Temporomandibular disorders in adolescents with headache

Background. Headache is a common complaint in all age groups and is a frequent cause of medical consultations and hospitalization. Objectives. The aim of this study was to evaluate the prevalence of bite and non-bite parafunctions as well as the signs and symptoms of temporomandibular disorder (TMD) in adolescents presenting with primary headaches. Material and methods. Parents of adolescents presented with headaches to the Department of Developmental Neurology within a 12-month period were asked to complete a questionnaire developed by the authors of this study. Of the 1000 patients evaluated, 19 females and 21 males, aged 13 to 17 years, met the inclusion criterion – a confirmed clinical diagnosis of migraine or a tension headache according to the International Classification of Headache Disorders, 2 nd edition. The diagnostic algorithm of the study group consisted of a full medical history, an assessment of the occurrence of bite habits and a physical examination based on the Research Diagnostic Criteria for Temporomandibular Disorders (RDC/TMD). Results. Bite and non-bite parafunctions were found in 36 of the study group patients. A significant difference (p = 0.0003) between the number of bite parafunctions and non-bite parafunctions was found in females but not in males. However, bite parafunctions were more frequent in boys compared to girls (p = 0.01). Conclusions. Our findings suggest that it may be useful for pediatricians and neurologists to include TMD dysfunctions as a part of a standard examination of adolescents presenting with persistent headaches.


Introduction
Headaches are one of the most common complaints in all age groups and a frequent cause of medical consultation and hospitalization. 1 They also have a significant impact on quality of life, with a detrimental effect on cognitive, emotional and social behavior. 24][5][6][7] Headaches can be broadly classified as primary or secondary. 8In the case of primary headaches, the problem lies in the pain itself -mainly migraine and tension-type pain.The diagnosis of primary headache is by means of the generally accepted clinical criteria developed by the International Headache Society, 2 nd edition (IHS-II). 9According to IHS-II, a headache can be attributed to temporomandibular disorders (TMD) when the coexistence of pain, mobility and acoustic symptoms of the temporomandibular joint are present.In the case of both headaches and TMD, pain can occur in the frontal, temporal, parietal and occipital regions. 9Population-based studies have previously examined the associations between TMD and psychological variables, pain conditions, and oral parafunctional habits. 10,11The international core tool used for TMD diagnosis is the Research Diagnostic Criteria for Temporomandibular Disorders (RDC/TMD) developed by Dworkin and LeResche and based on a biopsychosocial model. 12The RDC/TMD is derived from a consensus of leading researchers and clinicians and utilizes operationalized diagnostic criteria. 12The tool standardizes the evaluation and classification of patients, including young people with TMD, and assesses both physical disorder factors and psychosocial illness impact factors, axis I and axis II. 13Axis I is a set of diagnostic clinical procedures that provides data necessary for a physical diagnosis.][14][15] In adolescents, a variety of TMD symptoms, such as pain in the pre-auricular area, tenderness during mandibular movements, joint crepitus or restricted mandibular movements, may be detected, although less frequently than in adult populations. 16][19][20] It has been suggested that parafunctional activities may overload the dentition and masticatory system and may play an etiological role in the development of TMD. 21he detrimental effects of oral parafunctions will depend on their frequency, intensity and duration, as well as habits.Both masticatory and facial muscles respond to emotional states. 17,22The prevalence of TMD increases with age due to the escalating exposure of children and adolescents to stress at school, during exams and while adapting to adult life. 21,23Among the different oral parafunctional habits, teeth clenching and grinding, nail biting and gum chewing are most prevalent. 24,25ased on the results of Karibe et al., other pain conditions and parafunctional habits may exist that are related to TMD symptoms, even in a young population, and these factors should receive urgent attention. 26Oral bite and non-bite parafunctional habits involving repeated or sustained occlusal contact can be harmful to teeth and other components of the masticatory system and can affect the muscles and/or temporomandibular joint (TMJ).Hence, we investigated the prevalence of TMD symptoms in adolescents (12-17 years) with headaches, and assessed the occurrence of parafunctional habits and symptoms of TMD.In this study, we tested the hypothesis that TMD symptoms are associated with parafunctions in adolescents suffering from headaches.

