Central Annals of Otolaryngology and Rhinology

Cite this article: Eibenstein A, De Luca M, Fioretti AB, Varakliotis T, Cisternino S, et al. (2015) Long Term Effects of L’Aquila Earthquake on Tinnitus. Ann Otolaryngol Rhinol 2(10): 1063.

*Corresponding authorTheodoros Varakliotis, Department of Applied Clinical Sciences and Biotechnology, L’Aquila University, Via Vetoio (Coppito 2), 67100 Coppito (AQ), Italy, Tel: 39-340-373-3263; Email:

Submitted: 24 August 2015

Accepted: 14 September 2015

Published: 15 September 2015

ISSN: 2379-948X

Copyright© 2015 Varakliotis et al.

OPEN ACCESS

Keywords•Tinnitus•Hyperacusis•Sleep disorders•Stress•Earthquake

Research Article

Long Term Effects of L’Aquila Earthquake on TinnitusAlberto Eibenstein, Matteo De Luca, Alessandra Barbara Fioretti, Theodoros Varakliotis*, Sara Cisternino, Luisa Crosta and Maria LaurielloDepartment of Applied Clinical Sciences and Biotechnology, L’Aquila University, Italy

Abstract

Aim: The aim of this study was to deeply investigate the relationship between tinnitus, hyperacusis, sleep disorders and perceived stress levels in a study group of patients with tinnitus exposed to a traumatic event (earth quake) and a control group of patients with tinnitus not exposed to a traumatic event.

Methods: We studied 83 patients with tinnitus. The study group was composed by 47 patients exposed to earthquake. The control group was composed by 36 patients not exposed to the earthquake. Each patient was studied with clinical history, ENT examination and audiological tests. The following questionnaires were carried out: Tinnitus Sample Case History (TSCH), Tinnitus Handicap Inventory (THI), Pittsburgh Sleep Quality Index (PSQI), Khalfa’s questionnaire and Brief Symptom Inventory (BSI 53).

Results: The psychological screening used in the study need to have confirmation of further more specific investigations to evaluate the possible correlation between PTSD and tinnitus. It is possible that the exposure to a traumatic event, such as the earthquake, may have had an influence in the genesis of tinnitus. Analysis of the study group has revealed higher scores in the PSQI test and in the BSI test components of anxiety, somatization and depression.

Conclusion: The connection between psychopathology, tinnitus and treatment is complex and, perhaps not sufficiently investigated with adequate methodologies. Psychiatric comorbidity in subjects affected by tinnitus is frequent, even if this study showed that the relationship between psychopathology and tinnitus is not linear.

INTRODUCTIONTinnitus is commonly known as a complex of annoying

ringing, buzzing or hissing in the ears. The prevalence of tinnitus ranges from 10 to 20% [1-4] it can be persistent, intermittent or throbbing. Many hypotheses have tried to explain the origin of tinnitus even if none has yet been proven. Tinnitus may be a consequence of modified neural activity in the central auditory system due to a peripheral damage in the auditory structures [5]. The pathophysiological mechanism may be a thalamo-cortical dysrhythmia with a consequent decreased auditory stimulation and surrounding brain area hyperactivity inducing a topographical reorganization [6]. Central theories suggest an increased spontaneous activity associated with tinnitus in the dorsal cochlear nucleus [7] and the inferior colliculus of the brainstem [8,9].

Hypersensitivity to sound is a common description of distinct nosological phenomena of peripheral and central hearing disorders. Recruitment accompanying neurosensorial hearing

loss is distinguished from hyperacusis and from phonophobia; the latter defined as an anxious sensitivity towards specific sounds largely independent of their intensity. While recruitment can be described as a peripheral effect caused by a lack of outer hair cell moderation, hyperacusis and phonophobia represent disturbances of central auditory processing without peripheral pathology, often combined with psychosomatic reactions. Several studies have reported high hyperacusis scores for tinnitus patients [10-13]. An increase of central gain would amplify spontaneous and stimulus-induced activity which leads to tinnitus and hyperacusis respectively. Tinnitus may be also associated with sleep disorders [14], changes in quality of life and substantial modifications of behaviour, including anxiety, irritability and depression [15].

Many studies showed that up to 77% of tinnitus sufferers might have psychiatric comorbidities [16-18]. The outcomes of these studies also demonstrated that subjects with tinnitus show a lifetime prevalence of depression significantly higher than the general population [19-21].

