instructed to wear the appliance 22 h per day, removing it only for meals and were treated by the same expert operator (the author A.G.) In the study group, sEMG was performed using TEETHAN® (Teethan S.p.a. Garbagnate Milanese, Milan, Italy) a 4-channel wireless electromyograph, featuring surface electrodes placed at the level of the masseter muscles and anterior temporalis muscle [13,14]. All patients underwent clinical follow up during the subsequent weeks, and painful muscles at palpation, pain arising during mandibular function (functional pain) and headache, were recorded by using the VAS scale, on a range of scores from 0 to 100. Follow-ups were scheduled after 4 weeks (T1) and after 8 weeks (T2) from in the initial phase.

#### *Data Handling and Statistical Analyses*

The sample size was evaluated a priori by performing analysis for estimating the minimum number of subjects to achieve a statistical power of 80% with alpha 0.05 on the comparison between groups for the primary outcome. The results showed that a minimum of 18 subjects per group was required. Applying the Shapiro–Wilk W test normal distribution of data was confirmed for the variables muscular pain at palpation (Shapiro– Wilk W = 0.95; *p* = 0.14) and headache (Shapiro–Wilk W = 0.96; *p* = 0.19). Differently, for functional complaints, data did not show a normal distribution (Shapiro–Wilk W = 0.92; *p* = 0.008). Descriptive statistics for the variables muscular pain at palpation and headache included mean and standard deviation. While functional pain was described as median with 25th and 75th percentiles. In order to analyze the variables of muscular pain at palpation and headache, a *t*-test for independent samples was performed to analyze the differences between the groups at each time point while a one-way ANOVA test was adopted to analyze the significance of changes over time. When significant, a post-hoc Tukey test was employed to further illuminate the statistically significant differences. For the variable of functional pain, the Friedman test and the Wilcoxon signed rank test were used to evaluate intra-groups differences; while the Mann–Whitney test was adopted to evaluate between groups differences at T0, T1 and T2. Statistical analyses were performed

with the software StatPlus Pro for MAC (build 7.3.3.0/Core v7.3.32; AnalystSoft Inc., 2020, Walnut, CA, USA). For each test, p was set at 0.05 level.

#### **3. Results**

Table 1 reports descriptive statistics for the variables muscular pain at palpation and headache. Table 2 reports descriptive statistics for the variable functional pain.

**Table 1.** Descriptive statistic for muscular pain at palpation and headache. VAS scores mean ± standard deviation (SD).


**Table 2.** Descriptive statistic for functional pain. VAS scores, median, 25th and 75th percentiles.


\* *p* < 0.05.

#### *3.1. Muscular Pain at Palpation*

At T0, VAS score averaged 54 in group 1 and 60 in group 2 (range: 10–90 for the whole sample), without any statistically significant difference between the two groups. While at T2, a significantly lower mean VAS score was observed in the study group respect to the control group (mean difference = −21; 95% C.I. = −43.04–1.04; t = 3.22; *p* < 0.05) (Figure 2). **2021**, , x FOR PEER REVIEW 5 of 12

**Figure 2.** Muscle pain at palpation (mean VAS scores and SD) in the two groups. \* indicates between groups statistically significant differences (*p* < 0.05).

Considering the trend of the variable in each group over time, VAS significantly decreased at T1 in the test group, achieving a mean value of 15 (T0-T1 mean difference = 39;

95% C.I. = 16.95–61.04; t = 5.99; *p* < 0.01), and it remained almost stable at T2, with a mean value of 13 (T0-T2 mean difference = 41; 95% C.I. = 18.95–63.04; t = 6.29; *p* < 0.01) (Figure 3). **2021**, , x FOR PEER REVIEW 6 of 12

**Figure 3.** Muscle pain at palpation and headache (mean VAS scores and SD) in the study group, with statistically significant differences overtime (\* = *p* < 0.05; \*\* = *p* < 0.01).

In the control group, it scored from 60 to 24 at T1 (T0-T1 mean difference = 36; 95% C.I. = 13.95–58.04; t = 5.53; *p* < 0.01), and 34 at T2 (T0-T2 mean difference = 26; 95% C.I. = 3.95–48.04; t = 3.99; *p* < 0.01) (Figure 4). **2021**, , x FOR PEER REVIEW 7 of 12

#### *3.2. Functional Pain*

− − At T0, the median VAS score in the study group 29.5, and it was 52.5 in the control group, (range: 10–90 for the whole sample), without any statistically significant difference between the two groups. At T1 the study group showed a statistically significant lower VAS score, with respect to the control group (Mann–Whitney U = 282,000; *p* = 0.026) (Table 2). No statistically significant differences were observed at T2. Considering the trend over time, the study group experimented with a statistically significant reduction of pain over time, from T0 to T1 (Wilcoxon ranks z = −3.82; *p* < 0.01); and from T0 to T2 (Wilcoxon ranks z = −3.57; *p* < 0.01) (Figure 5).

