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CMD as an Indicator of Altered Physiological Stress Reactivity: A Highly Standardized Experimental ProtocolA
AnkeHollinderbäumer1✉Phone+49-6131-17-6747Emailhollinde@uni-mainz.de
MonikaBjelopavlovic2Emailmonika.bjelopavlivic@unimedizin-mainz.de
PeerW.Kämmerer1Emailpeer.kaemmerer@unimedizin-mainz.de
Univ.-Prof. Dr. med. Dent
ChristinaErbe3Emailerbe@uni-mainz.deProf. Dr.
JochenHardt4Emailhardt@uni-mainz.deUniv.-Prof. Dr.
KatjaPetrowski4Emailkpetrows@uni-mainz.deProf. Dr. med. Dr. med. dent.
Univ.-11
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Department of Oral and Maxillofacial Surgery - Facial Plastic SurgeryUniversity Medical Center of the Johannes Gutenberg-University MainzAugustusplatz 255131MainzGermany2Department of Prosthetic DentistryUniversity Medical Center of the Johannes Gutenberg- University MainzAugustusplatz 255131MainzGermany
3Department of Orthodontic DentistryUniversity Medical Center of the Johannes Gutenberg- University MainzAugustusplatz 255131MainzGermany
4Department of Medical Psychology and Medical SociologyUniversity Medical Center of the Johannes Gutenberg-University MainzDuesbergweg 655131MainzGermany
Anke Hollinderbäumer1*, Monika Bjelopavlovic2, Peer W. Kämmerer1, Christina Erbe3, Jochen Hardt4 and Katja Petrowski4
1Department of Oral and Maxillofacial Surgery - Facial Plastic Surgery, University Medical Center of the Johannes Gutenberg-University Mainz, Augustusplatz 2, 55131 Mainz, Germany
2Department of Prosthetic Dentistry, University Medical Center of the Johannes Gutenberg-University Mainz, Augustusplatz 2, 55131 Mainz, Germany
3Department of Orthodontic Dentistry, University Medical Center of the Johannes Gutenberg-University Mainz, Augustusplatz 2, 55131 Mainz, Germany
4Department of Medical Psychology and Medical Sociology, University Medical Center of the Johannes Gutenberg-University Mainz, Duesbergweg 6, 55131 Mainz, Germany;
* Correspondence: hollinde@uni-mainz.de; Tel.: +49-6131-17-6747; Fax: +49-6131-17-5569
Dr. rer. physiol. Anke Hollinderbäumer (A.H.) hollinde@uni-mainz.de
PD Dr. med. dent. Monika Bjelopavlovic (M.B.) monika.bjelopavlivic@unimedizin-mainz.de
Univ.-Prof. Dr. med. Dr. med. dent. Peer Kämmerer (P.K.) peer.kaemmerer@unimedizin-mainz.de
Univ.-Prof. Dr. med. Dent Christina Erbe (C.E.) erbe@uni-mainz.de
Prof. Dr. Jochen Hardt (J.H.) hardt@uni-mainz.de
Univ.-Prof. Dr. Katja Petrowski (K.P.) kpetrows@uni-mainz.de
Concent to Participate declaration:
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All participants signed the consent form of the study. Participation was voluntary. There were no disadvantages for students who did not take part. It was made clear to all participants that they could withdraw from the study at any time without giving reasons and that they would not suffer any disadvantages as a result. A
The consent form and the participant information was approved by the local ethic committee. The local Ethics Committee of the Landesärztekammer Rheinland-Pfalz, Germany (No #2019–14188), approved the study protocol. All participants received an allowance of fifty euros after successful attendance.A
Funding
Declaration:
Funding Declaration. Not applicable
Ethics declarations
Institutional review board statement
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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee (Ärztekammer Rheinland-Pfalz, reference number: #2019–14188 and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.Informed consent
statement
Informed consent
was obtained from all subjects involved in the study.
Competing interests
The authors declare no competing financial interests.
Clincal trail Number
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Clinical trial number: not applicable.Consent to Publish
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Consent to publish: not applicableA
Data Availability
Data can be requested from the corresponding author.
