Functional disorders of the stomatognathic system constitute a wide spectrum of pathologies including dysfunctions affecting temporo-mandibular joints and masseter muscles which are responsible for proper mobility of mandible and occlusion. These dysfunctions are manifested by pain in the ear region, impairment of the course of abduction and adduction of the mandible, lack of symmetry of its lateral movements and excessive tension of stomatognathic system’s muscles.

Among functional complaints reported by patients, auriculo-vestibular symptoms such as earache, plugged ears sensation, sudden hearing impairment, tinnitus, dizziness and burning pain of the throat can be observed (1-3).

One of the main aims of prosthetic therapy of masticatory organ functional disorders’ syndrome is the eradication of articular and muscular pain, and restoration of normal functioning of the stomatognathic system, including symmetric and physiological function of the masseter muscles. Consecutive rehabilitation plays an adjuvant role in the therapy (4, 5).

The aim of the present study is the assessment of co-occurrence of functional disorders of the masticatory organ in patients referred for otolaryngological treatment because of auriculo-vestibular symptoms.


MATERIAL AND METHODS
Forty-two patients aged 24-46 years of both sexes (with prevalence of females), who were presented for otolaryngological treatment, were qualified for our study within the framework of the research project. The auriculo-vestibular symptoms reported by the patients included earache, tinnitus, hypoacusia, sudden hearing impairment and dizziness.

Specialist diagnostic examinations were carried out in the Otolaryngological Department and the Chair of Dental Prosthetics of the Jagiellonian University Medical College in Cracow. The laryngological investigation contains tests such as basic clinical assessment, including otoscopy, tuning fork trials, tonal and verbal audiometry, tympanometric measurements (assessment of stapes reflex) and electronystagmography.

In otolaryngological examination, the following symptoms were assessed: occurrence of inflammation (reddening, oedema), ulceration of the auricle, presence of nodules, anatomical deformities, fistulas and cicatrization. Instrumental examination included otoscopy, tuning fork trials, tonal audiometry, tympanometry and electronystagmography. Otoscopy was performed with the use of an electric otoscope with inbuilt low-voltage light and a magnifying system. During this examination, the condition of the external auditory canal and the tympanic membrane were evaluated with special attention paid to its colour, tone, transparency, mobility and presence of post-inflammatory cicatrization. Tuning fork trials allowed to assess conduction of both ears with Weber and Rinne test (using a 512 Hz tuning fork type C). Tonal audiomerty was carried out to determine the hearing threshold for clear tons, that is, deprived of harmonic vibrations, and to determine the threshold for normal hearing; the aim of verbal audiometry was to assess the ability of speech discrimination. In tympanometric examination, the acoustic resistance of the tympanic membrane was registered during the change of pressure in the external and internal ear. Electronystagmography was used for the diagnostics of spontaneous and induced nystagmus on the basis of the changes of the corneal and retinal potential and amplitude, frequency and nystagmus speed.

After otolaryngological examinations, the patients were referred to the Department of Dental Prosthetics of the Jagiellonian University Medical College for specialist functional tests of the masticatory organ.

Dental diagnostics included patients’ history and specialist functional tests carried out in accordance with stomatognatic system functional analysis form, used in Department of Prosthetic Dentistry.

Information concerning the general patients’ condition, as well as drugs used on pain occurrence or other symptoms or dysfunctions within head and face region, interfering with physiological activity of masticatory organ (food mastication, long-term speech) were recorded on patients’ history. In case of muscle pain or/and temporo-mandibular joints pain, the most important was its location, intensity, irradiation, duration, circumstances accompanying pain intensification or remission, and tension headache. In patients that reported appearance of acoustic symptoms, time of occurrence was crucial, as well as, if the symptoms lasted uninterrupted to the moment of dental examination. Taking into consideration etiological factors, information concerning the occurrence of parafunctions, especially in dental articulation (proceeding with opposing teeth contact), including bruxism, was crucial. Patients were also asked to make self-assessment of their psycho-emotional condition, frequency of stress situations’ occurrence, and methods of stress management. While conducting masticatory organ functional examination, condition and pathologies present within dentition (pathological teeth attrition, malocclusions) and extent of dental defects were estimated. The significant part of the examination was assessment of path and range, as well as adduction and abduction jaw movements and lateral mandibular movements’ symmetry. Position of static occlusion was examined (with occlusal tracing paper) and dynamic occlusion (visual examination of contact configuration of the opposing teeth) in laterotrusive and mediotrusive side.