VAS mean score

**2021**, , x FOR PEER REVIEW 8 of 12

**2021**, , x FOR PEER REVIEW 8 of 12

**Figure 5.** Box plots represent median, 25th and 75th percentiles of VAS scores for functional pain in the study group over time. \* indicates statistically significant differences, *p* < 0.05.

− − − The control group showed a statistically significant decrease of VAS score from T0 to T1 (Wilcoxon ranks z = −3.40; *p* < 0.01); from T0 to T2 (Wilcoxon ranks z = −3.74; *p* < 0.01); and from T1 to T2 (Wilcoxon ranks z = −3.04; *p* < 0.01) (Figure 6). − − − − − −

**Figure 6.** Box plots represent median, 25th and 75th percentiles of VAS scores for functional pain in the control group over time. \* indicates statistically significant differences, *p* < 0.05.

#### *3.3. Muscular Tension Headache*

The trend of headache VAS score for both the groups, at any stage, is depicted in Figure 7.

**Figure 7.** Headache at palpation (mean VAS scores and SD) in the two groups. \*\* indicates between groups statistically significant differences (*p* < 0.01).

At T0, VAS averaged 35 in group 1, and 44 in group 2 (range: 10–70 for the whole sample) without any statistically significant difference between the two groups. At T1, the study group showed a significantly lower mean VAS score, respect to the control group (mean difference = 27; 95% C.I. = 42.34–11.65; t = 5.95; *p* < 0.01). However, there was not any statistically significant difference between the two groups at T2. Considering the trend over time, VAS significantly decreased in the study group till a value of 11 (mean difference T0-T1 = 24; 95% C.I. = 8.65–39.34; t = 5.29; *p* = 0.0001) and remained almost stable at T2 (mean difference T0-T2 = 23; 95% C.I. = 8.25–38.94; t = 5.20; *p* = 0.0001) (Figure 3). Differently, in the control group VAS scores decreased overtime more slowly and became 38 at T1, and 22 at T2 (T0-T2 mean difference = 22; 95% C.I. = 6.65–37.34; t = 4.85; *p* = 0.00059) (Figure 4). The percentages of VAS score improvement for all the considered variables in the two groups are reported for both the groups in Table 3.

**Table 3.** Intra-group differences expressed in percentage for both the groups.


#### **4. Discussion**

This observational study was aimed to compare the effect of occlusal appliances adjusted with sEMG aid (the study group) versus the conventional adjustment procedure (the control group) in the management of TMDs related pain.

The comparison of the VAS scores between the two groups showed some improvements for both groups. However, it seems that there was a better trend for the study group, respect to the control group. For the study group, the improvement of symptoms was obtained after the first four weeks (T0-T1 difference), with an improvement in percentages of all the variables investigated. While the control group showed a slightly different trend after the first four weeks of treatment, with a lower improvement (in percentage) than the study group. In addition, the control subjects showed a recurrence of light symptoms as shown by the score obtained for muscle palpation after the first four weeks, between T1 and T2, but results indicate that there was a statistically significant improvement of this variable from T0 to T2. Overall, in conclusion, between T1 and T2 there were positive results, for both the groups, according to all the other variables.

Thus, the present observations confirm that the most common and widespread therapy procedure for TMDs consisting of the use of occlusal appliances, is useful in controlling the pain related to altered muscular activity [7,8]. Thus, the present findings seem to support the principle that occlusal appliances could be able to maintain a primary role in the symptomatic treatment of TMD patients, allowing a change in the distribution of joint load vectors and relaxation of muscle fibers.

The TMJ is located near a major nerve in the face, which is at the center of a network of nerves that connect throughout the face, head and neck. So when the TMJ is affected, pain can spread throughout the face, head and neck (the eyes, ears, mouth, forehead, cheeks, tongue, teeth and throat). Even the muscles of the neck can be involved.

TMDs are diffused in males and females with a prevalence of female gender [15]. They are also observed in the pediatric and adolescent population, (about 11% was reported) [2] in which they were related also to poor cervical posture, [16] and in some cases occlusal appliances were also referend to influence the general mandibular posture [17]. Diagnosis is made through an anamnestic questionnaire and clinical exam with palpation [18].