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Abstract
Background
Craniomandibular dysfunction (CMD) is a multifactorial disorder frequently associated with psychological stress. Its prevalence is particularly high in populations exposed to significant stress, such as students during exam periods. While subjective assessments have linked CMD to psychological stress, physiological evidence remains limited. Heart rate variability (HRV) is an established biomarker for autonomic regulation and stress reactivity, making it a valuable tool for assessing stress responses in CMD.
Objective
This study examines stress reactivity in students with and without CMD symptoms using HRV as a physiological marker and a standardized stress protocol.
Methods
A total of 138 healthy students (aged 23–36 years) were recruited.
A
CMD symptoms were assessed using a standardized protocol based on the bruxism guideline, focusing on palpation-induced pain and range of motion limitations. Psychological stress was measured using the Perceived Stress Scale (PSS) and Beck Depression Inventory-II (BDI-II).Acute stress was induced using the Trier Social Stress Test (TSST), and HRV was recorded at baseline (pre-stress) and during stress exposure. RR intervals were analyzed using KUBIOS software, with root mean square of successive differences (RMSSD) as a key parameter.
Statistical analyses employed linear mixed models, adjusting for confounders such as age, sex, and baseline stress levels.
Results
CMD symptoms, especially pain caused by palpation, correlated significantly (p < 0.0048) with psychological stress markers. These students also had higher levels of depression (p < 0.0015). Due to participant dropout, the statistical significance of the analysis of heart rate variability was limited. The effect differences indicated a trend towards prolonged autonomic dysregulation in students with CMD pain.
Conclusion
The findings provide physiological evidence linking CMD to stress, and show altered autonomic responses in students with CMD symptoms. Early symptom recognition, stress management programs and strategies should be integrated into CMD treatment. Future research should include cortisol as an additional biomarker and employ larger, longitudinal studies to improve clinical applicability.
Key words:
Craniomandibular dysfunction
CMD
stress
Heart rate variability
HRV
psychological stressinduction
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1. Introduction
A growing number of studies have shown that stress and psychological distress are considered to be the most important factors or catalysts for the onset and development of craniomandibular dysfunction (1). A large amount of patients with craniomandibular dysfunction and associated symptoms (65.2%) have reported suffering from chronic stress (2). In line, significantly higher levels of stress in patients with craniomandibular dysfunction and bruxism than in patients without (3). The prevalence increases whereby the patients age decreases. The prevalence of CMD among students varies a lot between 44.3% (4) and 90.1% compared to faculty at 75.7% (5). Students reported more symptoms and had significantly more parafunctional activities than faculty members. (6).
Craniomandibular dysfunctions (CMD) are disorders of the temporomandibular joint and surrounding musculature that can lead to pain and dysfunction in the head, neck, and shoulder region (7). Since the diagnosis depends on various factors and the term "craniomandibular dysfunctions" serves merely as a collective term for an extremely large and, above all, variable symptom complex, there is no uniform definition. One possible definition for CMD has been proposed by the German Society for Functional Diagnostics and Therapy (DGFDT) and states, "CMD includes pain and/or dysfunction of the masticatory muscles and/or temporomandibular joints and/or dysfunction of occlusion."(1). Symptoms of Craniomandibular Dysfunction can vary widely, ranging from mild discomfort to severe pain and dysfunction of the jaw and surrounding muscles. Also, symptoms such as: Teeth grinding or clenching, headaches, migraines or tinnitus are also mentioned. Just as variable as the symptoms are their causes. Since craniomandibular dysfunctions must be considered a multifactorial event. In addition to the psychosocial component, other possible causes such as injuries or trauma to the temporomandibular joint, incorrect or excessive loading, infections or inflammations, as well as osteoarthritis or arthritis should be considered (2). While occlusal disorders and dental morphology were previously held primarily responsible for the dysfunctions, a large number of studies now point to the relationship with psychosocial factors, especially stress (1).
Stress leads to excessive activation of the masticatory muscles (4), which results in increased strain on the temporomandibular joint and the surrounding muscles. This results in pain, muscular tension and restricted movement in the area of the jaw apparatus. There is also evidence that stress can be seen as a contributing factor to the development of bruxism (8). Graner et al. investigated 2018 the relationship between mental illness, stress and the prevalence of craniomandibular dysfunction (CMD) in Brazilian dental students. The results of the study showed that the prevalence of CMD among dental students was significantly higher (20–48%) than in the general population (20–25%). It was also found that psychological factors had a significant influence on the occurrence of CMD. For example, the risk of developing CMD was up to four times higher in students who had received psychiatric treatment before or during their studies and in those who rated their academic performance and social life more negatively. Furthermore, study participants who reported higher resilience had a lower prevalence of CMD, indicating a possible protective factor of resilience(9).
