ORL 2014;76:81–88 DOI: 10.1159/000360994 Received: April 22, 2013 Accepted after revision: February 8, 2014 Published online: April 25, 2014
© 2014 S. Karger AG, Basel 0301–1569/14/0762–0081$39.50/0 www.karger.com/orl
Original Paper
Impact of Identifying Factors Which Trigger Bothersome Tinnitus on the Treatment Outcome in Tinnitus Retraining Therapy Egisto Molini
Mario Faralli
Lucia Calzolaro
Giampietro Ricci
Otolaryngology and Cervico-Facial Surgery Division, Department of Medical-Surgical Specialities and Public Health, University of Perugia, Perugia, Italy
Key Words Tinnitus · Tinnitus retraining therapy · Hyperacusis · Tinnitus Handicap Inventory Abstract The aim of this work was to ascertain any differences in the effectiveness of rehabilitation therapy in relation to the presence or absence of a known negative reinforcement responsible for the tinnitus-related pathology. Between 1 January 2001 and 31 December 2008, we recruited 294 subjects suffering from incapacitating tinnitus and/or hyperacusis. The patients underwent tinnitus retraining therapy (TRT) according to the methods described by Jastreboff and Hazell [Tinnitus Retraining Therapy: Implementing the Neurophysiological Model. Cambridge, Cambridge University Press, 2004, pp 121–133]. We clinically assessed the presence or absence of known phenomena of associative learning, regarding the presence of adverse events temporally correlated with tinnitus and the treatment outcome. The separate analysis of the 2 subgroups shows a statistically significant difference in the improvement rate between the group with a known triggering factor and the group without a triggering factor, with a preponderance of the former with a 91% improvement rate versus approximately 56% for the latter. In our study, the inability to identify factors triggering bothersome tinnitus neg© 2014 S. Karger AG, Basel atively affected the treatment outcome in TRT.
Introduction
Tinnitus, the sensation of sound when there is no external acoustical stimulation [1], is due to the perception of the electrical activity of the auditory nervous system without any mechanical or vibratory activity of the cochlea [2]. Tinnitus is generated within the auditory nervous system. According to the theory of discordant damage [3], it is generated by the auditory periphery following partial damage to the organ of Corti, in which the outer hair cells Mario Faralli ENT, University of Perugia Ospedale S. Maria della Misericordia IT–06156 Perugia (Italy) E-Mail mario.far @ hotmail.it
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(OHC) degenerate, whereas the corresponding inner hair cells (IHC) are spared. The death of the OHC is followed by an increase in the release of glutamate by the undamaged IHC, which is responsible for the onset of tinnitus [4]. The excitatory activity of glutamate is also encouraged by the release of endogenous dynorphins by the lateral efferents at the type 1 nerve endings of the IHC during times of emotional stress [5]. The discordant loss of ciliated cells, with the sequence of described phenomena, leads to an increase in the nervous activity of the cells of the dorsal cochlear nucleus that is directly proportionate to the number of OHC that have been lost [6]. The significant correlation between the level of activity of the dorsal cochlear nucleus and the presence of tinnitus gives this nucleus a highly relevant role as the cerebral centre responsible for modulating tinnitus. Its strategic position and nervous connections (cortical, from the locus coeruleus and the caudal pontine reticular nucleus for auditory attention [7–10] and states of anxiety and fear [11, 12], and from the raphe nuclei for depressive states [13, 14]) also play a key role in the hierarchy of functional processes responsible for the perception of tinnitus [15]. In some cases, tinnitus originates in the central auditory system or in brain structures related to the central auditory system. This statement is supported by the fact that tinnitus persists in patients with vestibular schwannoma after auditory nerve section or destruction of the inner ear [16–18] or begins post-operatively in patients who have not experienced it previously [19]. Tinnitus has also been referred to as a phantom auditory perception [3] because its characteristics resemble those of phantom pain and phantom limbs [3, 20, 21]. Auditory imagery is likewise a phantom perception. It generally refers to perceptions of voices without understandable speech, music or other complex auditory perceptions in the absence of appropriate stimulation [22], and it is a central type of tinnitus involving reverberatory activity in the auditory cortex [23]. Tinnitus is transformed from a simple acoustical phenomenon, and thus acquires clinical significance, when it monopolizes the patient’s attention, interfering with his or her ability to concentrate and hindering normal everyday activities. Moreover, since the perception of tinnitus is associated with a feeling of persistent annoyance, frustration, rage, anxiety and depression, it negatively affects night rest and the quality of sleep. Consequently, it has a strong impact on the perceived quality of life (tinnitus-related pathology). According to the neurophysiological model, a tinnitus-related pathology arises following the association of the auditory phenomenon with one or more negative emotional states; tinnitus is continuously associated with aversive emotional states through a learning process, thus generating a conditioned reflex [14]. Emotive stimuli, processed by the subcortical centres of the brain (the amygdala in the limbic system activated by the posterior nuclei of the thalamus through the thalamic or subcortical pathway, the so-called low road), generate initial autonomic and neuroendocrine reactions that warn the organism, altering the heart rate, regulating perspiration, accelerating the respiratory rate and regulating muscle tension [24, 25]. This rapid and unconscious response represents a primitive defence mechanism. Emotive stimuli, also transmitted simultaneously by the thalamus to the associative cortices (the so-called high road), are processed in a slower but more sophisticated manner, producing a conscious response better suited to the situation [24, 25]. Many patients report that the onset of tinnitus is not correlated with any known event [26] or triggering factor and, in fact, conditioning can also occur in the absence of the perception of a stimulus (unconscious learning) [27]. In this case, the assumptions and considerations made in an attempt to explain the presence of tinnitus, along with the fear of potentially serious medical and psychiatric consequences that are a threat to health, can take on the role of an unconditioned stimulus [28–30]. However, a tinnitus-related pathology can arise in all cases of bothersome tinnitus, even if a triggering factor is not identified. In fact, ‘the negative emotional reactions of the autonomic nervous system (e.g., caused by annoyance due to inability to control tinnitus) are