For the study group, the best results were obtained after the first four weeks (T0-T1 difference), with an improvement in percentages of all the variables investigate: in particular, muscular pain at palpation improved by 72.2%, headache by 68.5% and functional pain

by 66.6%, with statistically significant differences. The control group showed a slightly different trend after the first four weeks of treatment, with a lower improvement (in percentage) than the study group: muscular pain at palpation improved by 60%, headache by 13% and functional pain by 36%. In the control group, headache showed an improvement later than other symptoms, as results indicate that there was a statistically significant improvement of this variable from T0 to T2 in group 2. After the first four weeks, between T1 and T2, there was a recurrence of light symptoms as shown by the score obtained by the control group for muscle palpation (41% worsening between T1 and T2) (Figure 4). Overall, between T1 and T2, there were positive results for both the groups, according to all the other variables. It can be concluded from the present data that the general outcome was an overall improvement for both groups between T0 and T2.

The results observed in the study group, where the occlusal appliance adjustment was aided by sEMG, seem to suggest that a better adjustment of the appliance was performed, helping the clinician to increase the predictability in the balance of the bilateral contacts of the occlusal appliance, as previously suggested [19–22]. The use of electromyography to adjust an occlusal splint is only one of the techniques that can be used for the adjustment of an occlusal splint, so the present results cannot be generalized for all the other technique.

Multiple designs are available, such as hard, soft, and anterior repositioning splint. At present, there is no consensus on which design is superior, as results from different studies are equivocal in terms of the efficacy of different designs of occlusal splints [2].

It should be considered that the traditional procedure applied in the control group, without using any digital equipment, could bring results more dependent on the practitioner's expertise. The worsening percentage for muscle pain to palpation, registered between T1 and T2 in group 2 may be justified by the fact that, after an initial unlocking of the occlusion and subsequent improvement of the symptomatology, the modified occlusion could have determined the onset of new symptoms. For this reason, occlusal appliances are generally preferred and recommended against irreversible treatments, as modifying the occlusion in the long term could expose the patient to the risk of recurrence of symptomatology. On the other hand, the sEMG seems a useful method for improving the quality and predictability of the appliance adjustment, even though it also requires a learning curve for its use.

#### **5. Conclusions**

An occlusal appliance seems to be able to achieve a clinical improvement of TMDs related pain and headache, independently from the adjustment procedure adopted.

However, the use of an sEMG device as an aid in the calibration procedure seems to allow a better trend because the improvement of symptoms was obtained before and after the first four weeks, with an improvement in percentages of all the variables investigated. Meanwhile, the conventional procedure was obtained later than the improvement.

Future studies will clarify the effects of other material-based appliances or adjustment procedures for clinics.

**Author Contributions:** Conceptualization, S.T., A.G. and A.N.; methodology, S.T., A.G., M.R.A., A.N.; validation, S.T., A.N., V.Q. and G.M.; formal analysis, S.T. and A.N.; investigation, A.G. and M.R.A.; resources, A.G. and M.R.A.; data curation, S.T. and A.N.; writing—original draft preparation, S.T., A.G. and A.N.; writing—review and editing, S.T. and A.N.; supervision, S.T. and V.Q.; project administration, V.Q. and G.M.; All authors have read and agreed to the published version of the manuscript.

**Funding:** This research received no external funding.

**Institutional Review Board Statement:** The study was conducted according to the guidelines of the Declaration of Helsinki and approved by the Institutional Review Board (or Ethics Committee) of the University of L'Aquila, but approval was waived for this study, due to retrospective construction.

**Informed Consent Statement:** Informed consent was obtained from all subjects involved in the study. Written informed consent has been obtained from the patients to publish this paper.

**Data Availability Statement:** The data that support the findings of this study are available from the University of L'Aquila, but restrictions apply to the availability of these data, which were used under license for the current study, and so are not publicly available. Data are however available from the authors upon reasonable request and with permission of the University of L'Aquila partner.

**Acknowledgments:** The authors acknowledge Ettore Accivile for clinical support.

**Conflicts of Interest:** The authors declare no conflict of interest.

#### **References**


### *Article* **Electromyographic Patterns of Masticatory Muscles in Relation to Active Myofascial Trigger Points of the Upper Trapezius and Temporomandibular Disorders**