Even if these studies establish a clear connection between craniomandibular dysfunctions and stress (1, 2, 3, 5, 10), there is currently a lack of objective evidence that also highlights the connection physiologically by means of heart rate variability (HRV) measurement during a standardized stress test.
The heart rate variability gives us a very reliable indication of a patient's physiological stress level. HRV stands for heart rate variability and is a measure of the heart's ability to adapt to changing demands and can serve as an indicator of the body's ability to adapt and adjust (11). It is the variations in the intervals between heartbeats regulated by the autonomic nervous system. A high HRV is considered an indicator of healthy autonomic regulation of the body. A lower HRV, on the other hand, may indicate a disturbed balance between the sympathetic and parasympathetic nervous systems, and is associated with health problems such as stress, mental illness, or cardiovascular disease. HRV is measured by examining the precise temporal resolution of RR intervals in the electrocardiogram (ECG)(11, 12).
Empirical studies on the relationship between CMD and HRV compared with a control group uniformly showed that patients with CMD had significantly lower HRV than the control group (13, 14, 15). This suggests that craniomandibular dysfunction is most likely associated with impaired autonomic regulation of the body. Most likely, there is a relationship between CMD and HRV and that successful treatment of CMD can also lead to an improvement in the autonomic regulation of the body and vice versa.
It is unclear here to what extent HRV stress reactivity is impaired in these patients. This requires measurement of HRV under standardized conditions using stress induction as well as a detailed diagnosis of the symptom picture. Therefore, the aim of our study is to find out to what extent stress reactivity is impaired in patients with crandiomandibular dysfunctions by means of a standardized stress test.
2. Materials and methods
2.1 Study Participants
The study, designed as a pilot study, comprises 138 healthy students who were recruited via electronic tenders (e-tendering) using the snowball method (16). After the clinical measurements and the psychological measurements 56 students rested. 60 percent were female. Age showed a range of 23–36 years. People with acute or chronic illnesses, psychiatric diagnoses, regular medication or substance use, and relevant stressful events in the last six months were excluded. Heavy smoking (> 10 cigarettes/day) and ages outside the range of 22–37 years also led to exclusion. These criteria were verified in a telephone screening using the Structured Clinical Interview (SCID; (17))) for the Diagnostic and Statistical Manual of Mental Disorders (DSM-IV,(18)).
Ethics
All participants received an information sheet to inform them about the study and its content. They signed the consent form of the study. Participation was voluntary. There were no disadvantages for students who did not take part. It was made clear to all participants that they could withdraw from the study at any time without giving reasons and that they would not suffer any disadvantages as a result. The consent form and the participant information was approved by the local ethic committee. The local Ethics Committee of the Landesärztekammer Rheinland-Pfalz, Germany (No #2019–14188), approved the study protocol.
2.2 Materials
Clinical Measures – CMD Diagnosis
The clinical functional status was assessed using a questionnaire to determine the prevalence and effects of craniomandibular dysfunction (CMD) The CMD criteria were standardized according to DGFDT (1). The test subjects were asked about:
Pain or impairment in various head/neck regions
Discomfort or pain on palpation of various muscle groups
Strain noises of the temporomandibular joint
Impairments or pain with different temporomandibular joint movements
Psychological Measures
The psychological and general status of the participants was measured with seven instruments:
(1) The Structured Clinical Interview for DSM Disorders (SCID; (17)) is a semi-structured clinical interview based on the diagnostic criteria of the DSM (Diagnostic and Statistical Manual of Mental Disorders; (18)). It is used to reliably and validly assess mental disorders.
(2) The Symptom-Check-List-90-R (SCL;(19)) is a self-report instrument for the evaluation of psychological and physical impairment, consisting of 90 items with a five point rating scale (total score range: 20–80).
(3) The German version of the Perceived Stress Scale (PSS; (20)) contains 14 items using a five-point Likert scale that ranges from 1 (never) to 5 (very often).