Material and methods
Parents of all adolescents presenting with headaches in the Department of Developmental Neurology at Poznan University of Medical Sciences in Poland, from March 2013 to March 2014, were asked to complete a questionnaire survey developed by the authors of the study.Out of the 1000 patients evaluated in the Department, 40 children and adolescents aged 13-17 years met the inclusion criterion of the study -a confirmed clinical diagnosis of migraine or tension type headache according to the International Classification of Headache Disorders, 2 nd edition (ICHD-2). 9he mean age of the patients was 14.9 ±1.7 years.During hospitalization, all the subjects in this group were examined by a certificated child neurologist and a full medical history was provided.Data from the questionnaire survey was also used to confirm the ICHD-2 criteria for migraine and tension type headache.The questionnaire study was approved by the Ethics Committee of the Poznan University of Medical Sciences, Poland.

Questionnaire survey
The diagnoses of all subjects in the investigated group were confirmed both by questionnaire and clinical assessment.3][14][15] The questionnaire survey focused on the characteristics of the headache, its frequency and the presence of additional symptoms.It also included questions about the history of head and neck injuries, mouth breathing, incorrect ingestion, and parafunctional habits.Parafunctional habits were categorized according to the following classification: bite habits (that involve the contact of opposing teeth), such as teeth grinding or/and habitual teeth clenching; non-bite habits (which do not involve the contact of opposing teeth) such as tongue, lip/cheek biting, biting or chewing on objects and/or nail biting.

Examination of TMD -RDC/TMD questionnaire (axis II) and examination (axis I)
All functional examinations of the stomatognathic system were performed by the same dentist as well as the evaluation of the occurrence of clinical TMD signs or symptoms.The clinical examination required about 10-15 min, whereas completing the questionnaire required up to 30-45 min.
The axis II component of the RDC⁄ TMD is a measure of depression and non-specific physical symptoms, typical pain intensity (characteristic pain intensity) and painrelated disability classification which are reliable and valid indicators with respect to the selected reference standards and for application to this patient population.Questions regarding sexual behavior were excluded.If a patient has experienced facial pain, or pain in the stomatognathic system or temples for the last month, the second part of the form was completed -the Chronic Pain Grade Protocol. 12,13This included pain insensitivity, disability due to pain, depression, fainting accidents, dizziness, heartache, and stomach or throat discomfort.
The physical examination was performed according to axis I of the RDC/TMD.The classification included 3 major groups: 1. muscle disorders; 2. disc displacements; 3. arthralgia, osteoarthritis, and osteoarthrosis of the TMJ.In order to diagnose a muscle-related TMD, pain must be present in the jaw, temples, face, pre-auricular area or inner ear at rest or during activities; tenderness/palpation must be present in at least 3 out of 20 palpation sites, with at least 1 tender site situated ipsilaterally to the complaint pain.The following areas were palpated bilaterally (with tenderness ranges of no pain, mild pain, moderate pain, and severe pain): the posterior/middle/anterior temporal muscle, superior/middle/inferior masseter muscle, posterior mandibular region, submandibular region, lateral/posterior pole of the temporomandibular joint, lateral pterygoid area and tendon of temporal muscle.Using the observed signs and symptoms, the RDC/TMD specifies diagnostic algorithms along with a classification system dividing TMD diagnoses into 3 main groups and 8 subgroups (Table 1).This classification system only applies to the most common TMD diagnoses.The examination included: measurement of the range of mandibular movements, assessment of pain in joints and muscles in motion, and palpation of clicks or crepitus during mandibular movements.
The presence of bite and non-bite parafunctions, occurrence of etiological factors of TMD, prevalence of TMD according to RDC/TMD, prevalence of headache in each TMD-elicited from patient history, and clinical examinations are presented in the tables as counts (in absolute numbers) while frequencies are expressed in percentages.A test for differences between 2 proportions was used to detect the differences between the occurrence of parafunctions and gender.To check the dependency between gender and TMD type, the χ 2 test was used.The data obtained from the study was then analyzed using STATISTICA v. 10.0 (StatSoft Inc., Tulsa, USA).The level of significance was set at p ≤ 0.05.

Results
The study group consisted of 19 female (47.5%) and 21 male (52.5%) patients, aged 13 to 17 years.All participants had experienced episodes of headache for at least 3 months and this was the main reason for their admission to the department.A total of 12 participants (30.0%) from the study group manifested migraine headaches according to ICHD-2 diagnostic criteria, while 28 participants (70.0%) fulfilled the diagnostic criteria for tension type headaches.
In the examined group of 40 adolescents presenting with primary headaches, bite and non-bite parafunctions were found in 36 (90.0%) patients.The study found no correlation between gender and the presence of parafunctional habits in general.There was a significant difference (p = 0.0003) between the number of bite (31.6%) and non-bite parafunctions (89.5%) in female patients, which was not observed in male patients (p = 0.73).Boys (71.4%) presented more frequently with bite parafunctions compared to girls (31.6.0%;p = 0.01) (Table 2).In patients with a history of head trauma, malocclusion, abnormal swallowing or mouth breathing, the number of bite and non-bite parafunctional habits was high, ranging from 81.8% to 100% (Table 3).