**Grzegorz Zieli ´nski 1 , Aleksandra By´s 1 , Jacek Szkutnik 2 , Piotr Majcher <sup>1</sup> and Michał Ginszt 1, \***


**Abstract:** The presented study aimed to analyze and compare the electromyographic patterns of masticatory muscles in subjects with active myofascial trigger points (MTrPs) within upper trapezius, patients with temporomandibular disorders (TMDs) and healthy adults. Based on the diagnostic criteria of MTrPs according to Travell & Simons and the Research Diagnostic Criteria for Temporomandibular Disorders, 167 people were qualified for the study. Subjects were divided into 3 groups: with active MTrPs in the upper trapezius, with diagnosed temporomandibular disorders (TMDs) and healthy adults. Measurements of the bioelectric activity of the temporalis anterior (TA) and masseter muscle (MM) were carried out using the BioEMG III ™. Based on statistical analysis, significantly lower values of TA resting activity were observed among controls in comparison to MTrPs (1.49 µV vs. 2.81 µV, *p* = 0.00) and TMDs (1.49 µV vs. 2.97 µV, *p* = 0.01). The POC index values at rest differed significantly between MTrPs and TMDs (86.61% vs. 105%, *p* = 0.04). Controls presented different electromyographic patterns within AcI in comparison to both MTrPs (4.90 vs. −15.51, *p* = 0.00) and TMDs (4.90 vs. −16.49, *p* = 0.00). During clenching, the difference between MTrPs and TMDs was observed within MVC TA (91.82% vs. 116.98%, *p* = 0.02). TMDs showed differences within AcI in comparison to both MTrPs group (−42.52 vs. 20.42, *p* = 0.01) and controls (−42.52 vs. 3.07, *p* = 0.00). During maximum mouth opening, differences between MTrPs and TMDs were observed within the bioelectric activity of masseter muscle (16.45 µV vs. 10.73 µV, *p* = 0.01), AsI MM (0.67 vs. 11.12, *p* = 0.04) and AcI (13.04 vs. −3.89, *p* = 0.01). Both the presence of MTrPs in the upper trapezius and TMDs are related to changes in electromyographic patterns of masticatory muscles.

**Keywords:** electromyography; temporalis anterior; masseter muscle; myofascial pain; myofascial trigger points; trapezius

### **1. Introduction**

Myofascial trigger points (MTrPs) are defined as hyperactive points located in the tense area of the skeletal muscle or its fascia. MTrPs are associated with the development of myofascial pain syndrome (MPS), causing local or referred pain [1]. The compression stimulation of MTrPs may induce a local pain sensation or a referred pain response [2]. The development of MTrPs may be caused by the accumulation of microtraumas within the muscle or its direct injury [1,3]. Muscle overload and consequently the formation of MTrPs, is the result of prolonged or repeated low-amplitude muscle contractions, eccentric contractions and maximal or submaximal muscle contractions [3,4]. Moreover, MTrPs can arise as a result of nutrient deficiencies, hormonal disorders or muscle imbalances [4], fatigue and even viral infections [2,5]. The pathology mentioned above may be related to tissue hypoxia processes in the MTrPs environment [6] when the concentration of

**Citation:** Zieli ´nski, G.; By´s, A.; Szkutnik, J.; Majcher, P.; Ginszt, M. Electromyographic Patterns of Masticatory Muscles in Relation to Active Myofascial Trigger Points of the Upper Trapezius and Temporomandibular Disorders. *Diagnostics* **2021**, *11*, 580. https:// doi.org/10.3390/diagnostics11040580

Academic Editors: Daniel Fried and Luis Eduardo Almeida

Received: 23 February 2021 Accepted: 20 March 2021 Published: 24 March 2021

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

inflammatory mediators increases near MTrPs [7]. The above factors may lead to increased nociceptor activity, which results in increased pain response [8]. It is estimated that the prevalence of MPS in clinical populations varies widely, ranging from 9% to 85% [9].

The temporomandibular joint (TMJ) is a bilateral joint composed of the temporal bone′ s articular surface and the head of the mandible [10]. TMJ is separated into two synovial joint cavities by an articular disc, allowing a smooth articulation between the mandibular condyle and the articular eminence. Moreover, the TMJ disc increases the contact area between opposing articulating surfaces, distributing lower stresses to a larger surface area in the joint [11]. The anterior portion of the TMJ disc is attached to the joint capsule, articular eminence, anterior condyle and the lateral pterygoid′ s upper area. The posterior portion attaches superiorly to the temporal bone and inferiorly to the posterior condyle. Several ligaments, TMJ disc, articular capsule and masticatory muscles stabilize the TMJ and manage the TMJ forces [12]. Both TMJ dysfunction and abnormalities within masticatory muscles may lead to Temporomandibular Disorders (TMDs). TMDs affect the TMJ, masticatory muscles and/or surrounding tissues and are mainly characterized by pain, acoustic symptoms and limited, incorrect or parafunctional muscle activity [13]. The most common conditions comprising TMDs are myofascial pain, disc displacements and TMJ arthritides [13]. In addition, MPS associated with the presence of MTrPs accounts for approximately 45% of all reported cases of TMDs [14]. Moreover, TMDs significantly reduced life quality and are recognized by the World Health Organization as the third most common dental disease [15,16]. The American National Institute of Dental and Craniofacial Research estimates that TMDs affect 5 to 12% of the population, more often women than men [17]. However, TMDs′ etiology is multifactorial and still unclear, with some suggesting that due to their association with other somatic syndromes, TMDs may be part of the same phenomenon [18].