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individual items generate seven “components”. The sum of scores for these seven components yields one global score. A PSQI score higher than 5 yielded a diagnostic sensitivity of 89.6% and specificity of 86.5% (kappa = 0.75, p less than 0.001) in distinguishing good and poor sleepers. The clinometric and clinical properties of the PSQI suggest its utility both in psychiatric clinical practice and research activities [24]. The PSQI differentiates “poor” from “good” sleep by measuring seven domains: subjective sleep quality, sleep latency, sleep duration, habitual sleep efficiency, sleep disturbances, use of sleep medication, and day time dysfunction over the last month.

BSI evaluates psychological distress and psychiatric disorders. The test can be used for areas such as patient progress, treatment measurements, and psychological assessment [25]. The test is a 53-item self-report scale that uses the 5 points Likert scale. The BSI-53 is an easily administered, objective, and accurate tool useful in identifying psychopathology in patients thought to have psychogenic dizziness. It is recommended as a valuable addition to the battery of tests performed when evaluating the dizzy patient [26, 20]. The score reflects the 9 primary symptom dimensions (somatization, obsessive-compulsive, interpersonal sensitivity, depression, anxiety, hostility, phobic anxiety, paranoid ideation and psychoticism) of the 90-item Symptom Checklist - Revised (SCL-90-R) and is designed to assess the psychological status of psychiatric and medical patients.

According to inclusion criteria, 83 consecutive patients with tinnitus were enrolled. A descriptive statistical analysis was conducted of the variables considered. The Wilcoxon rank sum test was used to evaluate the difference between the study group patients and the control group patients. The Spearman correlation was used to estimate the association between age, gender, tinnitus onset, THI scores, Khalfa’s questionnaire scores, PSQI scores and BSI scores for both groups. All statistical analyses were performed using SAS software (version 9.2, 2002-2008; SAS Institute, Inc., Cary, NC).

RESULTS AND DISCUSSIONThe age and mean questionnaires scores of the 83 patients

(55 males, 28 females) of the study are shown in Table 1. A statistical significance for tinnitus familiarity was pointed out. In the study group (L’Aquila), the familiarity for tinnitus was present in 11 patients (23,40%), while in the control group was present in 10 patients (27,78%) (p=0.049). The different duration from tinnitus onset between the two groups was statistically significant. In 36 patients (76,59%) of the study group, the onset was after the earthquake (i.e. the tinnitus occurred in the last 5 years), in the control group only in 16 (44,44%) patients the onset of tinnitus has been in the last 5 years (p=0.471). As regards the mode of tinnitus onset, in the study group 28 patients (59,57%) reported a suddenly onset, while in the control group a suddenly onset occurred only in 8 patients (22,22%) (p=0.0008). Tinnitus was present in the left ear in 8 patients (22,22%) of the control group, and in none of the patients in the study group (p=0.0052). Tinnitus was bilateral in 28 patients (59,57%) of the study group and in 8 patients (22,22%) of the control group (p = 0.0018). Continuous (non pulsatile) tinnitus was present in 60 of 83 patients (72,2%), in 32 patients of the study group (68,08%) and in 28 patients of the control group (77.7%). 23 patients

The aim of the present study was to evaluate patients with tinnitus giving them a series of validated questionnaires in order to better characterize the disorder and the level of disability. We wanted to analyze possible differences between a group of patients with tinnitus exposed to a traumatic event (earthquake) and a group of patients with tinnitus not exposed to the trauma. The use of specific questionnaires, as reported in the literature, allowed us to investigate the close correlation between tinnitus, hyperacusis, reduced sleep quality and psychological/mood disorders. The analysis focused on a study-group exposed to the earthquake on April, 6th 2009 and a control group not exposed to the earthquake. Exclusion criteria were organic diseases of the ear, psychiatric disorders and/or psychiatric treatment.

MATERIALS AND METHODSWe studied 83 patients with tinnitus (55 males, 28 females,

average age 57.61). The study group was composed of 47 patients exposed to the earthquake of April, 6th 2009, recruited at the ENT department of San Salvatore Hospital of L’Aquila. The control group was composed of 36 patients not exposed to the earthquake, recruited at the ENT department of European Hospital in Rome. Each patient was studied by clinical history, ENT examination, pure tone audiometry and tympanometry. Pitch and loudness of tinnitus, Minimum Masking Level (MML) and Loudness Discomfort Level (LDL) were used as specific tests to evaluate tinnitus and hyperacusis. Informed consent was obtained from each patient.