RDC/TMD examination (axis I)
Using the axis I RDC/TMD diagnostic criteria, it was found that among 40 adolescents presenting with headaches, 16 patients (40.0%) suffered from muscle disorders (Ia), 13 patients (32.5%) had disc displacement with reduction (IIa) and 11 patients (27.5%) showed no dysfunctions.Bite and non-bite parafunctions were present in 100% of cases with muscle disorders (Ia), 100% of cases with disc displacement with reduction (IIa) and in 63.6% of patients with no symptoms of TMD (Table 4).Analysis of the 16 patients with muscle disorder (Ia) showed that the pain was mainly located in the frontal (50.0%) and temporal region (43.8%).Among the 13 patients manifesting disc displacement with reduction (IIa), 38.5% experienced pain in the temporal, parietal and occipital region and 30.8% in the frontal region.Among the 11 patients showing no symptoms from TMJ, 90.9% of cases experienced headache in the frontal region (Table 5).

Chronic Pain Grade classification and depression RDC/TMD questionnaire survey (axis II)
The prevalence of chronic pain located in the facial area (Chronic Pain Grade) according to RDC/TMD axis II is presented in Fig. 1.To facilitate the interpretation of data, the 4 grade scale of chronic pain used in RDC/TMD questionnaire was simplified to: 0 -absence of pain and 1 -presence of pain.In 16 subjects presenting with muscle disorder (Ia) chronic pain was diagnosed in 62.5%.Among 13 patients presenting with disc displacement with reduction (IIa) chronic pain was present in 69.2%.Among There was a significant difference (p = 0.0003) between the number of bite (31.6%) and non-bite parafunctions (89.5%) in girls, which was not observed in the case of boys (p = 0.72).The study revealed no statistically significant differences (ns) between girls and boys in the case of non-bite parafunctions (p = 0.3).However, bite parafunctions (p = 0.01) presented more frequently in boys.patients showing no symptoms from TMJ chronic pain was experienced by only 9.1% (Fig. 2).The depression and somatization symptoms grade scale, according to the RDC/TMD diagnostic criteria, was also simplified as: 0 -absence of pain and 1 -presence of pain.Depression was diagnosed in 1 patient in the Ia group and 1 patient in the IIa group.Non-specific physical symptoms were present in 3 cases in the Ia and 4 cases in the IIa group (Table 6).Subjects without TMD did not show any depression or non-specific physical symptoms.