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sufficient negative reinforcement to create a conditioned reflex linking the tinnitus signal within the auditory pathways with the limbic and the autonomic nervous system and other system in the brain’ [31]. The tinnitus retraining therapy (TRT) adopted by our audiology laboratory uses counselling in order to influence the cortical areas and reduce the negative descending pathways to the subcortical centres, to reclassify tinnitus at the conscious level as unimportant stimulus, reassigning it to the category of neutral stimuli, and to demystify it, thus decreasing the reactions of the autonomic nervous system; these are known to be milder towards a known event than an unknown one, reducing autonomic reactions, creating positive associations with tinnitus and reducing the level of stress. The counselling is associated with sound therapy that decreases the intensity of the tinnitus signal and thus the level of excitation of the subcortical auditory centres, the cortical areas, the limbic system and the autonomic nervous system [32, 33]. The aim of this work was to establish any differences in the effectiveness of rehabilitation therapy in relation to being able to identify a specific factor that can be linked to the emergence of bothersome tinnitus on treatment outcome. Materials and Methods Between 1 January 2001 and 31 December 2008, we progressively recruited 294 subjects suffering from incapacitating tinnitus and/or hyperacusis with an onset at least 6 months earlier. The selected patients were monitored for a minimum of 18 months, at the end of which they were judged to have improved based on the criteria listed below. All the subjects were assessed with two questionnaires: the first, which included a visual analogue scale to determine the extent of the distress caused by tinnitus [34], was supplemented by another one, Tinnitus Handicap Inventory (THI) [35], that made it possible to categorize each patient according to a specific degree of distress (five degrees in increasing order of gravity) [36]. The compilation of the questionnaires allowed us to assign the patients to 5 categories described by Jastreboff and Hazell [37], with category 4 being divided into 2 subcategories. An audiological assessment was then performed, including tonal and vocal audiometry, evaluation of the loudness discomfort level, pitch matching, loudness matching, minimal suppression levels and duration of residual inhibition. To complete the above, once the presence of hyperacusis was excluded, we conducted impedance measurements, investigating the stapedial reflex threshold, brainstem auditory evoked potentials, transient evoked otoacoustic emissions and distortion product otoacoustic emissions. In the cases in which the previous examinations indicated the need for in-depth diagnostic imaging, a cerebral MR was performed. The patients then underwent TRT according to the methods described by Jastreboff and Hazell [38]. Finally, we clinically assessed the presence or absence of the advent of the phenomena of associative learning – conscious and unconscious – regarding the presence of adverse events temporally correlated with tinnitus, such as particular negative circumstances (e.g., the state of health of the patient and his or her family, unpleasant workplace conditions, etc.), physical variations in the characteristics of tinnitus that had previously been well tolerated, negative advice offered by physicians and the media, and assumptions, considerations, personal convictions and ideas related to tinnitus. The results were evaluated after 18 months, comparing our results with the criteria indicated for suspending the therapy [39]; the subjects were considered to have improvement if the score on the scale of symptoms was ≤2, associated with a grade 1 on the THI and an awareness value of the presence of tinnitus of ≤10% in wakefulness, without any interfering with regular activities. If these results were not attained within the established time frame, the therapy was considered a failure.
Results
During the period of the study, we treated 294 patients, of whom 168 (57.14%) were in category 1, 78 (26.53%) in category 2, 36 (12.24%) in category 3, 6 (2.04%) in category 0, and 6 (2.04%) in category 4 T (tinnitus). No subjects from category 4 H (hyperacusis) were treated.
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Table 1. TRT results on the basis of the patients’ categories described by Jastreboff and Hazell [37] and the presence or absence of
triggering factors (see text for explanations) Categories
Total 0 1 2 3 4T 4H
Total patients
Patients with improvement
Patients without improvement
With event total
improved
Without event
294 (100%) 6 (2.04%) 168 (57.14%) 78 (26.53%) 36 (12.24%) 6 (2.04%) –
231 (78.57%) 6 (100%) 151 (89.88%) 46 (58.97%) 28 (77.77) 0 (0%) –
63 (21.42%) 0 (0%) 17 (10.11%) 32 (41.02%) 8 (22.22%) 6 (100%) –
189 (64.28%) 6 (3.17%) 115 (60.84%) 34 (17.98%) 28 (14.81%) 6 (3.17%) –
172 (91%) 17 (8.99%) 6 (100%) 0 (0%) 109 (94.78%) 6 (5.21%) 34 (100%) 0 (0%) 23 (82.14%) 5 (17.85%) 0 (0%) 6 (100%) – –
not improved
total
improved
not improved
105 (35.71%) – 53 (50.47%) 44 (41.9%) 8 (7.61%) – –
59 (56.19%) – 42 (79.24%) 12 (27.27%) 5 (62.5%) – –
46 (43.8%) – 11 (20.75%) 32 (72.72%) 3 (37.5%) – –