The phenomenon of referred pain is the subject of discussion concerning the stomatognathic system disorders. However, the mechanisms causing this phenomenon have not been clearly explained [19]. Trigger points in the upper trapezius have been associated with tension-type headache episodes [20]. Therefore, through the mechanism of referred pain, MTrPs in the upper trapezius may be responsible for developing pain within the masticatory muscles. The association between TMDs and disorders within cervical spine muscles remaining unclear and there are just several studies confirming the relationship between MTrPs in the cervical muscles and TMDs [21]. Previous reports indicate the coexistence of MTrPs in the neck muscles in patients with TMDs [14,19,22]. However, according to the authors′ knowledge, there is a lack of studies that have analyzed the relationship between active MTrPs of the trapezius muscle and the masticatory muscle activity. Thus, the presented study aimed to determine, analyze and compare electromyographic patterns of masticatory muscles in relation to active MTrPs of the upper trapezius and TMDs. Based on the above-mentioned interactions between MTrPs in cervical spine muscles and the occurrence of TMDs, we hypothesize that MTrPs within the upper trapezius significantly influence the activity of the masticatory muscles. We also assume that the electromyographic patterns of masticatory muscles in individuals with MTrPs within trapezius and TMDs patients will differ from healthy individuals.

#### **2. Materials and Methods**

The study was carried out in accordance with the recommendations of the Helsinki Declaration and with the consent of the Bioethical Commission of the Medical University of Lublin (approval number KE-0254/346/2016, date of approval 23.11.2016). All participants were informed about the aim of the study and have given written consent for the research.

The inclusion criteria used in the presented study were: age range 18–35 years, good or very good general health status according to the RDC/TMD questionnaire, the presence of active MTrPs in the upper trapezius and absence of any type of TMDs (MTrPs group), presence of pain-related TMDs based on the Research Diagnostic Criteria for Temporomandibular Disorders RDC/TMD [23] without MTrPs in the upper trapezius (TMDs group) and absence of TMDs and active and/or latent MTrPs in the head and neck muscles (control group).

The diagnostic of pain-related TMDs was performed by an experienced dentist with a specialization in dental prosthetics. The TMDs group included only patients with masticatory muscle disorders diagnosed with myalgia—myofascial pain. Patients with temporomandibular joint disorders (e.g., joint pain, disc disorders, joint diseases), other masticatory muscle dysfunctions (e.g., contracture, tendonitis, myositis, spasm, hypertrophy), fibromyalgia, headaches attributed to TMD and coronoid hyperplasia were excluded from the presented study [24].

The presence of active MTrPs within the upper trapezius was established by the following diagnostic criteria according to Travell and Simons [2].


The following exclusion criteria were used: skin diseases in the head and neck area, neurological disorders in the head and neck area, neoplastic diseases (regardless of type and location), head and neck injuries within the last 6 months before the examination, surgical treatment in the area of head and neck in the last 6 months before the examination, class II and III according to Angle′ s classification, class I malocclusions patients, open bite, having an orthodontic appliance, lack of four support zones in dental arches, lack of more than four teeth within both dental arches and possession of dental prostheses (regardless of type). After applying the above criteria, 167 people (age 26 ± 8 years) were divided into three groups: 60 in the MTrPs group, 47 in the TMDs group and 60 controls (Table 1).


**Table 1.** General characteristics of participants.

\* Significant difference.

In the next stage, an electromyographic examination was carried out, which was always performed in the morning hours (9 am–11 am) to reduce the impact of the daily bioelectric variability of muscles on the results. The subjects sat on the dental chair, the head rested on the headrest and the torso was perpendicular to the ground. The lower limbs were straight, relaxed and parallel. Before electrode placement, the skin was cleansed with a 90% ethyl alcohol solution to reduce electrode–skin impedance. Ag/AgCl electrodes (SORIMEX, Poland) with a diameter of 30 mm and a conductive surface of 16 mm were used. The placement of the surface electrodes was performed following the Surface Electromyography for Non-invasive Assessment of Muscles (SENIAM) project [25]. The surface electrodes were placed on o the temporalis anterior (TA) and the superficial part of the masseter muscle (MM) in accordance with the course of the muscle fibers, according to the placement technique described by Ferrario et al. [26]. The reference electrode was placed on the forehead (Figure 1). An 8-channel BioEMG IIITM surface electromyography apparatus with BioPak Measurement System (BioResearch Associates, Inc. Milwaukee, WI, USA) was used for the study.