Discussion
Recent studies of young (preschool to maturity) outpatients and inpatients have revealed that the number of headache cases has increased over recent years. 10,27,28n accurate analysis of headache characteristics is crucial for a proper differential diagnosis. 29,30Long term stress provokes emotional anxiety and increases muscle hyperactivity and tension. 9,10,31Chronic muscle tension can lead to headaches located in the temporal, frontal, parietal or occipital region.Liljeström et al. observed a correlation between TMD and headache in a group of adolescents with primary headache and concluded that TMD should always be considered when headaches are associated with ear pain, difficulty in opening the mouth and fatigue or stiffness of the jaw. 32Bertoli et al. evaluated the signs and symptoms of TMD in 50 children, aged 4-18 years, who had headaches. 18They found a higher prevalence of signs and symptoms of TMD in patients with headaches compared to the control group.
Adolescents with TMD have reported significantly higher levels of stress and psychosocial problems. 33Other researchers have demonstrated a correlation between headache and stress level, parafunctional habits, pops and clicks in the TMJ, and pain during mandibular movement. 21,26,34ubjects may be unaware of diurnal clenching and nocturnal tooth grinding while sleeping. 11,35Considering the high frequency of parafunctions and TMD in children and adolescents, epidemiological research into the morphological and functional causes would be of great benefit. 11,16,27,36,37n our study, in the group of adolescents presenting with primary headache, 36 (90.0%) of the subjects were found to have bite and non-bite parafunctions.Bite parafunctional habits were present in 52.5% of cases while 82.5% of subjects revealed non-bite habits.It was demonstrated that occlusal parafunctions appeared more frequently in male patients.There was also a significant difference between the number of bite parafunctions (31.6%) and nonbite parafunctions (89.5%) in girls, but not in boys.No significant difference was noted in non-bite parafunctional habits between female and male patients.
All patients with a diagnosed muscle disorder or disc displacement with reduction displayed bite and non-bite parafunctional habits.The results are consistent with that of Glaros et al. 38  Farsi et al. in their population studies of school children did not find any differences in the number of TMD symptoms between genders, but revealed a more frequent occurrence of non-bite parafunctions compared to bite parafunctions. 25Nail biting was the most common non-bite oral parafunction (27.7%) while bruxism proved to be the least common parafunction (8.4%).
Among the etiological factors, traumas, including head traumas, often occur in children and adolescents, and may be a source of headaches as well as TMJ disorders. 39Katzberg et al. showed that traumas are the cause of 26.0% of TMD in children and adolescents. 40TMJ injury can occur due to impact (car accidents, contact sports), biting on hard objects or opening the mouth too wide.In the group of 40 subjects, 27.5% of participants had a history of head trauma with 81.8% exhibiting bite and non-bite parafunctions.Other etiological factors of these dysfunctions included malocclusion, abnormal swallowing or mouth breathing.Such activities in combination with   41 Our results demonstrate the presence of malocclusion in 45% of cases, mouth breathing in 27.5% of cases, abnormal swallowing in 25% of cases, and parafunctions in 81.8-100% of cases.Over the past several decades, the age of patients presenting with TMD has been gradually decreasing. 41n individuals from 7 to 11 years old, the number of disorders increased rapidly from 30.0% to 60.0%; while the age group 12 to 14 showed no increase until the age of 19, when the disorders increased to 80.0%.Studies of adult subjects have revealed that TMD symptoms are twice as frequent in females than in males. 42,43However, there was no significant difference in TMD incidence between males and females in the age group studied.
Analysis of the location of pain was also performed in 16 patients with muscle disorders, where (Ia) pain affected the forehead (50.0%) and temples (43.8%).Of the 13 subjects presenting with disc displacement with reduction (IIa), the pain was located in the temporal, parietal and occipital region (38.5%), and frontal region (30.8%).Among the 11 patients without TMD, 90.9% of cases involved the frontal region.Ballegaard et al. examined adult patients presenting with headaches and discovered a high (83.0%)percentage of disabilities caused by chronic pain of the face and TMJ. 44In contrast, our findings demonstrate that chronic pain (Chronic Pain Grade) in children occurs to a lesser extent (52.5%).Among the subjects presenting with muscle disorders (Ia), 62.5% of patients suffered from pain.However, 69.2% of patients presenting with disc displacement with reduction (IIa) experienced pain.Some children with TMD symptoms did not develop any facial pain.
Currently, the significance of psychophysical factors as a cause of diseases and TMJ disorders is being emphasized.List et al. revealed that, in adolescents with TMD, psychosocial factors such as increased levels of stress, somatic complaints and emotional problems seem to play a prominent role. 33The chief factors include: stress, nervousness, depression, and anxiety.The depression scale SCL-90 elaborated by Derogatis et al. has been included in the RDC/TMD diagnostic criteria by Dworkin et al. 12,45 Mental state assessment by Ballegaarda et al. revealed that 54.5% of patients with headache were affected by moderate to severe depression. 44Our findings revealed that children and adolescents suffered from depression and nonspecific physical syndromes to a lesser degree: depression in 6.3-7.7% of cases and nonspecific physical syndromes in 18.8-30.8% of cases.Patients without any TMD symptoms showed no depression or nonspecific physical syndromes.

Conclusions
1. On the basis of patient history and clinical examination of adolescents presenting with primary headache, a high incidence of TMD symptoms, bite and non-bite parafunctional habits was found.
2. This paper underscores the need for a multilevel diagnostic and therapeutic approach, the importance of a rigorous examination of the stomatognathic system and the identification of a destructive influence of parafunctional habits in adolescents suffering from headache.
3. RDC/TMD classification is a helpful tool for diagnosing TMD in children and youth presenting with primary headache.

Fig. 2 .
Fig. 2. Prevalence of chronic pain (according to Chronic Pain Grade) RDC/TMD axis II in TMD diagnoses (axis I) (headache groups)

Table 1 .
Categories of clinical conditions present in TMD, according to RDC/TMD axis I

Table 2 .
Presence of bite and non-bite parafunctions in the group of adolescents presenting with headache

Table 3 .
Occurrence of parafunctions depending on TMD etiological factors in adolescents

Table 4 .
Prevalence of TMD in the group of adolescents suffering from headache according to RDC

Table 5 .
Prevalence of headache in each TMJ disorder according to RDC/TMD axis I diagnostic criteria

Table 6 .
Prevalence (%) of depression and non-specific physical symptoms with a pain component and non-specific physical symptoms without a pain component in RDC/TMD diagnoses, axis I (headache groups)