Applying the described criteria, we observed recovery in 231 patients (78.57%) divided up as follows: 151 in category 1 (89.88%), 46 in category 2 (58.97%), 28 in category 3 (77.77%), and 6 in category 0 (100%). None of the 6 subjects in category 4 T improved (table 1). The 63 patients (21.42%) who did not improve were divided up as follows: 17 in category 1 (10.11%), 32 in category 2 (41.02%), 8 in category 3 (22.22%), 6 in category 4 T (100%), and none in category 0, as all of them improved (table 1). The study of the presence or absence of a triggering factor showed that it was present in 189 patients (64.28% of the total) and absent in 105 patients (35.71% of the total). Subjects with a negative identified associated event were distributed as follows: 115 (60.84% of the total with an event) were in category 1, 34 (17.98%) in category 2, 28 (14.81%) in category 3, 6 (3.17%) in category 0, and 6 (3.17%) in category 4 T. Of the subjects from this group, 172 (91%) improved. The subdivision of therapeutic success per category is 109 (94.78% of the group with an event) in category 1, 34 (100%) in category 2, 23 (82.14%) in category 3, and 6 (100%) in category 0. None of those in category 4 T improved. In the group with an identified event, 17 (8.99%) did not improve, of whom 6 (5.21%) were in category 1, 5 (17.85%) in category 3, 6 (100%) in category 4 T, and none in either category 0 or 2, as they had already shown improvement. Of the 105 subjects (35.71%) without an identified triggering factor, 53 (50.47%) were in category 1, 44 (41.9%) in category 2, 8 (7.61%) in category 3, and none in categories 0 and 4 T. In this group, 59 patients (56.19% of those without a known triggering factor) improved, and they were distributed as follows: 42 (79.24%) in category 1, 12 (27.27%) in category 2, and 5 (62.5%) in category 3; the other categories were not represented in this group. Lastly, the patients without a known negative event who showed no improvement totalled 46 (43.8% of those without a known triggering factor), of whom 11 (20.75%) were in category 1, 32 (72.72%) in category 2, and 3 (37.5%) in category 3; the other categories were not represented in this group. Discussion and Conclusions
The results of our study show an improvement rate following treatment in line with those reported in the literature, which average around 80% [40, 41] (table 1). All the patients from category 0, defined as being less serious and/or with recent onset of the pathology, improved. The worst results, where no patient improved, were observed in the category with incapacitating tinnitus accentuated by exposure to noise (4 T). Both of the aforesaid categories are composed of only a few individuals, totalling around 4.1% of the cases, and they are thus of little significance in terms of the entire population that was examined. Most of the treated patients – more than half of the total (57.14%) – were represented by subjects in whom the main symptom was tinnitus (category 1). In this category we observed a higher improvement
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rate, approximately 90%, second only to category 0. In patients with hyperacusis (category 3: 12.24% of the total), the rate of improvement (approximately 78%) was comparable to that of the total. The second-worst results – after the patients from category 4 T and in agreement with previous works [42] – were noted in subjects with hypoacusis and tinnitus (category 2: 26.53% of the total), among whom approximately only 59% of the cases improved because full TRT was not implemented [42] (table 1). The breakdown of the case study into 2 subgroups, based on the presence or absence of the triggering factor – conscious or otherwise – associated with tinnitus, has allowed us to make several interesting observations. The patients’ medical histories were drawn up carefully and over a long period of time, not only in the initial meetings but also over the months of treatment, and so an empathetic rapport had been established with the patients. Nevertheless, in 35.71% of the subjects, we did not observe the presence of any triggering factor associated with tinnitus, which led us to surmise that in this population of patients the reactions of the limbic and autonomic nervous system provide negative reinforcement [31], eliciting the conditioned response. Separate analysis of the 2 subgroups shows a statistically significant difference in improvement rate (χ2 = 46.547; p = 0.000) between the group with an identified triggering factor compared to the one without identified triggering factors, with a preponderance of the former with a 91% improvement rate versus approximately 56% for the latter (table 1). A further subdivision by category of the 2 subgroups shows that there is a statistically significant difference in the improvement rate (χ2 = 38.977; p = 0.000) among hypoacusis patients with tinnitus (category 2), in which, in the presence of a known triggering factor, all the patients improved, whereas in the subgroup of subjects without an identified triggering factor there was a low improvement rate (approximately 28%) (table 1). The fact that subjects with both hearing loss and tinnitus (category 2) demonstrate worse therapeutic results has already been reported in the literature [42], and various reasons have been cited. First of all, the cause was sought in the extent of the hearing loss, which was greater in the subjects who did not improve, although statistical analysis did not corroborate this [42]. Second, one of the causes given for unsuccessful therapy was the failure to use a hearing aid, which is essential in this category, given that 80% of the patients who used them improved versus 47.8% of patients with hypoacusis who improved without them [42]. The mechanism responsible for these results, which must nevertheless be viewed critically due to the small number of subjects studied [42], may be explainable with the persistence of a high signal-to-noise ratio in patients without hearing aids and thus the low rate of the effectiveness of sound therapy aimed at inducing habituation for tinnitus perception and eliminating the conditioned reflex. In fact, the appropriate fitting of hearing aids constitutes important remediation for patients who suffer from tinnitus and hearing loss simultaneously. The difficulty in counselling, responsible for habituation to the reaction, can be considered a cause for failure, as these patients rarely manage to achieve the ‘reclassification’ and ‘demystification’ of the memorized tinnitus, defining its presence as innocent and not the cause of hypoacusis, because it is difficult to overcome their conviction that ‘I would hear well if I didn’t have tinnitus’. These results point out that if TRT is not used properly, then results will be worse. In category 1 as well, we noted statistically significant differences in favour of a higher improvement rate in the subgroup in which we identified the presence of the triggering factor in contrast to subjects without an associated event (χ2 = 7.977; p = 0.005). Instead, there were no statistically significant differences between the 2 subgroups in which hyperacusis represented the main problem (category 3) (χ2 = 0.485; p = 0.486). The tinnitus-related pathology arises following phenomena of associative learning, conscious or unconscious. It also arises in all cases of bothersome tinnitus where a triggering factor is not identified; in these cases the only element responsible for the patient’s distress
