Sarmad.doc J Bagh College Dentistry Vol. 27(2), June 2015 Assessment of cortisol Oral Diagnosis 86 Assessment of cortisol as salivary psychological stress marker in relation to temporomandibular disorders among a sample of dental students Sarmad Qays Ali, B.D.S. (1) Raja Hadi, B.D.S., M.Sc., Ph.D. (2) ABSTARCT Background: University dental students perceived a higher level of stress prior to the final exam associated with raised salivary cortisol levels which could be considered as a useful noninvasive biomarker for measuring acute stress. Using a Helkimo anamnestic and clinical dysfunction scoring for temporomandibular disorders can give a better insight about the association of this marker and temporomandibular joint disorders. The aim of this study was to evaluation level of salivary cortisol in stressor students with temporomandibular disorder and the relation between this marker in relation to temporomandibular disorder severity. This might give a better understanding to the role of psychological stress as an etiological factor for developing temporomandibular joint problems. Materials and methods: A total eighty participants age between 20 to 24 were recruited for this study. The participants were University dental students under graduate students at final examination period who were examined and gave saliva samples in final examination period. Salivary assay kits as cortisol was used to measure those variables and a Helkimo anamnestic and clinical dysfunction scoring for TMD. Results: The group of participants with stress and temporomandibular disorder showed significantly higher levels of salivary cortisol than the control group, the salivary cortisol has statistically significant correlation with Helkimo anamnestic categories (Di-I mild, Di-II moderate and Di-III severe. Salivary cortisol levels show significant but weak association with two categories of clinical dysfunction criteria in Helkimo index system, which are Muscle pain and TMJ pain on palpation. Conclusion: This study demonstrated that University students perceived a high level of stress before the final examination. Salivary cortisol is the stress biomarker that is most often used to measure acute stress. Helkimo anamnestic and clinical dysfunction scoring criteria for still the pioneer for measuring a temporomandibular disorder. Keywords: stress, cortisol, Helkimo, temporomandibular joint TMJ, temporomandibular disorder TMD. (J Bagh Coll Dentistry 2015; 27(2):86-92). INTRODUCTION University students are liable to a higher level of stress especially in pre-examination period, if stress is prolonged, the stress response has two principal facets: the neuro-endocrine, which involves corticotropin-release hormone, activation of the hypothalamic-pituitary-adrenal axis and the secretion of cortisol into circulation. Cortisol is then filtered through the acinar cell membrane of the salivary glands, and is found in saliva in the free unbound form. Secondly, the stress response involves activation of the autonomic nervous system, release of catecholamines (e.g., plasma norepinephrine, pNE), and sympatho-mimetic manifestations, such as increase salivation, and increase secretion of Sα-amylase (1). Salivary cortisol levels increase under a variety of physical (i.e., exercise, heat and cold) and psychological (i.e., written examinations) challenges. Salivary and plasma cortisol levels always correlate with each other following stress, confirming that the two pathways are the same salivary cortisol increases with psychological stress and correlates serum cortisol (2). (1) Master Student. , Department of Oral Diagnosis, College of Dentistry, Baghdad University (2) Professor, Department of Oral Diagnosis, College of Dentistry, Baghdad University Temporomandibular joint dysfunction is an collective term covering pain and dysfunction of the muscles of mastication and the temporomandibular joints. The most important feature is pain, .followed by restricted mandibular movement and noises from the temporomandibular joints (TMJ) during jaw movement (3). Although temporomandibular disorder TMD is not life threatening, it can be detrimental to quality of life (4) because the symptoms can become chronic and difficult to manage. Usually people affected by TMD are between 20 and 40 years of age, and it is more common in females than males (5). The etiology of TMDs is multifactorial which is thought to be caused by multiple, poorly understood factors (6). But the exact etiology is unknown (7). There are factors which appear to predispose to TMD (genetic, hormonal, anatomical), factors which may precipitate it (trauma, occlusal changes, parafunction), and also factors which may prolong it (stress and again parafunction) (8). Overall, 2 hypotheses have dominated research into the causes of TMD, namely a psychosocial model and a theory of occlusal disharmony (7). Oral habits or parafunctions, defined as any oral nonfunctional activity or behaviour involving J Bagh College Dentistry Vol. 27(2), June 2015 Assessment of cortisol Oral Diagnosis 87 the masticatory system, are neither uncommon nor are they always harmful (9). It is only when such activities exceed an individual’s physiologic tolerance that breakdown of the masticatory system may occur. In such cases the initial breakdown takes place in the tissue with the lowest structural tolerance in that particular individual, e.g. joints, teeth or muscles (10). Oral habits or parafunctions have been reported to be common worldwide, with many students and adolescents performing them on a daily basis (11). Oral habits include a variety of activities, such as continuous gum chewing, nail biting, and chewing on writing implements (pencils, pens). Oral habits such as these are common among students, and they were shown to have a potentially detrimental effect on the masticatory system (12,13). Saliva has been described as the mirror of the body. The wide spectrum of compounds present in saliva may provide information for clinical diagnostic applications. Saliva is a good medium because its collection is noninvasive and the donation process is relatively stress free, so that multiple collections can be performed without imposing too much discomfort on the donor (14). Cortisol, known more formally as hydrocortisone is a steroid hormone, more specifically a glucocorticoid, produced by the zona fasciculata of the adrenal cortex (15). It is released in response to stress and a low level of blood glucocorticoids. Its primary functions are to increase blood sugar through gluconeogenesis; suppress the immune system; and aid in fat, protein and carbohydrate metabolism. It also decreases bone formation (16). In the blood only 1 to 15% of cortisol is in its unbound or biologically active form. The remaining cortisol is bound to serum proteins (17). Unbound serum cortisol enters the saliva via intracellular mechanisms, and in saliva the majority of cortisol remains unbound to protein, because of partial conversion of cortisol to cortisone during passage through the salivary glands, the absolute level of free cortisol in saliva is 10% to 35% lower than it is in blood (18). Salivary cortisol levels are unaffected by salivary flow rate or salivary enzymes (19). SUBJECTS, MATERIALS AND METHODS The subjects: A total eighty participants age between 20 to 24 were recruited for this study. The participants were University dental students under graduate students at final examination period who were examined and gave saliva samples in final examination period. The participants in this study divided into two groups: -Case group: sixty stressed students with temporomandibular disorders (TMD). -Control group: twenty students without stress and temporomandibular disorders (TMD). *Inclusion criteria 1. University dental students (20-24) years old from both genders with stress and temporomandibular disorders were included in the case group. The female students were in the luteal phase of menstrual cycle to be equal to male in the activity of hypothalamus- pituitary-adrenal axis. 2. University dental students (18-30) years old from both genders without stress and temporomandibular disorders were included in the control group. * Exclusion criteria Students with a history of use of corticosteroids in the past year, a history of antidepressant medication or