On palpation of masticatory organ muscles (masseter, temporal muscle, lateral pterygoid, medial pterygoid as well as biventer muscle, and floor of mouth) the level of muscle tone in comparison to physiological norm was examined, and the occurrence of provoked pain was estimated. On examination of temporo-mandibular joints close attention was paid to the occurrence of acoustic symptoms during mandible vertical movements and their character (e.g. crepitus, grating sounds), and pain ailments on palpation and mandible motion.

The specialist examination was supplemented with the close analysis of functional temporo-auricular radiograms of temporo-mandibular joints, taken in Schuller projection in mandible central occlusion and maximum mandible adduction. These examinations allow for direct assessment of the joint osseous structure, position of articular heads in glenoid cavity being crucial for diagnostics, indirect assessment of articular discs and the range of articular heads mobility in joints (e.g. joint subluxation). Examinations were carried out and the results prepared in Chair of Radiology JU MC. For functional examination results, analysis of mandible articular heads location in central occlusion was significant, assessed indirectly based on the dimension of articular fossa (frontal dimension- in front of the articular head, upper dimension- above articular head, back dimension- behind the articular head) and the location of articular heads in the maximum mandible adduction.

Dental and functional examinations of the stomatognathic system were supplemented with electromyography of the masseter muscles’ tone and the anterior part of the temporal muscles at central occlusion, simultaneously for the right and left side, using an eight-channel device BIO EMG II. Superficial bipolar electrodes were used with constant distance between the measuring poles, which were placed along the course of muscular fibres. Surface electrode was located in the medial line of the forehead. During EMG examination the patient was in a sitting position with no back support, his hands resting on the knees.

Electromyography was repeated three times at each examination session. Average values were analyzed in order to assess objectively the patients’ muscular tone, and to compare their electric potentials with the normal potential levels for the masseter and anterior part of temporalis muscles. The asymmetry between the activities of left and right-side muscles was quantified by the asymmetry index Naeije i Maccarolla (6).



RMS – root mean square value

A positive index indicates a right – side dominance and negative index a left – side dominance of muscle´s activity.

The results obtained underwent statistical analysis based on the calculation of mean values, mean standard deviations, minimal and maximal values, analysis of variance test for dependent random variables, and Tukey’s post-hoc test.


RESULTS
Results of otolaryngological examinations

Specialist otolaryngological examinations among 12 patients (out of 42) showed no otolaryngological cause of the reported auriculo-vestibular symptoms such as sudden occurrence of low-intensity tinnitus, otalgia lasting 2-3 weeks, plugged ears sensation, burning pain of the throat and dizziness at various times of the day. Otolaryngological treatment of auriculo-vestibular symptoms in the group of remaining 30 patients was effective.

Results of functional examinations of the masticatory organ

Functional examinations of the masticatory organ carried out among 42 patients revealed no disorders in 30 patients, and numerous dysfunctions in 12 patients (8 females and 4 men). Out of 12 patients, only 10 fully dentulous patients (7 females and 3 males), 7 were qualified for further dental examinations; 2 partially edentulous patients were excluded from the study because of numerous missing teeth in both jaws with no prosthetic restoration, which could prevent correct interpretation of the results.

The history elicited from the patients revealed self-induced pain in the peri-auricular region lasting about 1-12 weeks, located in one or both sides of the face. The pain appeared during mastication or in border left and right lateral jaw position that is in the maximal mandible depression or mandible adduction as well as during lateral mandibular movements. Pain irradiation in temporal and occipital region was recorded in 4 cases. Acoustic symptoms, heard by patients at least 2 months before the prosthetic consultation, were reported by 3 patients. Earlier, sudden maximal dimension of mandible depression limitation was noted in 2 patients. Difficulties with mastication and intensified masseter muscle and temporalis muscle tone, were recorded in 4 patients. Auriculo-vestibular symptoms (plugged ears sensation, hearing impairment, burning in the throat) were recorded in all patients’ histories. The results of the subjective examination are presented in Table 1.

Table 1. The results of the subjective examination.

The functional analysis disclosed deviation from the norm in maximal dimension of mandible depression (up to 18 mm), and mandible lateral movements (up to 5 mm). Abnormal jaw path and disturbances in vertical movements were recorded in 7 patients. Rest position distance was smaller in 2 patients. Configuration of occlusal contacts in central and eccentric occlusion was abnormal in 8 patients. In 5 cases pain on palpation was noted and in 7 cases pain in temporo-mandibular joints, provoked by palpation, was recorded. Increased muscle tone on palpation was present in all patients. Masseter muscle hypertrophy was noted in 1 case and the symptoms of parafunctions occurrence in oral cavity region were detected in 7 patients. Occurrence of acoustic symptoms such as crepitus in temporo-mandibular joints was confirmed in 3 patients (Table 2).