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is tinnitus, which may simply be annoying because reactions of the limbic and autonomic nervous system give negative reinforcement [31]. We must theorize which mechanisms are responsible for therapeutic failure in subjects in whom the pathology stems from triggering factors. This aspect was particularly evident in category 2, in which none of the patients without known triggering factors improved, but was also present to a significant level in category 1. Moreover, this trend was not confirmed in patients with hyperacusis (category 3), in whom we did not find any statistically significant differences among the results of the 2 subgroups. The approach used to treat all our patients (TRT) uses counselling to arrive at habituation to the reaction by no longer activating the limbic system and autonomic nervous system and, through sound therapy, to habituate the patient to the perception that blocks the arrival of the tinnitus signal at the superior cortical areas responsible for the awareness of its presence. Although it is a slow process, it can gradually be established automatically once habituation to the reaction has been achieved. Habituation is a non-associative learning process that tends to reduce the emotional and behavioural manifestations elicited by tinnitus. Presentation of the conditioned stimulus is required in order to extinguish the conditioned reflex, because habituation can only arise if tinnitus is detected [43, 44]. Habituation, extinction of the orientation reflex and extinction of the conditioned reflex are different terms that essentially refer to the same phenomenon [45]. The rehabilitation therapy for subjects with a tinnitus-related pathology due to the presence of a conditioned reflex helps convert an associative learning process into non-associative habituation. The tinnitus-related pathology is caused by the negative consequences of associative learning with or without identified triggering factors. In the latter, where the ongoing presentation of tinnitus – a stimulus that is annoying in itself regardless of its absolute or relative intensity – is enough on its own to trigger and sustain adverse emotional reactions of the limbic and autonomic nervous system [31], we registered the worst treatment outcome. In category 1, one of the 3 main categories we treated, the therapy was not as effective in subjects in whom we were unable to identify an associated event. The same thing happened in category 2, where the negative results can also be due to factors other than an unidentified triggering factor, such as non-implemented amplification [42]. In patients in whom the prevalent symptom was hyperacusis (category 3), the therapeutic objective was to desensitize the auditory system by systematically exposing the subjects to different sounds, exploiting underlying physiological processes that do not involve the conditioned reflex and conscious thought [46]. To a varying extent, hyperacusis may also be associated with misophonia and the two phenomena are not clearly distinguishable in the same patient [47]. Misophonia is characterized by a negative reaction to a sound with a specific pattern and meaning to a given patient. The physical characteristic of a sound is secondary. Reactions to the sound depend on the patient’s past history and on non-auditory factors like the patient’s previous evaluation of the sound, his or her psychological profile, and the context in which the sound is presented [48]. In misophonia, a condition in which external sounds and noises are disturbing because they are associated with a negative meaning, the therapy is based on associating them with something pleasant in order to arrive at an active extinction of the conditioned reflex [46]. The use of sound generators with the initial sound levels determined by the patient’s annoyance level represents a desensitizing approach that follows the modes used to treat other pathological conditions [49]; these initial sound levels were gradually increased but always kept below the sound level that evokes annoyance used in the therapy of hyperacusis [50]. The treatment of hyperacusis thus requires a completely different approach than the one used for tinnitus and misophonia. Therefore, in the patients in category 3 in whom hyperacusis and misophonia can variably be associated, the therapy that is used is oriented towards active extinction of the conditioned reflex and desensitization
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to external sounds. Category 3 is the only one in which the goal of the therapy is to desensitize the auditory system by systematic exposure to a variety of sounds and to associate those sounds with something positive to reverse the conditioned reflex [46]. In conclusion, the tinnitus-related pathology linked to classic conditioning benefits from rehabilitative therapy in a high percentage of cases in line with those reported in the literature, but our inability to identify factors triggering bothersome tinnitus negatively affects the treatment outcome in the 3 subgroups without a negative event in the main categories. The simplest explanation of this result could be that identifying such factors would positively influence the effectiveness of counselling in the subgroups of patients with a negative event, which would in turn affect the treatment outcome. Identifying a factor providing the negative reinforcement is helpful and can be done effectively but should not be crucial for the treatment in the TRT. Our results could indicate that counselling was not aimed at subgroups without a correlated event and should thus be modified to decrease the need for identifying a specific factor linked to the emergence of bothersome tinnitus, shifting the focus toward mechanisms involved in generating the tinnitus signal, and they point out that it is correct to disregard which factor was involved in creating functional links between the auditory and the limbic and the autonomic nervous systems. Our experience indicates that the good results achieved with TRT in patients with debilitating tinnitus can be improved further by adapting counselling in subgroups without a correlated event and by completing therapy with the use of hearing aids when indicated.