(4) The Beck Depression Inventory (BDI-II;(21)), records depressive symptoms including 21 symptoms and attitudes that can be rated in terms of intensity from 0 to 3 (total score range: 0–63).
(5) The STAI (22) measures both anxiety in the current situation “state anxiety” and anxiety as a trait “trait anxiety”. Both forms of anxiety are assessed with 20 questions each on a four-point Likert scale ranging from 1 (not at all) to 4 (very much).
(6)The Primary Appraisal Secondary Appraisal (PASA; (23)) measures the cognitive appraisal processes. In the initial assessment, or primary appraisal, specific situations are evaluated as threatening or challenging. The second appraisal describes an individual’s perceived coping skills. A stress index is calculated as an integrated measure of transactional stress. A high stress index score indicates a higher general stress perception. The scale comprises 16 items to be rated on a six-point Likert scale ranging from 1 (completely disagree) to 6 (completely agree).
(7) The visual analogue scale (VAS) was used to assess the self-reported stress perception after both conditions and rates from 0 (no stress) to 100 (maximum stress).
Heart Rate Measurement
The Polar V800 system with H10 chest strap (Polar, Finland) was used for continuous heart rate monitoring. The R-R intervals were analysed using Kubios software, which automatically filtered out artifacts and extra beats. The evaluation was carried out at five-minute intervals during the test and recovery phases.
Trier Social Stress Test
The Trier Social Stress Test (TSST; (24) according to Kirschbaum et al. (1993) is a standardized laboratory paradigm. It was developed to induce moderate psychological stress through a combination of social evaluation threat an uncontrollability. Athe standardized procedure reliably induces physiological and psychological stress reactions.
2.3. Procedures
Both test conditions (stress vs. rest) were conducted on two separate dates within one week. The sessions took place in the afternoon (between 2:00 p.m. and 5:00 p.m.), with the order of the conditions determined at random. The participants were asked to refrain from eating, drinking and smoking for at least two hours before testing and during the two-hour testing session. Before the actual test conditions began, each subject completed a 15-minute preparation phase. This included a three-minute test to determine respiratory sinus arrhythmia, in which the respiratory rate was standardised to six breaths per minute. Afterwards, the healthy participants went through the two 15-minute conditions (stress and resting): The Trier Social Stress Test (TSST) according to Kirschbaum et al. (24) was used to induce acute stress. This comprises three consecutive sections (preparation, free speaking/ interview and a mental arithmetic task), each lasting five minutes. In the control condition, the participants spent the time relaxing, for example by reading magazines. The cognitive appraisal was evaluated three minutes after the start of either condition by the Primary Appraisal Secondary Appraisal (PASA;(23)). Immediately after both conditions, the self-reported stress perception of both conditions was measured with the visual analogue scale (VAS). The participants were fitted with a chest trap to measure the heart rate during the whole experimental protocol with the Polar monitoring system V800 with the H10 sensor (Polar, Finland). An overview of the examination procedure is given in Fig. 1.
Fig. 1
Overview of the examination procedure
Figure 1 Overview of the examination procedure. PASA Primary Appraisal Secondary Appraisal, TSST Trier Social Stress Test, VAS Visual Analogue Scale.
3. Results
3.1 Evaluation of the CMD "Clinical Functional Status"
34 out of 66 students stated that they had pain and 32 students said they had no pain.
Number | Percent | |
|---|---|---|
Headaches | 16 | 30,8% |
Temple pain | 12 | 22,6% |
Ear/ jaw joint pain | 12 | 22,6% |
Table 1 shows that 12 to 16 out of 34 students reported pain in the head and face area.
3.2 CMD criteria and the psychological symptoms
Table 2 shows correlations between CMD criteria and various psychological symptoms.