**Figure 1.** Electrodes placement during the electromyographic examination.

The activity of the masticatory muscles (TA, MM) was recorded in the following protocol: during resting mandibular position (10 s), during maximum voluntary clenching (three clenches of 3 s, each with a 2-s break), during maximum voluntary clenching on dental cotton rollers (three clenches of 3 s, with a 2-s break) and during maximum mouth opening (three abductions of 3 s, with a 2-s rest between) [27,28].

The electromyographic signals were amplified and purified from 99% of the noise scale on a linear scale using the BioPak digital NoiseBuster filter.

Based on the bioelectric data obtained, the following indices were calculated according to standardized protocols:

 • MCV (maximum voluntary contraction) based on the formula [28]:

MCV = [voluntary teeth clenching/voluntary teeth clenching on cotton rollers] × 100%

• POC (percentage overlapping coefficient) based on the formula [29]:

POC = [(MMright + TAright)/(MMleft + TAleft)] × 100%

• AsI (asymmetry index) based on the formula [30]

− ASI = [(RMSright − RMSleft)/(RMSright + RMSleft)] × 100

 • AcI (activity index) based on the formula [30]:

> − ACI = [(RMSmasseter − RMStemporal)/(RMSmasseter + RMStemporal)] × 100

 • TC (torque) based on the formula [31]:

$$\text{TC} = \left[ (\text{TA}\_{\text{right}} + \text{MM}\_{\text{left}}) - (\text{TA}\_{\text{left}} + \text{MM}\_{\text{right}}) \right] \times 100\%$$

The checklist developed by the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) initiative was used to assess the methodological quality of the presented study [32]. IBM SPSS Statistics 21 software was used for statistical analysis. First, the normality of the distribution of variables was verified using the Shapiro-Wilk test and the Kolmogorov–Smirnov test (with Lillierfors correction). All the distributions were abnormal; therefore, the Kruskal—Wallis test was used. The significance level was set at 0.05. When there were significant differences between the analyzed groups, the post-hoc test was applied (Dunn′ s Test).

#### **3. Results**

#### *3.1. General Characteristics of Participants*

There were no significant differences in the number of participants and gender between study groups and controls. Post-hoc analysis showed considerable age differences between the TMDs and the rest of the groups (MTrPs group and controls) (Table 1).

There were significant differences in the mandibular range of motion (ROM) between TMDs group vs. controls and TMDs vs. MTrPs. TMDs presented a decrease within the maximum comfortable pain-free opening (MCO), maximum mouth opening (MMO) and protrusion compared to other groups. Moreover, statistical analysis showed differences in the right lateral excursion (RLE) between the TMDs and controls. The mean mandibular ROM values were similar between MTrPs and controls (Table 2).

**Table 2.** Comparison of the mean values (± SD) of mandibular range of motion during maximum comfortable pain-free opening (MCO), maximum mouth opening (MMO), right lateral excursion (RLE), left lateral excursion (LLE) and protrusion between groups.


\* Significant difference.

#### *3.2. Electromyographic Analysis of Resting Masticatory Muscle Activity*

Based on statistical analysis, significantly lower values of TA resting activity were observed among controls in comparison to MTrPs (Controls: 1.49 µV vs. MTrPs: 2.81 µV; *p* = 0.00) and TMDs (Controls: 1.49 µV vs. TMDs: 2.97 µV; *p* = 0.01), as presented in Table 2. The values of POC index at rest differed significantly between MTrPs and TMDs (MTrPs: 86.61% vs. TMDs: 105%; *p* = 0.04). Significant differences in electromyographic patterns between MTrPs and the other groups were also observed for the AsI TA (MTrPs: −14.72 vs. TMDs: −1.48 and Controls: −4.48; *p* = 0.00 and *p* = 0.01, respectively) and TC (MTrPs: −90.43% vs. TMDs: 0.28% and Controls: −3.67%; *p* = 0.02 and *p* = 0.03, respectively). Controls presented different electromyographic patterns within AcI in comparison to both MTrPs (Controls: 4.90 vs. MTrPs: −15.51; *p* = 0.00) and TMDs (Controls: 4.90 vs. TMDs: −16.49; *p* = 0.00) (Table 3).