The following questionnaires were carried out: Tinnitus Sample Case History (TSCH), Tinnitus Handicap Inventory (THI), Pittsburgh Sleep Quality Index (PSQI), Khalfa’s questionnaire and Brief Symptom Inventory (BSI 53).

TSCH is a standardized questionnaire with items on background (age, gender, family history of tinnitus), tinnitus history (initial onset, associated events, pattern, site, loudness, pitch, percentage of awake time aware of tinnitus, previous tinnitus treatments, modifying influences, hyperacusis, alteration by movements, effect of nocturnal sleep, effect of stress, effect of medications) and related conditions (hearing impairment, noise annoyance, headaches, vertigo/dizziness, mandibular joint disorder, neck pain, psychiatric problems) [14]. THI is a self- administered questionnaire to evaluate the impact of tinnitus on the quality of life. THI is a 25-items questionnaire and the questions are divided into 3 subgroups: functional, emotional and psychological. Eleven items are included in the functional scale, 9 in the emotional scale and 5 in the psychological scale. Mc Combe et al. [22] proposed a grading of the disorder based on the scores of the THI questionnaire: grade 1 - very slight tinnitus - (THI score 0-16), grade 2 - mild tinnitus - (THI score 18-36), grade 3 - moderate tinnitus - (THI score 38-56), grade 4 - severe tinnitus - (THI score 58-76), grade 5 - catastrophic tinnitus - (THI 78-100).

Khalfa’s Hyperacusis Questionnaire is a tool suitable to quantify and evaluate the impact of hyperacusis on the quality of life. The score greater than 28 seems is indicative of a strong auditory hypersensitivity [23].

PSQI is a self-rated questionnaire that assesses sleep quality and disturbances over a 1-month time interval. Nineteen

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had intermittent tinnitus trend (27,7%), of those 15 where in the study group (31,91%) and 8 in the control group (22,22%). Finally, pulsatile tinnitus affected only 6 patients (7,2%), 1 patient of L’Aquila group (2,1%) and 5 patients of the control group (13,8%). For what concerns the impedenzometry all the patients had a bilateral type a tympanogram and normal reflexes.

The influence of nocturnal sleep on tinnitus based on TSCH was significant in 13 patients (36,11%) of the control group and in 7 patients (14,89%) of the study group (p=0.0376). The physical discomfort caused by sounds was more frequently absent in the study group (17 patients) than in the control group (4 patients) (p=0.0198).

As regards to dizziness, in the study group 28 patients (59,57%) reported to be affected, but only 10 patients (27,78%) reported it in the control group (p=0.0072). In the study group 28 patients (59,57%) reported other pain syndromes, while in the control group these were reported only in 11 patients (30,55%) (p=0.0256).

Regarding the Khalfa’s hyperacusis questionnaire scores we found higher statistically significant scores in the control group (p<0.05).

PSQI was positive (score>5) in 35 patients of the study group (74,47%) and in 8 patients (22,22%) of the control group (p=0.0062). The average score of the PSQI test was higher in the study group than in the control group (p<0.05). The domains of PSQI more compromised in the study group were sleep latency, sleep duration, sleep efficiency and sleep disorders (p<0.05).

Regarding the BSI-53 scores, because of poor compliance by patients of both groups, who had the opportunity to refuse to answer questions, it was possible to analyze only some domains of the test: anxiety, depression and somatization. Regarding the scores higher statistically significant scores were reported in the study group in all the three domains of anxiety (p<0.01), somatization (p<0.001) and depression (p<0.005).

Further statistical correlations between questionnaires scores were evaluated with the Spearman correlation (r) and are reported in Table 2. The THI and the Khalfa’s scores (r = 0.603) prove greatly in tune: a high score on the THI matched by an equally high score to Khalfa’s, confirming the close correlation between tinnitus and hyperacusis. We found a high correlation between the total score of the THI and Khalfa’s attentional component score (r=0.58417; p<0.0001) too. The high correlation between the functional component of the THI and the Khalfa’s attentional component score (r=0.61467; p<0.0001) is shown in the Figure 1.