Occlusion | Palpation | Iso/ Mobi | Horiz. KR | Verti. KR | |
|---|---|---|---|---|---|
Pain | -0.0070 p < 0.9616 N = 50 | 0.4155 p < 0.0022 N = 52 | 0.3973 p < 0.0035 N = 52 | 0.1177 p < 0.4469 v44 | -0.0609 p < 0.6714 N = 51 |
PSS - Overall score | -0.1680 p < 0.2436 N = 50 | 0.3849 p < 0.0048 N = 52 | 0.1667 p < 0.2376 N = 52 | -0.4179 p < 0.0048 N = 44 | -0.0464 p < 0.7466 N = 51 |
PSS - Helplessness | 0.0466 p < 0.7480 N = 50 | 0.3636 p < 0.0081 N = 52 | 0.2195 p < 0.1179 N = 52 | 0.0404 p < 0.7944 N = 44 | -0.0598 p < 0.6767 N = 51 |
PSS – Self-efficacy | -0.0316 0.8278 N = 50 | 0.0772 0.5864 N = 52 | 0.2380 0.0893 N = 52 | -0.3312 0.0281 N = 44 | -0.0979 0.4945 N = 51 |
BDI-II | -0.0294 p < 0.8409 N = 49 | 0.4330 p < 0.0015 N = 51 | 0.2753 p < 0.0506 N = 51 | 0.0002 p < 0.9989 N = 43 | -0.1026 p < 0.4629 N = 50 |
SCL_90 - Global Severity Index | -0.0633 p < 0.6727 N = 47 | 0.6034 p < 0.0000 N = 49 | 0.4062 p < 0.0038 N = 49 | -0.1415 p < 0.3777 N = 41 | 0.0607 p < 0.6820 N = 48 |
| Iso/Mobi = Isometry/Mobility, Horiz.KR = Horizontal Jaw Relation, Verti.KR = Vertical Jaw Relation | |||||
Palpation of the temporomandibular joint correlates significantly with the psychological stress parameters, with the exception of negative self-efficacy. However, isometry/mobility and horizontal jaw relation also show significant correlations. Only for the vertical jaw relation were no correlations with psychological stress parameters.
3.3 psycological stressinduction
Following the “TSST”, the test subjects completed VAS questionnaire after the procedure and before the resting condition, in which 68% stated that the statement “I found the situation challenging” was somewhat to completely true. The statement “The situation was stressful for me” was also rated by many participants (75%) as somewhat to fully accurate.
Occlusion | Palpation | Iso/ Mobi | Horiz. KR | Verti. KR | |
|---|---|---|---|---|---|
STAI | 0.4340 p < 0.0046 N = 41 | -0.02807 p < 0.0683 N = 43 | -0.0817 p < 0.6025 N = 43 | -0.1945 p < 0.2557 N = 36 | -0.0520 p < 0.7435 N = 42 |
PASA - primary appraisal | 0.2017 p < 0.2182 N = 39 | 0.3603 p < 0.0242 N = 39 | 0.1963 p < 0.2309 N = 39 | 0.0337 p < 0.8474 N = 35 | -0.2432 p < 0.1357 N = 39 |
PASA – secondary appraisal | -0.0710 p < 0.6635 N = 40 | -0.0936 p < 0.5605 N = 41 | -0.0745 p < 0.6433 N = 410 | 0.0087 p < 0.9610 N = 34 | 0.0217 p < 0.8929 N = 41 |
PASA – stress Index | -0.0575 p < 0.7585 N = 31 | 0.3097 p < 0.0900 N = 31 | 0.1981 p < 0.2853 N = 31 | 0.0597 p < 0.7672 N = 27 | -0.2414 p < 0.1908 N = 31 |
The perceived stress at the beginning of the “TSST” shows a significant correlation with increased values in the “palpation” of the temporomandibular joint.
3.4 Group comparison of students with CMD and without CMD on perceived stress symptoms
Table 4 compares students who reported CMD pain with students who did not report CMD pain.