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Pulec JL: Tinnitus: surgical therapy. Am J Otol 1984;5:479–480. Berliner KL, Shelton C, Hitselberger WE, Luxford WM: Acoustic tumours: effect of surgical removal on tinnitus. Am J Otol 1992;13:13–17. Moller AR: Similarities between chronic pain and tinnitus. Am J Otol 1997;18:577–585. Muhlnickel W, Elbert T, Taub E, Flor H: Reorganization of auditory cortex in tinnitus. Proc Natl Acad Sci USA 1998;95:10340–10343. Godwin PE: Tinnitus and auditory imagery. Am J Otol 1980;2:5–9. Jastreboff PJ, Hazell JWP: Tinnitus Retraining Therapy: Implementing the Neurophysiological Model. Cambridge, Cambridge University Press, 2004, p 7. Cannon WB: Bodily Changes in Pain, Hunger, Fear, and Rage. New York, Appleton, 1920. Schachter S, Singer J (eds): Cognitive, social, and physiological determinants of emotional state. Psychol Rev 1962;69:379–399. Meikle MB, Griest SE: Gender-based differences in characteristics of tinnitus. Hear J 1989;42:68–76. LeDoux JE: The Emotional Brain: The Mysterious Underpinnings of Emotional Life. New York, Touchstone, 1998. Henry JA, Schechter MA, Nagler SM, Fausti SA: Comparison of tinnitus masking and tinnitus retraining therapy. J Am Acad Audiol 2002;13:559–581. Jastreboff PJ: Clinical implication of the neurophysiological model of tinnitus; in Reich GE, Vernon JA (eds): Proceedings of the Fifth International Tinnitus Seminar 1995. Portland, American Tinnitus Association, 1996, pp 500–507. Jastreboff PJ, Hazell JWP: Treatment of tinnitus based on a neurophysiological model; in Vernon JA (ed): Tinnitus Treatment and Relief. Needham Heights, Allyn & Bacon, 1998, pp 201–217. Jastreboff PJ, Hazell JWP: Tinnitus Retraining Therapy: Implementing the Neurophysiological Model. Cambridge, Cambridge University Press, 2004, p 46. Jastreboff PJ, Hazell JWP: Tinnitus Retraining Therapy: Implementing the Neurophysiological Model. Cambridge, Cambridge University Press, 2004, pp 85–114. Jastreboff PJ, Hazell JWP: Tinnitus Retraining Therapy: Implementing the Neurophysiological Model. Cambridge, Cambridge University Press, 2004, pp 115–120. Jastreboff PJ, Hazell JWP: Tinnitus Retraining Therapy: Implementing the Neurophysiological Model. Cambridge, Cambridge University Press, 2004, pp 229–230. Newmann CW, Jacobson GP, Spitzer JB: Development of the tinnitus handicap inventory. Arch Otolaryngol Head Neck Surg 1996;122:143–148. McCombe A, Bagueley D, Coles R, McKenna L, McKinney C, Windle-Taylor P: Guidelines for the grading of tinnitus severity: the results of a working group commissioned by the British Association of Otolaryngologists, Head and Neck Surgeons, 1999. Clin Otolaryngol 2001;26:388–393. Jastreboff PJ, Hazell JWP: Tinnitus Retraining Therapy: Implementing the Neurophysiological Model. Cambridge, Cambridge University Press, 2004, pp 121–133. Jastreboff PJ, Hazell JWP: Tinnitus Retraining Therapy: Implementing the Neurophysiological Model. Cambridge, Cambridge University Press, 2004, pp 63–142. Jastreboff PJ, Hazell JWP: Tinnitus Retraining Therapy: Implementing the Neurophysiological Model. Cambridge, Cambridge University Press, 2004, pp 145–169. Herraiz C, Hernandez FJ, Plaza G, De Los Santos G: Long-term clinical trial of tinnitus retraining therapy. Otolaryngol Head Neck Surg 2005;133:774–779. Sheldrake JB, Hazell JWP, Graham RL: Results of tinnitus retraining therapy; in Hazell JWP (ed): Proceedings of the Sixth International Tinnitus Seminar. London, Tinnitus Hyperacusis Centre, 1999, pp 292–296. Molini E, Faralli M, Calenti C, Ricci G, Longari F, Frenguelli A: Personal experience with tinnitus retraining therapy. Eur Arch Otolaryngol 2010;267:51–56. Konorski J: Conditioned Reflexes and Neuronal Organization. London, Cambridge University Press, 1948. Falls WA: Extinction: a review of theory and the evidence suggesting that memories are not erased with nonreinforcement; in O’Donohue W (ed): Learning and Behaviour Therapy. Needham Heights, Allyn & Bacon, 1998, pp 205–299. Henry JA, Trune DR, Robb MJA, Jastreboff PJ: Tinnitus Retraining Therapy: Clinical Guidelines. San Diego, Plural Publishing, 2007, p 45. Jastreboff PJ, Hazell JWP: Tinnitus Retraining Therapy: Implementing the Neurophysiological Model. Cambridge, Cambridge University Press, 2004, p 51. Jastreboff PJ, Jastreboff MM: Tinnitus retraining therapy for patients with tinnitus and decreased sound tolerance. Otolaryngol Clin North Am 2003;36:321–336. Jastreboff PJ, Jastreboff MM: Using TRT to treat hyperacusis, misophonia and phonophobia. ENT Audiol News 2013;21:88–90. McKenna L, Baguley D, McFerran D: Living with Tinnitus and Hyperacusis. London, Sheldon Press, 2010, p 105. Jastreboff PJ, Hazell JWP: Tinnitus Retraining Therapy: Implementing the Neurophysiological Model. Cambridge, Cambridge University Press, 2004, p 130.
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Original Paper
Impact of Identifying Factors Which Trigger Bothersome Tinnitus on the Treatment Outcome in Tinnitus Retraining Therapy Egisto Molini
Mario Faralli
Lucia Calzolaro
Giampietro Ricci
Otolaryngology and Cervico-Facial Surgery Division, Department of Medical-Surgical Specialities and Public Health, University of Perugia, Perugia, Italy
Key Words Tinnitus · Tinnitus retraining therapy · Hyperacusis · Tinnitus Handicap Inventory Abstract The aim of this work was to ascertain any differences in the effectiveness of rehabilitation therapy in relation to the presence or absence of a known negative reinforcement responsible for the tinnitus-related pathology. Between 1 January 2001 and 31 December 2008, we recruited 294 subjects suffering from incapacitating tinnitus and/or hyperacusis. The patients underwent tinnitus retraining therapy (TRT) according to the methods described by Jastreboff and Hazell [Tinnitus Retraining Therapy: Implementing the Neurophysiological Model. Cambridge, Cambridge University Press, 2004, pp 121–133]. We clinically assessed the presence or absence of known phenomena of associative learning, regarding the presence of adverse events temporally correlated with tinnitus and the treatment outcome. The separate analysis of the 2 subgroups shows a statistically significant difference in the improvement rate between the group with a known triggering factor and the group without a triggering factor, with a preponderance of the former with a 91% improvement rate versus approximately 56% for the latter. In our study, the inability to identify factors triggering bothersome tinnitus neg© 2014 S. Karger AG, Basel atively affected the treatment outcome in TRT.