We also found a high correlation between the PSQI and BSI-53 scores regarding “anxiety”, “depression” and “somatization” in the study group rather than in the control group (r=0.61155; p<0.0001). The higher statistically significant correlations between questionnaires scores are reported in Table 3.

The aim of this study was to investigate the relationship between tinnitus, hyperacusis, sleep disorders and perceived stress levels in a study group of patients with tinnitus exposed to a traumatic event (earthquake) and a control group of patients with tinnitus not exposed to a traumatic event.

A bilateral (p = 0.0018) and suddenly onset (p=0.0008) tinnitus was more frequently pointed out in the study group than in the control one. Dizziness (p=0.0072) and pain syndromes (p=0.0256) were more often reported in the study group.

The exposure to a traumatic event such as the earth quake, might influence the genesis of tinnitus, which could be considered

Figure 1 Correlation between THI attentional component score and Khalfa’s test attentional component score.

Table 1: Age and mean questionnaires scores of all 83 patients.

average median minimum maximum

Age 57,61 53 14 83

THI score 40,31 42 2 92

THI functional score 15,13 14 0 42

THI psycological score 9,31 9 0 20

THI emotional score 15,68 14 0 36

Hyperacusis score 14,28 14 0 39Hyperacusis attenctional score 3,46 3 0 12

Hyperacusis social score 5,48 5 0 18Hyperacusis emotional score 5,34 5 0 12

PSQI score 8,98 8 1 23PSQI subjective sleep quality 1,31 1 0 3

PSQI sleep latency 2,71 3 0 6

PSQI sleep duration 1,51 1 0 3

PSQI sleep efficiency 0,48 0 0 3

PSQI sleep disorders 1,48 1 0 3

PSQI meds to sleep 0,63 0 0 3

PSQI daily disfunction 0,89 1 0 3

BSI anxiety 8,57 7 0 23

BSI somatization 7,51 6 0 24

BSI depression 6,42 5 0 23Abbreviations: THI: Tinnitus Handicap Inventory, PSQI: Pittsburgh Sleep Quality Index, BSI: Brief Symptom Inventory

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Table 2: Mean scores of questionnaires in the study group and in the control group. Study GroupMean score

Control GroupMean score P

THI score 39,64 43,98 0,4141

THI functional score 13,68 17,09 0,1345

THI psycological score 9,57 8,91 0,7458

THI emotional score 15,23 16,29 0,5046

Hyperacusis score 13,72 15,03 0,0368

Hyperacusis attenctional score 3,15 3,89 0,0892

Hyperacusis social score 5,32 5,69 0,2413

Hyperacusis emotional score 5,26 5,46 0,6611

PSQI score 10,06 6,11 0,0316

PSQI subjective sleep quality 1,41 1,17 0,2214

PSQI sleep latency 3,17 2,08 0,0277

PSQI sleep duration 1,75 1,19 0,0218

PSQI sleep efficiency 0,62 0,28 0,0481

PSQI sleep disorders 1,61 1,31 0,0403

PSQI meds to sleep 0,77 0,46 0,2321

PSQI daily dysfunction 0,81 0,99 0,1551

BSI anxiety 10,36 6,41 0,0091

BSI somatization 9,83 4,61 0,0002

BSI depression 7,81 4,71 0,0459

Table 3: More statistically significant correlations between questionnaires scores.

r p

THI total score - hyperacusis attentional score 0,585 0,0001

THI attentional component score - hyperacusys attentional component score 0,615 0,0001

THI emotional component score - hyperacusys total score 0,534 0,0001

THI emotional component score - hyperacusys attentional component score 0,511 0,0001

THI total score - hyperacusis total score 0,585 0,0001

PSQI subjective sleep quality score - BSI depression score 0,515 0,0001

PSQI total score - BSI somatization score 0,541 0,0001

PSQI total score - BSI depression score 0,554 0,0001

PSQI total score - BSI anxiety score 0,515 0,0001

PSQI total score - BSI total score (sum of anxiety, somatization and depression scores) 0,612 0,0001

BSI total score (sum of anxiety, somatization and depression scores) - PSQI sleep latency score 0,511 0,0001

THI total score - BSI anxiety score 0,519 0,0001

THI emotional component score - BSI anxiety score 0,533 0,0001

Abbreviations: THI: Tinnitus Handicap Inventory, PSQI: Pittsburgh Sleep Quality Index, BSI: Brief Symptom Inventory.

as a stressor, as well as stress might be framed as a cause of tinnitus. In regard to the relationship with stress, many studies are focused on the role of tinnitus as a “stressor” [27] and other papers describe how some stressful events can be identified prior to the emergence of the tinnitus. A directly proportional relationship is identifiable between stress levels and intensity of perceived somatic distress [28]. Xu J et al. investigated the effects of negative events on patients with tinnitus, and demonstrated that negative life events may reduce the quality of life in tinnitus patients, suggesting to pay more attention to those events during

psychological counseling [29].