Table 2. Results of functional stomatognatic system examinations.

Radiographic analysis of functional temporo-auricular radiograms of temporo-mandibular joints taken in Schuller projection revealed asymmetry in the position of the mandibular heads in the temporal fossa in the position of central occlusion in 2 cases and excessive dimension of mandible depression in 1 case (Fig. 1).

Fig. 1. Asymmetry in the position of the mandibular heads in the temporal fossa in the position of central occlusion in radiographic investigation.

Electromyographic examination of the masseter muscles and anterior temporal muscles confirmed clinically manifested increased tone of these muscles in the central occlusion (Table 3 and 4). Lack of symmetry in the muscular tone was noted, which was proved by the difference in the potentials of the right and left sides of the same muscle ranging between 4.7 µV and 42.5 µV. Muscle tone asymmetry index was positive for masseter muscles (2.641), which indicates the right-side muscle activity dominance, and negative for temporal muscles (-2.944), which shows left-side muscle activity dominance (Table 5).

Table 3. Electric potentials of masseter and temporalis muscle expressed in micro voltage-µV.

Table 4. Assessemet of the level of significance for electric potentials of examined muscles.

Table 5. The asymmetry index of the masseter and anterior part of temporalis muscles.

Excess of the physiological level of muscular tone, the norm of which is within 10-15 µV (5), ranged from about 30 µV to 120 µV for the masseter muscles, and from 10 µV to 105 µV for the temporal muscles. It indicated that in patients with no otolaryngological causes of auriculo-vestibular symptoms, the predominant problem was functional disorder of the masticatory organ accompanied by the increase in muscular tone markedly exceeding the physiological norm.

In the group of 12 patients referred to the Otolaryngological Department, successive prosthetic treatment was performed with the use of occlusive splints and reconstructive procedures, aiming at restoration of correct relation between the jaws, combined with physiotherapy and psychological support. In follow-up examinations carried out after 6 and 9 months of the prosthetic treatment beginning, the auriculo-vestibular symptoms were excluded in all patients.


DISCUSSION
Common occurrence of auriculo-vestibular symptoms with functional disorders of the masticatory organ is receiving more and more attention in literature. This co-existence can be associated with the common filogenetic and ontogenetic development of the muscles: medial pterygoid, soft palate tensor and tympanic tensor, which originate from the first branchial arch (6-8). Moreover, anatomical adjacency of the temporo-mandibular joints and the middle ear can promote transmission of excessive mechanical forces originating from the region of the TM joints to the ear via the disc-malleus ligament or as a result of direct pressure and irritation of the auriculo-temporal nerve by the mandibular head in the region of the petro-tympanic fissure. This creates an impulse for reflex contraction of the tympanic tensor muscle. Posterior translocation of the mandibular heads can cause pressure on the tympanic artery and vein, leading to the blood supply impairment and functions of the middle ear, contraction of the stapes muscle and, in consequence, immobilization of the stapes. In these reciprocal relations, the innervation of the tympanic tensor, soft palate tensor and masseter muscles by the mandibular branch of the trigeminal nerve seems to play a significant role. The increase in the tone of one group of muscles is frequently accompanied by excessive tension in the muscles of the other group (9-15). Functional disorders of the masticatory organ are frequently reported by patients seeking prosthetic treatment. Co-ocurence of auriculo-vestibular symptoms such as: hearing impairment, dizziness, tinnitus, diagnosed in the control group, have been noticed by many authors treating patients with functional dysfunctions of masticatory organ (16-24).

Tinnitus and dizziness analyzed by Chole R. (25) appeared significantly more often in patients with functional disorders than in control group formed with patients searching general medical treatment.

Among patients referred to Department of Otolaryngology females predominated (7 females and 3 men), which was also noticed by Lam et al. (26), as from among 344 examined patients with functional disorders, women significantly outnumbered men. Alarmingly high percentage of patients in this study constituted patients with auriculo-vestibular symptoms (59%).

