Otolaryngology–Head and Neck Surgery (2008) 139, 391-394
ORIGINAL RESEARCH—OTOLOGY AND NEUROTOLOGY
Tinnitus aurium in persons with normal hearing: 55 years later Luca Del Bo, MSc, Stella Forti, BMath, Umberto Ambrosetti, MD, Serena Costanzo, Davide Mauro, BSc, Gregorio Ugazio, MD, Berthold Langguth, MD, and Antonio Mancuso, MSc, Milan, Italy; and Regensburg, Germany OBJECTIVE: The aim of this study was to investigate the effect of silence on the appearance of auditory phantom perceptions in normal-hearing adults, with specific emphasis on the influence of suggestion. STUDY DESIGN: Cross-sectional survey. SUBJECTS AND METHODS: Fifty-three normal-hearing young Caucasian adults were subjected to two 4-minute sessions in an anechoic sound chamber. In the first session the chamber was empty; in the second session the chamber contained a nonfunctioning loudspeaker. At the end of each session, subjects had to indicate which sounds they perceived from a list of 23 different sounds. RESULTS: When the loudspeaker was not present, 83 percent of the participants reported that they experienced at least one sound, and the percentage increased to 92 percent when the loudspeaker was present. CONCLUSION: These results confirm the emergence of tinnituslike perceptions in a nonclinical population in a silent environment and indicate that suggestive mechanisms play only a minor role in their generation. © 2008 American Academy of Otolaryngology–Head and Neck Surgery Foundation. All rights reserved.
T
innitus and auditory hallucinations are the perceptions of sound in the absence of external sounds.1 Tinnitus is a very frequent phenomenon. It is estimated that in Western countries approximately one of eight persons experiences tinnitus.2,3 Tinnitus research has been strongly influenced by the work of Heller and Bergman in 1953.4 In this study, 80 subjects between 18 and 60 years of age with self-reported normal hearing entered a soundproof chamber with an ambient noise level between 15 dB and 18 dB for about 5 minutes. These subjects received instructions to take note of possible sounds heard in the soundproof chamber. Of the subjects, 93.75 percent reported having heard at least one sound (in reality, a tinnitus). On the basis of this observation, the concept that tinnitus is a normal physiological phenomenon in a silent environment developed. Further-
more, avoidance of silence and the use of sound-enriched environments became an important strategy for the treatment of tinnitus.5,6 Heller and Bergman’s experiments were repeated only recently.7-9 On the basis of epidemiological data suggesting an influence of race and gender on the prevalence of bothersome tinnitus in African Americans,10,11 Tucker et al7 focused on the effect of gender and race on the perception of tinnitus in silence. In this study, only 64 percent of the subjects reported the perception of sounds after sitting for 20 minutes in a soundproof room. Recently Knobel and Sanchez9 were able to show that attentional mechanisms have a strong impact on the perception of sounds in silence. When focusing their attention on the auditory system, 68.2 percent of participants experienced tinnitus, but when subjects were instructed to focus on the visual system, only 45.5 percent reported tinnitus, and this rate decreased to 19.7 percent during a cognitive task. These results clearly indicate an important influence of top-down mechanisms on the perception of phantom sounds. The purpose of our study was to repeat the classic Heller and Bergman experiment in an audiologically wellinvestigated sample, because, in 1953, audiological control examinations were not carried out and, therefore, slight hearing loss of the participants could not be ruled out as a confounding factor. Our further goals were to investigate the relationship between distortion product otoacoustic emission tests and the prevalence of phantom auditory perceptions in silence as well as the influence of suggestive factors. For the latter purpose, we investigated whether the prevalence of sound perception depended on the presence of a loudspeaker in the soundproof room.
METHODS Participants Fifty-three healthy young volunteers (39 male, 14 female, average age 22 years, ranging from 19 to 29 years) with
Received April 24, 2008; revised June 13, 2008; accepted June 13, 2008.
0194-5998/$34.00 © 2008 American Academy of Otolaryngology–Head and Neck Surgery Foundation. All rights reserved. doi:10.1016/j.otohns.2008.06.019
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normal hearing participated in the study. Subjects were recruited among students of the University of Milan. All participants gave written informed consent for the study. This study was approved by the Independent Ethics Committee of the Fondazione Ascolta e Vivi. All subjects were initially submitted to audiometric evaluation including pure tone audiometry (PTA; 250-16,000 Hz), impedancemetry, and high-definition distortion product otoacoustic emissions (DPOAEs; 15 points/octave). Normal hearing was defined as a PTA maximum threshold of 20 dB HL for frequencies between 250 and 16,000 Hz in both ears, and a type A tympanogram and contralateral stapedial reflex recordable at the threshold (90 dB). Exclusion criteria were abnormal or absent otoacoustic emissions, chronic tinnitus, strong acoustic input in the last 24 hours (discotheque, amplificatory activities, noisy recreation activities, etc), regular pharmacological treatment, and alcohol or drug abuse. These very restrictive criteria for normal hearing were chosen to exclude subliminal hearing disorders in the participants that could be present even with a normal audiogram. Relevant anamnestic data and information about acoustic habits were assessed by specific questionnaires.