**Table 3.** Comparison of the mean values (± SD) of resting bioelectric activity of temporalis anterior (TA), masseter muscle (MM) and electromyographic indices between groups.

\* Significant differences (*p* < 0.05) between groups (Kruskal-Wallis test).

#### *3.3. Electromyographic Analysis of Masticatory Muscle Activity during Clenching*

During clenching, difference between MTrPs and TMDs was observed within bioelectric activity of masseter muscle (MTrPs: 120.43 µV vs. TMDs: 68.30 µV; *p* = 0.00) and MVC TA (MTrPs: 91.82% vs. TMDs: 116.98%; *p* = 0.02). Moreover, differences between TMDs and controls were obserwed within bioelectric activity of TA (TMDs: 89.56 µV vs. Controls: 118.37 µV; *p* = 0.03) and MM (TMDs: 68.3 µV vs. Controls: 133.63 µV; *p* = 0.00). In addition, TMDs showed differences within AcI in comparison to both MTrPs group (TMDs: −42.52 vs. MTrPs: 20.42; *p* = 0.01) and controls (TMDs: −42.52 vs. Controls: 3.07; *p* = 0.00) (Table 4).

**Table 4.** Comparison of the mean values (± SD) of bioelectric activity of temporalis anterior (TA), masseter muscle (MM) and electromyographic indices between groups during clenching.


\* Significant differences (*p* < 0.05) between groups (Kruskal-Wallis test).

#### *3.4. Electromyographic Analysis of Masticatory Muscle Activity during Maximum Mouth Opening*

During maximum mouth opening, differences between MTrPs and TMDs were observed within the bioelectric activity of masseter muscle (MTrPs: 16.45 µV vs. TMDs: 10.73 µV; *p* = 0.01), AsI MM (MTrPs: 0.67 vs. TMDs: 11.12; *p* = 0.04), AcI R (MTrPs: 14.35 vs. TMDs: −0.23; *p* = 0.03), AcI L (MTrPs: 11.32 vs. TMDs: −11.06; *p* = 0.00) and AcI (MTrPs: 13.04 vs. −3.89; *p* = 0.01). Moreover, TMDs showed differences within AcI L in comparison to controls (TMDs: −11.06 vs. Controls: 7.65; *p* = 0.02) (Table 5). In terms of other indices, the differences between the studied groups did not reach the assumed significance level (Tables 3–5).


**Table 5.** Comparison of the mean values (± SD) of bioelectric activity of temporalis anterior (TA), masseter muscle (MM) and electromyographic indices between groups during maximum mouth opening.

\* Significant differences (*p* < 0.05) between groups (Kruskal–Wallis test).

#### **4. Discussion**

The referred pain induced from active MTrPs in the neck muscles shared a similar pain pattern as spontaneous TMDs [19]. Thus, MTrPs in the upper trapezius may be responsible for the development of pain within the masticatory muscles. However, the association between TMDs and disorders within trapezius remaining unclear. Thus, the presented study aimed to determine, analyze and compare electromyographic patterns of masticatory muscles in relation to active MTrPs of the upper trapezius and TMDs. To our knowledge, this is the first study to evaluate electromyographic patterns of masticatory muscles in relation to active myofascial trigger points of the upper trapezius and temporomandibular disorders. We hypothesized that MTrPs within the upper trapezius significantly influence the activity of the masticatory muscles. We also assumed that the electromyographic patterns of masticatory muscles in the group with MTrPs within trapezius and TMDs patients would be different from healthy individuals.

During the electromyographic examination, significantly higher values of resting activity within temporalis anterior were observed among both MTrPs and TMDs patients in comparison to healthy individuals. The above-mentioned association was not observed within masseter muscle. Moreover, the differences within the distribution of resting muscle activity between the temporalis anterior and the masseter muscle significantly influenced activity index values in both studied groups. Both MTrPs and TMDs patients showed negative (−). AcI values, compared to healthy individuals whose AcI values were slightly positive (+). Negative values of AcI among MTrPs and TMDs indicate the predominance of the temporalis anterior during rest, in contrast to healthy controls with slight positive AcI values (masseter muscle advantage). However, the electromyographic patterns of teeth clenching differ significantly between MTrPs and TMDs patients regarding the activity index. The positive values of AcI during clenching showed the predominance of masseter muscle activity among individuals with active MTrPs within trapezius, unlike TMDs patients with negative values of AcI, indicating the predominance of the temporalis anterior during clenching tasks. In addition, the MVC index within the TA was significantly lower in MTrPs patients than in TMDs and healthy participants. Different electromyographic patterns between TMDs and MTrPs were also observed during maximum mouth opening in terms of bioelectric activity of the masseter muscle, as well as AsI MM and AcI indices.