A poor quality of sleep and the increase of PTSD have been the outcomes of a paper (Ferrara M. 2009), whose preliminary analysis showed significantly higher scores in the group of L’Aquila patients after the earthquake [30]. Our study confirmed a poor quality and disturbances of sleep in the study group (p=0.0062) being sleep latency, sleep duration, sleep efficiency, and sleep disorders the more compromised PSQI domains (p<0.05). Hyperacusis and tinnitus have been suggested

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to result from an increased central gain [31-34] even when hearing loss is not detectable on the audiogram [35]. Regarding the Khalfa’s hyperacusis scores we found higher statistically significant scores in the control group (p<0.05) demonstrating that hyperacusis is not significantly associated with tinnitus in subjects exposed to a traumatic event. Regarding the THI total score and the 3 subscales score we found no statistically significant differences between the two groups (p>0.05).

The individual THI and Khalfa’s scores (r = 0.603) proved greatly in tune. We found a high correlation between the total score of the THI and Khalfa’s attentional component score (r=0.58417; p<0.0001) and between the functional component of the THI and the Khalfa’s attentional component score (r=0.61467; p<0.0001) too, confirming the close correlation between tinnitus and hyperacusis.

Epidemiologic studies showed that anxiety and depression exacerbated the discomfort engendered by tinnitus because patients developed a conditioned reflex of focusing on the tinnitus [36]. Belli et al showed that 27% of patients with tinnitus had at least one psychiatric diagnosis (anxiety disorders 28%, somatoform and mood disorders 15%, and personality disorders 3%), versus 5.6% of control subjects [37]. Anxious and depressive symptoms seem to be the most common complications of tinnitus [26, 38]. Folmer et al. showed that tinnitus patients with concomitant depression reported the same level of tinnitus loudness of patients without a history of depression, but they had higher ratings of tinnitus severity [39]. The same authors reported in a different paper that tinnitus severity was positively correlated with quantitative measures of anxiety and depression [40].

As far as BSI is concerned, the study group reported higher statistically significant scores in the domains of anxiety (p<0.01), somatization (p<0.001) and depression (p<0.005). The central processes, especially anxiety, exacerbate the discomfort and whether or not the tinnitus is a disturbing cause of further central auditory processing of the tinnitus “signal” and its psychological validation. The high correlation between the PSQI and BSI-53 scores regarding “anxiety”, “depression” and “somatization” in the study group (r=0.61155; p<0.0001) confirmed that perception of tinnitus can considerably change in relation to coping capabilities and high stress levels [41] and, on the other hand, abnormal physiological stress reactions might play a role in the onset, maintenance, and exacerbation of tinnitus symptoms [42,43] even in subjects exposed to a traumatic event. The relationship between tinnitus and stress is due to the connection between inner ear sensitivity and neuroendocrinological modulation linked to stress activation [42]. The role of psychosomatic and stress reactions in the perception of tinnitus is corroborated by the neurophysiological model proposed by Jastreboff and Hazell [44]. According to this model tinnitus becomes chronic and decompensated as a consequence of malfunction of the neural network that involves sensory, limbic and autonomic components [28]. Dysfunctions of the same neural network have been described in subjects affected by emotional and anxiety disorders [45] and it is known from animal studies that psychopharmacological treatment produces a “normalization effect” on the functionality of these areas [46].

CONCLUSIONOur results pointed out that the exposure to a traumatic

event such as an earthquake was able to influence the genesis, the duration and the severity of tinnitus.

Our study revealed higher scores in the BSI domains of anxiety, somatization and depression in the study group. So even if the connection between psychopathology and tinnitus is not linear, our study pointed out that the predisposition to neurotic disorders and the lack of coping capabilities may play a critical role in the clinical history of patients affected by severe post-traumatic tinnitus.

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