The results of the examinations that were carried out, indicate necessity of functional dysfunctions’ verification within the stomatognatic system in case of lack of otolaryngological causes of auriculo-vestibular symptoms, according to Turp and Ramirez (18, 24). In Tuz H. et al. study the incidence of auriculo-vestibular symptoms’ occurrence in a group of patients with functional disorders was estimated and it was demonstrated that in a group of 200 examined patients 77.5%, that is 155 persons, were diagnosed with at least one of the symptoms regarded as auriculo-vestibular group (29). The similar incidence was stated by Manni et al., as in 53 patients treated due to functional disorders, 67.9% of patients were diagnosed with at least one functional disorder (10).

Results of electric potentials of masseter and anterior part of temporal muscles’ estimation, analyzed in activity, in central mandibular occlusion, indicate much higher electric potentials in comparison to physiological norm. Similar results were achieved by numerous authors who compared the tension level of masseter and temporal muscles in patients with stomatognatic system functional disorder and healthy controls (16, 18, 19, 24, 27-29). Different results can be found in Manni et al. study because higher electric potentials were observed in control group than in patients treated due to functional disorders (10).

In case of 10 patients examined in a study (referred from Department of Otolaryngology) application of specialist prosthetic treatment caused permanent disappearance of auriculo-vestibular symptoms. The same result is described by Cooper et al. and Kuttila M et al. who conducted orthopedic treatment with occlusal splints used to reposition the jaw in patients with functional disorders having symptoms such as: earache, hearing impairment, tinnitus. This caused the significant reduction or disaapearance of auriculo-vestibular symptoms (30, 31). Peloz in his study emphasizes that in 37% of 221 treated patients with functional disorders, there were some auricular symptoms that were eliminated by the use of stabilization splint, commonly used in prosthetic treatment. Moreover, correlation between the incidence of auriculo-vestibular symptoms and clinically diagnosed disc dislocation without blocking was found by the author (32).

The accompanying otolaryngological symptoms impede the patients’ everyday life, their professional work as well as correct diagnosis of this disorder. Tinnitus can interfere with speech understanding and hinder sleep, dizziness is a frequent cause of the fear of free mobility. Because of otolaryngological symptoms caused by this disorder, the patients are frequently referred for specialist treatment which is not related to stomatognathic system (16-20). The coexistence of auriculo-vestibular symptoms and otolaryngological disorders within the masticatory organs is due to the activation of the brain-auriculo-ventricular axis, mediated mostly via trigeminal nerves. The treatment of masticatory organ disorders requires multi-specialistic and therapeutic approach.


CONCLUSIONS
Results of dental examinations revealed numerous abnormalities of the function and biomechanics in the masticatory organ which can coexist with otolaryngological symptoms of auriculo-vestibular type.

Functional disorders of the masticatory organ and auriculo-vestibular symptoms, observed in our study, require preparation and introduction of common otolaryngological and dental management for diagnostics and therapy of patients with this kind of disorder.

Acknowledgements: We are very grateful to Professor Stanislaw Konturek for his assistance and kindness.

Conflict of interests: None declared.