The above changes in the masticatory muscle activity seem to be related to the integrated pain adaptation model, which assumes a new muscle activation strategy to maintain homeostasis [33]. The presented model postulates that the key factor in maintaining homeostasis may be the need to minimize the generation of further pain at rest or during movement. Thus, changes in the electromyographic patterns of masticatory muscles may be associated with the presence of pain due to active MTrPs. Previous studies indicate the association between the active MTrPs within masticatory muscles, increased muscle

activity during rest and a decrease in sEMG values during teeth clenching [34–36]. The above-mentioned association may be linked with TA resting activity obtained in our work, both in TMDs and MTrPs groups, showing a similar resting activity pattern in both groups of patients.Note, however, that the AcI values differed significantly between MTrPs and TMDs during clenching tasks. The predominance of TA muscle activity in TMDs patients could be caused by reducing contraction patterns within the MM, which seems to be confirmed in the Mapelli et al. study [37]. However, the MTrPs group presented an entirely different electromyographic pattern with decreased temporalis anterior activity, both during teeth clenching and maximum mouth opening. We suspect that this altered pattern may be related to the occurrence of active MTrPs in the trapezius muscle, which, as a result of a referred pain mechanism, alters TA activity. Our suppositions seem to be in line with the referred pain patterns presented by Travell and Simons, in which the temporal area is one of the most commonly painful regions raised from MTrPs located in the upper trapezius [38]. As, based on our data, we cannot directly confirm this mechanism, we should treat this as a supposition and future studies should test if this mechanism is true.

Our hypothesis that MTrPs within the upper trapezius significantly influence the masticatory muscle activity seems to be confirmed in the presented research. This notion is in line with the results of previous findings showing the relationship between MTrPs in the upper trapezius and tension-type headache episodes [20,39–43]. In addition, the presence of bilateral pain hypersensitivity in the trigeminal region in patients with idiopathic neck pain was observed in La Touche et al. study, which suggests a sensitization process of the trigeminocervical nucleus [44]. Moreover, a study conducted by De-la-Llave-Rincon et al. suggests that chronic pain in the cervical region influences the formation of latent trigger points in the masticatory muscles [45]. The relationship between the masticatory muscles and the pain within the cervical area seems to be confirmed by Testa et al. [46]. In the above-mentioned study, patients with chronic pain in the cervical spine region presented the altered distribution of the electromyographic patterns within masticatory muscles during clenching. The authors also suggest that changes in the activity of the masticatory muscles observed in patients with cervical spine pain patterns may affect the development of TMDs.

Our assumption that the electromyographic patterns of masticatory muscles in the group with MTrPs within trapezius and in TMDs patients will be different from healthy individuals seems to be justified by obtained results. However, we cannot clearly explain the significant differences observed between MTrPs and TMD within the electromyographic patterns, which requires further research.The presented study has several limitations. Firstly, the diagnostics criteria for TMDs were changed to DC/TMD in 2014. However, there is no validated Polish version of the DC/TMD so far. Therefore, we used the clinical examination based on the Axis-I protocol of the RDC/TM. Moreover, the Axis I section of the RDC/TMD form is widely used in the current literature in high-impact journals [47–50]. Secondly, the study sample consists of young adults aged 18 to 35. Thus, future research should include a population with an expanded age range.

#### **5. Conclusions**

Both the presence of MTrPs in the upper trapezius and TMDs are related to changes in electromyographic patterns of masticatory muscles. Future research is needed to explain the above differences and underlying mechanisms.

**Author Contributions:** Conceptualization, G.Z., A.B. and M.G.; data curation, G.Z., A.B. and M.G.; investigation, G.Z., A.B., J.S. and M.G., methodology, M.G. and G.Z.; project administration, P.M. and M.G.; resources, P.M. and J.S.; supervision, M.G.; writing—original draft, G.Z., A.B. and M.G.; writing—review and editing, M.G. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research received no external funding.

**Institutional Review Board Statement:** The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Bioethical Commission of the Medical University of Lublin (approval number KE-0254/346/2016, date of approval 23.11.2016).

**Informed Consent Statement:** Informed consent was obtained from all subjects involved in the study.

**Data Availability Statement:** The data presented in this study are available on request from the corresponding author.

**Acknowledgments:** We acknowledge support from the Medical University of Lublin for Open Access Publishing.

**Conflicts of Interest:** The authors declare no conflict of interest.

#### **References**