head injury, on hormone supplements including oral contraceptives at the time of saliva collection., orthodontic treatment, occlusal disharmonies like cross bite and premature contact or dental pain. Those with muscle tenderness due to systemic diseases as fibromyalgia, neuralgia and local infection and Cases with more than 2 missing posterior teeth. Materials: High sensitivity, salivary cortisol enzyme immunoassay kits (Uscn Life Science Inc. Wuhan, China). Methods of examination: The participants examined according to Helkimo anamnestic and clinical dysfunction index of temporomandibular disorders which consists of standardized series of diagnostic tests based on clinical signs and symptoms. Statistical Analysis Statistical analysis was computer aided. An expert statistical advice was sought for. Statistical analyses were done using IBMSPSS version 21 computer software (Statistical Package for Social Sciences). Data were presented in measures of mean, standard deviations, range (minimum- maximum values), median, frequency and percentages. The significance in difference between the means (quantitative data) for two groups was tested using independent student t- test, while using Analysis of Variance (ANOVA) for more than two groups the receiver operating J Bagh College Dentistry Vol. 27(2), June 2015 Assessment of cortisol Oral Diagnosis 88 characteristics (ROC) and predictive value (PV) was used in this study. The correlation coefficient value (r) either positive (direct correlation) or negative (inverse correlation) with value <0.3 represent no correlation, 0.3-<0.5 represent weak correlation, 0.5-<0.7 moderate strength, >0.7 strong correlation. Probability test (P value) was considered statistically significant when the P value < 0.05 and regarded as highly statistically significant when the P value < 0.001. RESULTS The data related to salivary cortisol levels showed normal distribution in both case and control groups. The group of participants with stress and TMD showed significantly higher levels of salivary cortisol (mean 177.8 ± SE 12.24 ng/ml) than the control group (mean 22.9 ± SE 2.28 ng/ml). See Table 1 and Figure 2. Table 1: The salivary cortisol levels in the case and control groups. P Study groups Salivary cortisol Cases with stress Controls <0.001 (9.6 to 413) (9.8 to 46) Range 177.8 22.9 Mean 94.8 9.9 SD 12.24 2.28 SE 60 20 N Figure 2: Dot diagram with error bar chart demonstrates the comparison of salivary cortisol levels in both control and stress with TMD groups. Bars represent the median while range lines represent the 95% Confidence Interval CI (measurements in ng/ml and P value< 0.001). The predictive value measurements for salivary cortisol showed highly positive predictive value (PPV) at 50% and 90% levels with the cut- off point of 70.1 ng/ml. Above this point, the salivary cortisol can be used as biomarker for accurate prediction of stress and TMD (accuracy 93.7%). Correlation analysis of salivary cortisol with Helkimo anamnestic clinical dysfunction score shows positive association expressed by significant p value of 0.026. This means that the salivary cortisol has statistically significant correlation with Helkimo anamnestic categories (Di-I mild, Di-II moderate and Di-III severe). See Table 2 and Figure 3. Table 2: Association of Salivary cortisol levels with Helkimo anamnestic categories of TMD P Study groups Salivary cortisol (10–25) Di-III (Severe dysfunction) (5–9) Di-II (Moderate dysfunction) (1–4) Di-I (Mild dysfunction) <0.001 (185 to 364) (105 to 413) (9.6 to 410) Range 264.7 221.9 158.8 Mean 91.1 117.6 81.3 SD 52.6 32.63 12.26 SE 3 13 44 N Fig 3: Dot diagram with error bar chart demonstrating the association of salivary cortisol levels with Helkimo anamnestic categories of TMD. Bars represent mean of the salivary cortisol in each category, range lines represent standard errors and p value <0.05. In depth analysis with each single criteria used by Helkimo, revealed more interesting results. Salivary cortisol levels show significant but weak association with two categories of clinical dysfunction criteria in Helkimo index system, which are Muscle pain and TMJ pain on