Introduction
Tinnitus, the sensation of sound when there is no external acoustical stimulation [1], is due to the perception of the electrical activity of the auditory nervous system without any mechanical or vibratory activity of the cochlea [2]. Tinnitus is generated within the auditory nervous system. According to the theory of discordant damage [3], it is generated by the auditory periphery following partial damage to the organ of Corti, in which the outer hair cells Mario Faralli ENT, University of Perugia Ospedale S. Maria della Misericordia IT–06156 Perugia (Italy) E-Mail mario.far @ hotmail.it
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(OHC) degenerate, whereas the corresponding inner hair cells (IHC) are spared. The death of the OHC is followed by an increase in the release of glutamate by the undamaged IHC, which is responsible for the onset of tinnitus [4]. The excitatory activity of glutamate is also encouraged by the release of endogenous dynorphins by the lateral efferents at the type 1 nerve endings of the IHC during times of emotional stress [5]. The discordant loss of ciliated cells, with the sequence of described phenomena, leads to an increase in the nervous activity of the cells of the dorsal cochlear nucleus that is directly proportionate to the number of OHC that have been lost [6]. The significant correlation between the level of activity of the dorsal cochlear nucleus and the presence of tinnitus gives this nucleus a highly relevant role as the cerebral centre responsible for modulating tinnitus. Its strategic position and nervous connections (cortical, from the locus coeruleus and the caudal pontine reticular nucleus for auditory attention [7–10] and states of anxiety and fear [11, 12], and from the raphe nuclei for depressive states [13, 14]) also play a key role in the hierarchy of functional processes responsible for the perception of tinnitus [15]. In some cases, tinnitus originates in the central auditory system or in brain structures related to the central auditory system. This statement is supported by the fact that tinnitus persists in patients with vestibular schwannoma after auditory nerve section or destruction of the inner ear [16–18] or begins post-operatively in patients who have not experienced it previously [19]. Tinnitus has also been referred to as a phantom auditory perception [3] because its characteristics resemble those of phantom pain and phantom limbs [3, 20, 21]. Auditory imagery is likewise a phantom perception. It generally refers to perceptions of voices without understandable speech, music or other complex auditory perceptions in the absence of appropriate stimulation [22], and it is a central type of tinnitus involving reverberatory activity in the auditory cortex [23]. Tinnitus is transformed from a simple acoustical phenomenon, and thus acquires clinical significance, when it monopolizes the patient’s attention, interfering with his or her ability to concentrate and hindering normal everyday activities. Moreover, since the perception of tinnitus is associated with a feeling of persistent annoyance, frustration, rage, anxiety and depression, it negatively affects night rest and the quality of sleep. Consequently, it has a strong impact on the perceived quality of life (tinnitus-related pathology). According to the neurophysiological model, a tinnitus-related pathology arises following the association of the auditory phenomenon with one or more negative emotional states; tinnitus is continuously associated with aversive emotional states through a learning process, thus generating a conditioned reflex [14]. Emotive stimuli, processed by the subcortical centres of the brain (the amygdala in the limbic system activated by the posterior nuclei of the thalamus through the thalamic or subcortical pathway, the so-called low road), generate initial autonomic and neuroendocrine reactions that warn the organism, altering the heart rate, regulating perspiration, accelerating the respiratory rate and regulating muscle tension [24, 25]. This rapid and unconscious response represents a primitive defence mechanism. Emotive stimuli, also transmitted simultaneously by the thalamus to the associative cortices (the so-called high road), are processed in a slower but more sophisticated manner, producing a conscious response better suited to the situation [24, 25]. Many patients report that the onset of tinnitus is not correlated with any known event [26] or triggering factor and, in fact, conditioning can also occur in the absence of the perception of a stimulus (unconscious learning) [27]. In this case, the assumptions and considerations made in an attempt to explain the presence of tinnitus, along with the fear of potentially serious medical and psychiatric consequences that are a threat to health, can take on the role of an unconditioned stimulus [28–30]. However, a tinnitus-related pathology can arise in all cases of bothersome tinnitus, even if a triggering factor is not identified. In fact, ‘the negative emotional reactions of the autonomic nervous system (e.g., caused by annoyance due to inability to control tinnitus) are
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sufficient negative reinforcement to create a conditioned reflex linking the tinnitus signal within the auditory pathways with the limbic and the autonomic nervous system and other system in the brain’ [31]. The tinnitus retraining therapy (TRT) adopted by our audiology laboratory uses counselling in order to influence the cortical areas and reduce the negative descending pathways to the subcortical centres, to reclassify tinnitus at the conscious level as unimportant stimulus, reassigning it to the category of neutral stimuli, and to demystify it, thus decreasing the reactions of the autonomic nervous system; these are known to be milder towards a known event than an unknown one, reducing autonomic reactions, creating positive associations with tinnitus and reducing the level of stress. The counselling is associated with sound therapy that decreases the intensity of the tinnitus signal and thus the level of excitation of the subcortical auditory centres, the cortical areas, the limbic system and the autonomic nervous system [32, 33]. The aim of this work was to establish any differences in the effectiveness of rehabilitation therapy in relation to being able to identify a specific factor that can be linked to the emergence of bothersome tinnitus on treatment outcome. Materials and Methods Between 1 January 2001 and 31 December 2008, we progressively recruited 294 subjects suffering from incapacitating tinnitus and/or hyperacusis with an onset at least 6 months earlier. The selected patients were monitored for a minimum of 18 months, at the end of which they were judged to have improved based on the criteria listed below. All the subjects were assessed with two questionnaires: the first, which included a visual analogue scale to determine the extent of the distress caused by tinnitus [34], was supplemented by another one, Tinnitus Handicap Inventory (THI) [35], that made it possible to categorize each patient according to a specific degree of distress (five degrees in increasing order of gravity) [36]. The compilation of the questionnaires allowed us to assign the patients to 5 categories described by Jastreboff and Hazell [37], with category 4 being divided into 2 subcategories. An audiological assessment was then performed, including tonal and vocal audiometry, evaluation of the loudness discomfort level, pitch matching, loudness matching, minimal suppression levels and duration of residual inhibition. To complete the above, once the presence of hyperacusis was excluded, we conducted impedance measurements, investigating the stapedial reflex threshold, brainstem auditory evoked potentials, transient evoked otoacoustic emissions and distortion product otoacoustic emissions. In the cases in which the previous examinations indicated the need for in-depth diagnostic imaging, a cerebral MR was performed. The patients then underwent TRT according to the methods described by Jastreboff and Hazell [38]. Finally, we clinically assessed the presence or absence of the advent of the phenomena of associative learning – conscious and unconscious – regarding the presence of adverse events temporally correlated with tinnitus, such as particular negative circumstances (e.g., the state of health of the patient and his or her family, unpleasant workplace conditions, etc.), physical variations in the characteristics of tinnitus that had previously been well tolerated, negative advice offered by physicians and the media, and assumptions, considerations, personal convictions and ideas related to tinnitus. The results were evaluated after 18 months, comparing our results with the criteria indicated for suspending the therapy [39]; the subjects were considered to have improvement if the score on the scale of symptoms was ≤2, associated with a grade 1 on the THI and an awareness value of the presence of tinnitus of ≤10% in wakefulness, without any interfering with regular activities. If these results were not attained within the established time frame, the therapy was considered a failure.
Results
During the period of the study, we treated 294 patients, of whom 168 (57.14%) were in category 1, 78 (26.53%) in category 2, 36 (12.24%) in category 3, 6 (2.04%) in category 0, and 6 (2.04%) in category 4 T (tinnitus). No subjects from category 4 H (hyperacusis) were treated.