REFERENCES

1. Majewski S. Gnatofizjologia stomatologiczna. Normy okluzji i funkcje uk³adu stomatognatycznego [Dental gnathophysiology. Occlusal norms and stomatognatic system functions]. Warszawa/Lviv, PZWL, 2007/2008.
2. Okeson J. Leczenie dysfunkcji narz¹du ¿ucia i zaburzeñ zwarcia [Treatment of the temporo-mandibular joint disorders and occlusial dysfunction]. Lublin, Czelej, 2005.
3. Pihut M, Wisniewska G, Majewski P, Gronkiewicz K, Majewski S. Assessment of occlusal forces in the therapy of functional disorders with the use of botulinum toxin type A. J Physiol Pharmacol 2009; 60(Suppl 8): 113-116.
4. Krzek A. Atypical otalgia. Wiad Lek 1984; 37: 788-791.
5. Lewandowski L, Wybieralski J. Odontogenic and stomatogenic otalgia in diseases of the teeth, mouth and jaws. Otolaryngol Pol 1982; 36: 301-304.
6. Visser A, McCarroll R, Naeije M. Masticatory muscle activity in different jaw relation during submaximal clenching efforts. J Dent Res 1992; 71: 372-379.
7. Gola R, Chossegros C, Orthlieb JD, Lepetre C, Ulmer E. Otologic manifestations of the pain dysfunction syndrome of the stomatognathic system. Rev Stomatol Chir Maxillofac 1992-1993; 4: 224-230.
8. Kryshtalskyj B. The role of diagnostic arthroscopy in the management of temporomandibular joint dysfunction. J Otolaryngol 1991; 20: 325-328.
9. Powers WH, Britton BH. Nonotogenic otalgia: diagnosis and treatment. Am J Otol 1990; 2: 97-104.
10. Manni A, Brunowi P, Giuliani M, Modoni M, Bizzi G. Oto-vestibular symptoms in patients with temporomandibular joint dysfunction. Electomyographic study. Minerva Stomatol 1996; 45: 1-7.
11. Vernon J, Griest S, Press L. Attributes of tinnitus that may predict temporomnadibular joint dysfunction. Cranio 1992; 10: 282-287.
12. Jouniss S. The relationship between craniomandibular disorders and otitis media in children. Cranio 1991; 9: 169-173.
13. Menzyk K, Cajdler A, Pokorski M. Influence of physical activity on psychosomatic health in obese women. J Physiol Pharmacol 2008; 59(Suppl 6): 441-448.
14. Murtagh J. The painful ear. Aust Fam Physician 1991; 20: 1779-1783.
15. Vermon J, Griest S, Press L. Atrributes of tinnitus associated with the temporomandibular joint syndrome. Eur Arch Otorhinolaryngol 1992; 249: 93-94.
16. Chan S, Reade P. Tinnitus and temporomandibular pain- dysfunction disorder. Clin Otolaryngol Allied Sci 1994; 19: 370-380.
17. Fanali S, Cerri A. The otoneurological and dental picture of Costen’s pain- dysfunction syndrome. Minerva Stomatol 1993; 42: 37-43.
18. Turp JC. Correlation between myoarthropatlies of the masticatory system and ear symptoms (otalgia, tinnitus). HNO 1998; 46: 303-310.
19. Toller M, Juniper R. Audiological evaluation of the aural symptoms in temporomandibulon joint dysfunction. J Craniomaxillofac Surg 1993; 21: 2-8.
20. Salvinelli F, Casale M, Paparo F, Persico A, Zini C. Subjective tinnitus, temporomandibular joit dysfunction, and serotonin modulation of neural plasticity: casual or casual triad? Med Hypotheses 2003; 61: 446-448.
21. Mordarski S, Lysenko L, Gerber H, Zietek M, Grades T, Dominiak M. The effect of treatment with fentanyl patches on pain relief and improvement in overal daily functionating in patients with postherapeutic neuralgia. J Physiol Pharmacol 2009; 60(Suppl 8): 31-35.
22. Ciancaglini R, Loreti P, Radaelli G. Ear, nose, and throat symptoms in patient with TMD: the association of symptoms according to severity of arthopathy. J Orofac Pain 1994; 8: 293-297.
23. Remizer L, Ballesteros L, Sandoval G. Otological symptoms among patients with temporo-mandibular joint disorder. Rev Med Chil 2007; 135: 1582-1590.
24. Remizer L, Ballesteros L, Sandoval G. Topical review: temporo-mandibular disorder in an integral otic symptom model. Int J Audiol 2008; 47: 215-227.
25. Chole R, Parker W. Tinnitus and vertigo in patients wits temporo-mandibular disorder. Arch Otolaryngol Head Neck Surg 1992; 118: 817-821.
26. Lam D, Lawrence H, Tenebaum H. Aural symptoms in temporo-mandibular disorder patients attending a craniofacial pain unit. J Orofac Pain 2001; 15: 146-157.
27. Felicio C, Melchior MO, Ferreira C, Da Silva M. Otologic symptoms of orofacial myofunctional therapy. Cranio 2008; 26: 118-125.
28. Felicio C, Oliveiera M, Silva M. Effects of orofacial myofunctional therapy on temporo-mandibular disorders. Cranio 2010; 28: 249-259.
29. Tuz H, Onder E, Kisnisci R. Prevalence of otologic complaints in patients with temporo-mandibular disorder. Am J Orthod Dentofacial Orthop 2003; 123: 620-623.
30. Cooper B, Cooper D, Lucente F. Electromyography of masticatory muscle in craniomandibular disorders. Laryngoscope 1991; 1: 150-157.
31. Kuttila M, Le Bell Y, Savolainen-Niemi E, Kuttila S, Alanen P. Efficiency of occlusal appliance therapy in secondary otalgia and temporo-mandibular disorders. Acta Odontol Scand 2002; 60: 245-254.
32. Peroz I. Otalgia and tinnitus in patients with craniomandubular dysfunctions. HNO 2001; 49: 713-718.