palpation. The muscle of mastication with highest tenderness to palpation was master muscle followed by temporalis and lateral pterygoid with less tenderness. See table 3. The distribution percentage of varying oral habits in TMD students that shown as follow (See Table 4). J Bagh College Dentistry Vol. 27(2), June 2015 Assessment of cortisol Oral Diagnosis 89 Table 3: Association of salivary cortisol levels with individual clinical criteria used in Helkimo index for TMJ dysfunction Salivary cortisol Range Mean SD SE N P Gender Female (9.6 to 410) 191.1 94.2 17.19 30 0.28[NS] Male (11.2 to 413) 164.5 95.2 17.39 30 Mandibular mobility (opening, laterotrusive, protrusive) 0.027 Normal range of movement (9.6 to 394) 158.7 82.8 13.09 40 Slightly impaired mobility (105 to 413) 215.9 107.5 24.05 20 Severely impaired mobility ** ** ** ** 0 r=0.202 P=0.12[NS] Symptom: impaired TMJ function 0.01 Smooth movement without TMJ sounds and deviation on opening or closing movement <2 mm (104.4 to 410) 219.2 85.9 21.47 16 Sounds in 1 or both joints and/or deviation >2 mm on opening or closing movements (9.6 to 413) 156 90.2 13.92 42 Locking/and/or luxation of the TMJ (245 to 364) 304.5 84.1 59.5 2 r=-0.191 P=0.14[NS] Symptoms: Masseter pain 0.007 No tenderness to palpation in masticatory muscles (9.6 to 212.2) 114.7 75.8 26.78 8 Tenderness to palpation in 1-3 palpation sites (11.2 to 413) 177.6 89.8 13.11 47 Tenderness to palpation in > 4 palpation sites (185 to 394) 280.6 92.9 41.55 5 r=0.373 P=0.003 Symptoms: TMJ pain 0.045 No tenderness to palpation (9.6 to 410) 154.5 96.3 17.89 29 Tenderness to palpation laterally (16.4 to 413) 199.5 89.5 16.08 31 Tenderness to palpation posteriorly ** ** ** ** 0 r=0.286 P=0.027 Symptom: pain on movement of the mandible 0.09[NS] No Pain on movement (9.6 to 240) 162.9 68.1 14.53 22 Pain on 1 movement (11.5 to 413) 174.5 103.4 18 33 Pain on > 2 movements (139 to 390) 264.6 109.7 49.04 5 r=0.101 P=0.44[NS] Table 4: The distribution percentage of varying oral habits in TMD students. % N Oral habits 20.0 12 Non 28.3 17 Clenching 8.3 5 Grinding 6.7 4 Biting nail 21.7 13 Bruxism 15.0 9 Chewing 100.0 60 Total DISCUSSION For decades, research on the acute and chronic effects of stress has employed cortisol levels as an index of the individual response to stress (20). Salivary cortisol levels provide an accurate, reliable, and non-invasive measure of stress in both adults and children (21). Which match the J Bagh College Dentistry Vol. 27(2), June 2015 Assessment of cortisol Oral Diagnosis 90 result of this study that showed salivary cortisol is useful biomarker for assess psychological stress. Cortisol is a hormone secreted by the hypothalamus pituitary adrenal axis (HPAA) and has been used as an accurate biomarker in stress research for over half a century (22). In dentistry salivary cortisol has been used to measure the role of stress in a variety of settings from the anxiety of dental treatment to periodontal disease, dental caries and temporomandibular disorders (23-26). As already known, cortisol secretion increases significantly in the state of acute stress as in psychological stressor of written examinations (20, 27, 28). These results have an agreement with this study that have found a highly significant levels of salivary cortisol which in turn strongly support these previous studies that have showed and suggested the use of cortisol as non-invasive indicator for assessment stress with TMD. In 2004, Dickerson and Kemeny had found that the peak cortisol response occurs between 21 and 30 minutes from the onset of the examination, and that it does not depend on the duration of the examination (27). Salivary cortisol levels increase several fold within a short time period after the onset of psychological stress (29), and those results have an agreement with this study while disagree with (30-34), which showed that the results related to written examinations (tests) were heterogeneous and not necessarily accompanied by cortisol increase. The predictive value measurements for salivary cortisol showed highly positive predictive value (PPV) at 50% and 90% levels with the cut- off point of 70.1 