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Table 1. TRT results on the basis of the patients’ categories described by Jastreboff and Hazell [37] and the presence or absence of
triggering factors (see text for explanations) Categories
Total 0 1 2 3 4T 4H
Total patients
Patients with improvement
Patients without improvement
With event total
improved
Without event
294 (100%) 6 (2.04%) 168 (57.14%) 78 (26.53%) 36 (12.24%) 6 (2.04%) –
231 (78.57%) 6 (100%) 151 (89.88%) 46 (58.97%) 28 (77.77) 0 (0%) –
63 (21.42%) 0 (0%) 17 (10.11%) 32 (41.02%) 8 (22.22%) 6 (100%) –
189 (64.28%) 6 (3.17%) 115 (60.84%) 34 (17.98%) 28 (14.81%) 6 (3.17%) –
172 (91%) 17 (8.99%) 6 (100%) 0 (0%) 109 (94.78%) 6 (5.21%) 34 (100%) 0 (0%) 23 (82.14%) 5 (17.85%) 0 (0%) 6 (100%) – –
not improved
total
improved
not improved
105 (35.71%) – 53 (50.47%) 44 (41.9%) 8 (7.61%) – –
59 (56.19%) – 42 (79.24%) 12 (27.27%) 5 (62.5%) – –
46 (43.8%) – 11 (20.75%) 32 (72.72%) 3 (37.5%) – –
Applying the described criteria, we observed recovery in 231 patients (78.57%) divided up as follows: 151 in category 1 (89.88%), 46 in category 2 (58.97%), 28 in category 3 (77.77%), and 6 in category 0 (100%). None of the 6 subjects in category 4 T improved (table 1). The 63 patients (21.42%) who did not improve were divided up as follows: 17 in category 1 (10.11%), 32 in category 2 (41.02%), 8 in category 3 (22.22%), 6 in category 4 T (100%), and none in category 0, as all of them improved (table 1). The study of the presence or absence of a triggering factor showed that it was present in 189 patients (64.28% of the total) and absent in 105 patients (35.71% of the total). Subjects with a negative identified associated event were distributed as follows: 115 (60.84% of the total with an event) were in category 1, 34 (17.98%) in category 2, 28 (14.81%) in category 3, 6 (3.17%) in category 0, and 6 (3.17%) in category 4 T. Of the subjects from this group, 172 (91%) improved. The subdivision of therapeutic success per category is 109 (94.78% of the group with an event) in category 1, 34 (100%) in category 2, 23 (82.14%) in category 3, and 6 (100%) in category 0. None of those in category 4 T improved. In the group with an identified event, 17 (8.99%) did not improve, of whom 6 (5.21%) were in category 1, 5 (17.85%) in category 3, 6 (100%) in category 4 T, and none in either category 0 or 2, as they had already shown improvement. Of the 105 subjects (35.71%) without an identified triggering factor, 53 (50.47%) were in category 1, 44 (41.9%) in category 2, 8 (7.61%) in category 3, and none in categories 0 and 4 T. In this group, 59 patients (56.19% of those without a known triggering factor) improved, and they were distributed as follows: 42 (79.24%) in category 1, 12 (27.27%) in category 2, and 5 (62.5%) in category 3; the other categories were not represented in this group. Lastly, the patients without a known negative event who showed no improvement totalled 46 (43.8% of those without a known triggering factor), of whom 11 (20.75%) were in category 1, 32 (72.72%) in category 2, and 3 (37.5%) in category 3; the other categories were not represented in this group. Discussion and Conclusions
The results of our study show an improvement rate following treatment in line with those reported in the literature, which average around 80% [40, 41] (table 1). All the patients from category 0, defined as being less serious and/or with recent onset of the pathology, improved. The worst results, where no patient improved, were observed in the category with incapacitating tinnitus accentuated by exposure to noise (4 T). Both of the aforesaid categories are composed of only a few individuals, totalling around 4.1% of the cases, and they are thus of little significance in terms of the entire population that was examined. Most of the treated patients – more than half of the total (57.14%) – were represented by subjects in whom the main symptom was tinnitus (category 1). In this category we observed a higher improvement
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rate, approximately 90%, second only to category 0. In patients with hyperacusis (category 3: 12.24% of the total), the rate of improvement (approximately 78%) was comparable to that of the total. The second-worst results – after the patients from category 4 T and in agreement with previous works [42] – were noted in subjects with hypoacusis and tinnitus (category 2: 26.53% of the total), among whom approximately only 59% of the cases improved because full TRT was not implemented [42] (table 1). The breakdown of the case study into 2 subgroups, based on the presence or absence of the triggering factor – conscious or otherwise – associated with tinnitus, has allowed us to make several interesting observations. The patients’ medical histories were drawn up carefully and over a long period of time, not only in the initial meetings but also over the months of treatment, and so an empathetic rapport had been established with the patients. Nevertheless, in 35.71% of the subjects, we did not observe the presence of any triggering factor associated with tinnitus, which led us to surmise that in this population of patients the reactions of the limbic and autonomic nervous system provide negative reinforcement [31], eliciting the conditioned response. Separate analysis of the 2 subgroups shows a statistically significant difference in improvement rate (χ2 = 46.547; p = 0.000) between the group with an identified triggering factor compared to the one without identified triggering factors, with a preponderance of the former with a 91% improvement rate versus approximately 56% for the latter (table 1). A further subdivision by category of the 2 subgroups shows that there is a statistically significant difference in the improvement rate (χ2 = 38.977; p = 0.000) among hypoacusis patients with tinnitus (category 2), in which, in the presence of a known triggering factor, all the patients improved, whereas in the subgroup of subjects without an identified triggering factor there was a low improvement rate (approximately 28%) (table 1). The fact that subjects with both hearing loss and tinnitus (category 2) demonstrate worse therapeutic results has already been reported in the literature [42], and various reasons have been cited. First of all, the cause was sought in the extent of the hearing loss, which was greater in the subjects who did not improve, although statistical analysis did not corroborate this [42]. Second, one of the causes given for unsuccessful therapy was the failure to use a hearing aid, which is essential in this category, given that 80% of the patients who used them improved versus 47.8% of patients with hypoacusis who improved without them [42]. The mechanism responsible for these results, which must nevertheless be viewed critically due to the small number of subjects studied [42], may be explainable with the persistence of a high signal-to-noise ratio in patients without hearing aids and thus the low rate of the effectiveness of sound therapy aimed at inducing habituation for tinnitus perception and eliminating the conditioned reflex. In fact, the appropriate fitting of hearing aids constitutes important remediation for patients who suffer from tinnitus and hearing loss simultaneously. The difficulty in counselling, responsible for habituation to the reaction, can be considered a cause for failure, as these patients rarely manage to achieve the ‘reclassification’ and ‘demystification’ of the memorized tinnitus, defining its presence as innocent and not the cause of hypoacusis, because it is difficult to overcome their conviction that ‘I would hear well if I didn’t have tinnitus’. These results point out that if TRT is not used properly, then results will be worse. In category 1 as well, we noted statistically significant differences in favour of a higher improvement rate in the subgroup in which we identified the presence of the triggering factor in contrast to subjects without an associated event (χ2 = 7.977; p = 0.005). Instead, there were no statistically significant differences between the 2 subgroups in which hyperacusis represented the main problem (category 3) (χ2 = 0.485; p = 0.486). The tinnitus-related pathology arises following phenomena of associative learning, conscious or unconscious. It also arises in all cases of bothersome tinnitus where a triggering factor is not identified; in these cases the only element responsible for the patient’s distress