Group | Number | Mean | Std. dev. | df | t | p | |
|---|---|---|---|---|---|---|---|
VAS | No pain | N = 36 | 49.0799 | 9.02067 | 50 | -4.093 | 0.263 |
pain | N = 16 | 61.2109 | 11.59757 | ||||
PASA first arousal | No pain | N = 22 | 3.4716 | 0.60372 | 46 | -0.2489 | 0.8046 |
pain | N = 26 | 3.5240 | 0.81702 | ||||
PASA second arousal | No pain | N = 28 | 3.1339 | 0.5733 | 46 | -0.8950 | 0.3755 |
pain | N = 20 | 3.3 | 0.7111 | ||||
STAI | No pain | N = 26 | 45.8461 | 4.0958 | 50 | 0.6855 | 0.4962 |
pain | N = 26 | 44.9615 | 5.1461 | ||||
BDI | No pain | N = 32 | 5.9688 | 5.1085 | 59 | -2.2174 | 0.0305 |
pain | N = 29 | 9.4483 | 7.0740 | ||||
SCL total | No pain | N = 30 | 1.3825 | 0.2917 | 57 | -1.3106 | 0.1953 |
pain | N = 29 | 1.5088 | 0.4365 | ||||
PSS total | No pain | N = 32 | 25.4688 | 5.3521 | 61 | -1.139 | 0.1268 |
pain | N = 31 | 27.0323 | 5.5467 |
Tabel 4 shows a significantly higher value for depression among students within CMD. The other comparisons show no significantdifferences.
3.5 Heart Rate Variability under stressinduction
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Figure 2 Chance in stress levels in healthy students and CMD patients (CMD present), at 95% confidence interval, plotted in relation to RMSSDAt the beginning of the TSST, at time T0, both groups show a significantly increased RMSSD value. During the TSST, a decrease in the RMSSD value is observed, with the values for the CMD patients up to T2 being just below the values of the healthy individuals. From T2 onwards, the RMSSD values of the healthy subjects are below those of the CMD patients. From T2 to T3, both groups form a plateau
4. Discussion
The results of the study show that a high proportion of students (31 − 23%) reported pain in the head and face area after being interviewed using the CMD questionnaire (see Table 1) and can therefore be described as CMD patients (7). At the same time, the psychological symptoms of stress experience show significant correlations with individual CMD criteria (see Table 2). Psychological symptoms are most frequently associated with the palpation criteria. The fact that these are perceived first during palpation indicates a milder course of CMD.
With regard to stress induction by means of the standardized TSST procedure, we can see in Table 3 that the students describe the test situation as stressful overall and show significant correlations with CMD criteria at the beginning of the TSST. The fact that an increased heart rate variability, as a physiological parameter for stress experience or for ineffective stress management, does not show any significant differences can be attributed to the lack of power due to the small sample to be evaluated. In Fig. 2, a different course of the RMSSD can be described for both groups (pain vs. one pain), but this was not statistically significant.
Strengths: The study includes a random healthy cohort of students with a socially matched gender distribution and a narrow age range. The CMD criteria were standardized according to DGFDT (1). Criteria and collected from one person. The TSST as a standardized stress test was able to induce stress and was used for the first time to examine CMD patients.
Limitations: The study started with N = 138 students. 66 − 48 people were fully evaluated, which led to insufficient power, e.g., in the evaluation of heart rate variability. A more detailed analysis of the causes of dropouts would be helpful here. Also, no further heart rate measurements were carried out in the TSST during the recovery phase, as is part of the standardized protocol.
5. Conclusion
For further scientific procedure, it would be desirable to conduct the study again with the following modified parameters:
In addition to heart rate variability, also record and analyze cortisol values (25–27) as a further physiological parameter for stress experience in the participants.
Rethink and reduce the psychometric procedures.
Limit CMD diagnostics to the essential criteria and anamnesis data.
This increases the likelihood that participants will complete the documents in full and increases the number of people to be assessed. With a larger number of study participants, CMD subgroups could be formed, e.g. myofascial pain vs. temporomandibular joint disorders. This would make it possible to check whether these subgroups are affected differently.
For students for whom the stress experience will increase during the exam phase and for whom the current, still mild CMD progression may manifest itself, there should be offers for:
Stress recognition and
Stress management.
The correlation between stress and myogenous CMD is described in the literature (28–30). It would be desirable to investigate this under standardized conditions, as made possible by the TSST. A longitudinal study design could also better capture future developments of CMD in connection with stress reactivity.
The aim should be to recognize mild cases and prevent more chronic cases and their treatment with stress-reducing measures. In addition, the results underline the need for early diagnosis for effective management of CMD, as this is the only way to improve the quality of life of those affected.
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Author Contribution
AH analyzed and interpreted the data and wrote the main text of the manuscript. MB helped analyze the data and revised the manuscript.CE helped revise the manuscript.PK helped revise the manuscript.JH calculated the statistics.KP initiated the study and revised the manuscript.All authors reviewed the manuscript.
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