ng/ml. Above this point, the salivary cortisol can be used as biomarker for accurate prediction of stress and TMD (accuracy 93.7%). Temporomandibular joint disorder (TMD) represents a common health problem (35). It is an umbrella term embracing a number of clinical manifestations that involve the temporomandibular joint (TMJ), the masticatory muscles and the teeth. Patients with TMD usually suffer from muscle and/or joint pain on palpation and on mandibular movements, joint sounds and the mandibular range of motion may be limited (36). TMD can affect any patients regardless of age including children (37). Or gender with varying signs and symptoms (38). These investigations are in agreement with the result of this study that have found there is no significant difference between age and gender groups for both case groups (stress with TMD) and control without TMD problems, Statistical analysis showed the association of salivary cortisol with the clinical criteria of TMJ that involve pain of soft tissue (muscles and TMJ ligaments), while the other clinical criteria (impaired mobility, impaired TMJ function and painful movement of mandible) did not show any associated with salivary cortisol. This indicate that acute stress causing higher level of cortisol which have greater impact on the early clinical criteria such as muscle pain and TMJ pain and the other criteria that have established mobility impairment may not related to acute stress thus show no association. These other criteria may be related to chronic stress rather than acute type. TMDs can be subdivided into muscular and articular categories. Differentiation between the two is sometimes difficult because muscle disorders may mimic articular disorders, and they may coexist (39). In the present study it was used Helkimo anamnestic and clinical dysfunction index as a scoring for TMD students and the results that the muscles have pain on palpation as following: Masseter muscles (40%), Temporalis (31%), lateral pterygoid (9%), medial pterygoid (6%), anterior diagastric (4%) and Sternocleidomastoid (2%), while the students with no symptoms of myofascial pain (8%). Parafunctional habits of masticatory muscles, with and without associated chronic pain. In this study the distribution percentage of varying oral habits in TMD students that shown as follow: Clenching (28.3%), Bruxism (21.7%),Chewing: lip, gum, pen, cheek (15%), Grinding (8.3%), Bitting nail (6.7%), while those have no parafunctions habits was (20%). 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Tex Dent J 2000;117(7):30-9 J Bagh College Dentistry Vol. 27(2), June 2015 Assessment of cortisol Oral Diagnosis 92 الخالصة غیر حیوي لمؤشر ماسة حاجة نشأت لذلك نتیجة .النھائیة االمتحانات قبل النفسي التوتر من عالیة مستویات الى یتعرضون االسنان طب كلیة طلبة ان : الخلفیة ھلكیمو نظام استخدام أن .التوتر لقیاس حیوي كمؤشر اللعابي الكورتیزول ھرمون اعتبرت دراسات دةع ھنالك .الجامعة طلبة عند الحاد التوتر لقیاس تداخلي الوظیفي الصدغي المفصل واختالل الحیوي المؤشر ھذا بین العالقة عن جید تصور یعطي ان ممكن الصدغي للمفصل السریري الوظیفي االختالل مدى لتسجیل .السریري وھذا .الوظیفي الصدغي المفصل اختالل من یعانون واللذین للتوتر تعرضھم عند الجامعة طلبة عند اللعابي الكورتیزول ھرمون مستوى متقیی ھو :الدراسة اھداف .الصدغي لمفصل السریري الوظیفي الختالل مسبب كعامل النفسي التوتر لدور افضل فھم یعطینا ربما الى عشرین بین اعمارھم تتراوح اللذین بغداد جامعة االسنان طب كلیة طلبة من ثمانین من متكونة مجموعة على الدراسة ھذه انجاز تم : العمل وطریقة المواد سریریا فكانوا البقیة العشرون أما .الدراسة كمجموعة اختیروا الصدغي المفصل في سریري وظیفي اختالل من یعانون طالبا ستون منھم كان .عاما وعشرین اربعة واختالل اضطرابات وتشخیص البحث لمعاییر وفقا المشاركین فحص تم وقد .المراقبة كمجموعة اختیروا واللذین الصدغي المفصل في ظیفيو اختالل اي بدون .اللعابیین والكورتیزول االمیلیز تركیز لقیاس النھائي االمتحان قبل المحفز الغیر اللعاب عینات من لترات ملي خمسة جمع تم .ھلكیمو نظام حسب الصدغي المفصل .فیالدراسة للمشاركین الصدغي للمفصل الوظیفي االختالل و الكورتیزول ھرمون مستوى بین طردیة عالقة النتائج اظھرت لقد : النتائج السریري الوظیفي ختاللباال وعالقتھ الجامعة طلبة عند النفسي التوتر لقیاس حیوي كمؤشر الكورتیزول ھرمون استخدام امكانیة الدراسة ھذه من نستنتج : استنتاج .الصدغي للمفصل