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is tinnitus, which may simply be annoying because reactions of the limbic and autonomic nervous system give negative reinforcement [31]. We must theorize which mechanisms are responsible for therapeutic failure in subjects in whom the pathology stems from triggering factors. This aspect was particularly evident in category 2, in which none of the patients without known triggering factors improved, but was also present to a significant level in category 1. Moreover, this trend was not confirmed in patients with hyperacusis (category 3), in whom we did not find any statistically significant differences among the results of the 2 subgroups. The approach used to treat all our patients (TRT) uses counselling to arrive at habituation to the reaction by no longer activating the limbic system and autonomic nervous system and, through sound therapy, to habituate the patient to the perception that blocks the arrival of the tinnitus signal at the superior cortical areas responsible for the awareness of its presence. Although it is a slow process, it can gradually be established automatically once habituation to the reaction has been achieved. Habituation is a non-associative learning process that tends to reduce the emotional and behavioural manifestations elicited by tinnitus. Presentation of the conditioned stimulus is required in order to extinguish the conditioned reflex, because habituation can only arise if tinnitus is detected [43, 44]. Habituation, extinction of the orientation reflex and extinction of the conditioned reflex are different terms that essentially refer to the same phenomenon [45]. The rehabilitation therapy for subjects with a tinnitus-related pathology due to the presence of a conditioned reflex helps convert an associative learning process into non-associative habituation. The tinnitus-related pathology is caused by the negative consequences of associative learning with or without identified triggering factors. In the latter, where the ongoing presentation of tinnitus – a stimulus that is annoying in itself regardless of its absolute or relative intensity – is enough on its own to trigger and sustain adverse emotional reactions of the limbic and autonomic nervous system [31], we registered the worst treatment outcome. In category 1, one of the 3 main categories we treated, the therapy was not as effective in subjects in whom we were unable to identify an associated event. The same thing happened in category 2, where the negative results can also be due to factors other than an unidentified triggering factor, such as non-implemented amplification [42]. In patients in whom the prevalent symptom was hyperacusis (category 3), the therapeutic objective was to desensitize the auditory system by systematically exposing the subjects to different sounds, exploiting underlying physiological processes that do not involve the conditioned reflex and conscious thought [46]. To a varying extent, hyperacusis may also be associated with misophonia and the two phenomena are not clearly distinguishable in the same patient [47]. Misophonia is characterized by a negative reaction to a sound with a specific pattern and meaning to a given patient. The physical characteristic of a sound is secondary. Reactions to the sound depend on the patient’s past history and on non-auditory factors like the patient’s previous evaluation of the sound, his or her psychological profile, and the context in which the sound is presented [48]. In misophonia, a condition in which external sounds and noises are disturbing because they are associated with a negative meaning, the therapy is based on associating them with something pleasant in order to arrive at an active extinction of the conditioned reflex [46]. The use of sound generators with the initial sound levels determined by the patient’s annoyance level represents a desensitizing approach that follows the modes used to treat other pathological conditions [49]; these initial sound levels were gradually increased but always kept below the sound level that evokes annoyance used in the therapy of hyperacusis [50]. The treatment of hyperacusis thus requires a completely different approach than the one used for tinnitus and misophonia. Therefore, in the patients in category 3 in whom hyperacusis and misophonia can variably be associated, the therapy that is used is oriented towards active extinction of the conditioned reflex and desensitization
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to external sounds. Category 3 is the only one in which the goal of the therapy is to desensitize the auditory system by systematic exposure to a variety of sounds and to associate those sounds with something positive to reverse the conditioned reflex [46]. In conclusion, the tinnitus-related pathology linked to classic conditioning benefits from rehabilitative therapy in a high percentage of cases in line with those reported in the literature, but our inability to identify factors triggering bothersome tinnitus negatively affects the treatment outcome in the 3 subgroups without a negative event in the main categories. The simplest explanation of this result could be that identifying such factors would positively influence the effectiveness of counselling in the subgroups of patients with a negative event, which would in turn affect the treatment outcome. Identifying a factor providing the negative reinforcement is helpful and can be done effectively but should not be crucial for the treatment in the TRT. Our results could indicate that counselling was not aimed at subgroups without a correlated event and should thus be modified to decrease the need for identifying a specific factor linked to the emergence of bothersome tinnitus, shifting the focus toward mechanisms involved in generating the tinnitus signal, and they point out that it is correct to disregard which factor was involved in creating functional links between the auditory and the limbic and the autonomic nervous systems. Our experience indicates that the good results achieved with TRT in patients with debilitating tinnitus can be improved further by adapting counselling in subgroups without a correlated event and by completing therapy with the use of hearing aids when indicated.
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ORL 2014;76:81–88 DOI: 10.1159/000360994
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