Instrumentation Hearing sensitivity was assessed with an Orbiter 2922 (GN OTOMETRICS Madsen, Copenhagen, Denmark, version 2) audiometer together with a Madsen Electronics headset TDH-39 (ANSI 1996). For impedancemetry, Amplaid 720 equipment was used. DPOAEs were recorded with Scout Sport equipment from Bio-logic System Corp. The upper limit of the frequencies of the DPOAEs was 10 kHz with a range of 100 dB. The DP-Gram ranges were –30 to 70 dB and 250 to 16,000 Hz in conformity with the Vanderbilt 65/55, 95-5th percentile specifications. The parameters of the protocol for measuring the DPOAEs were beginning frequency of 500 Hz, ending frequency of 10,000 Hz, F2/F1 ratio 1.22, 15 points per octave, L1 level 65 dB, and L2 level 55 dB. Stopping criteria were minimum DP amplitude –10 dB, noise floor 17 dB, S/N ratio 6 dB, and point time limit 20 seconds. PTA and DPOAE were carried out in a silent cabin (background noise level 29 dBA) with a noise reduction coefficient of 20 dB.
Table 1 Experimental procedure Time (min)
Task
20 20 20 4 5 20 4 5
Quiet environment (sound level ⱕ 45 db(A)) Audiometric assessment (PTA, DPOAE) Quiet environment (sound level ⱕ 45 db(A)) Anechoic chamber Sound list assessment Quiet environment (sound level ⱕ 45 db(A)) Anechoic chamber with sound “expectation” Final sound list assessment
The listening sessions in the absence of ambient noise were carried out in anechoic sound chambers according to the ANSI S3.1 1977 Sound Chamber Ambient Noise and Qualification test: International Organization for Standardization 3745-1977, part 5 specification. Ambient noise of the sound-treated booth was measured with a Sinus GmbH data analyzer (model SoundBook 6034 Sinus Messtechnik GmbH, Leipzis Nordost, Germany), a Larson Davis sound level meter (model CAL200 series 4193 Larson Davis PCG Piezotronics div., Provo, Utah) and a Larson Davis microphone (model L&D 2541, series 7881). Ear-level measurements are reported in Figure 1.
Procedures The subjects were exposed to two 4-minute sessions in an anechoic sound chamber. The relatively short duration of 4 minutes was based on earlier studies demonstrating that auditory perceptions emerge in less than 4 minutes in the majority of participants.7 Both times participants received the instruction to listen for potential sounds (see Table 1 for detailed procedure). No information was given to the participants about what they might hear; however, they received a list of possible sounds before the experiment with the instruction to complete the assessment list at the end of the session. In the first session, the soundproof chamber was empty. In the second session, a fake loudspeaker was installed to further suggest the presence of sounds and to increase the expectation of hearing them. After the experiments, the participants were informed that no sounds were presented in the booth and that the experience of phantom sounds is a phenomenon without any pathological significance. This preventive counseling was performed to avoid the possibility that participants might obsessively focus on a phantom perception that previously escaped their attention and was made aware to them by the experiment.
Data Analysis
Figure 1 Sound level in anechoic sound chamber (1/3 octave, linear scale).
The homogeneity between the dichotomous responses (sound/no sound) in the two tests was analysed with the Fisher exact test, and Pearson 2 test was used to analyze the correlation between the number of reported sounds and
Del Bio et al
Tinnitus aurium in persons with normal hearing: . . .
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Table 2 Number of subjects hearing sounds and number of reported sounds
No. of subjects No. of reported sounds (mean ⫾ SD)
Empty soundproof room
Soundproof room with loudspeaker
P value
44 (83%) 2.17 (⫾1.684)
49 (92%) 2.58 (⫾1.646)
NS NS
NS, nonsignificant.
the mean values of the DPOAE amplitude level at every f2 primary frequency. The SAS statistical package, version 9.1 (SAS Institute, Cary, NC) was used for the analyses.
RESULTS In the empty soundproof room, 44 of 53 (83%) subjects perceived at least one sound, whereas 49 of 53 (92%) subjects reported sound perception in the presence of a fake loudspeaker (Table 2). In the empty soundproof room, the average number of sounds heard by each subject from the whole sample was 2.17 ⫾ 1.68 (minimum 0 sounds, maximum 6 sounds). In total, 21 types of sounds were perceived (plus the “other” category), of which the most common sounds perceived were a “buzz”, “hum”, and “acute sound.” With the presence of the loudspeaker, this average rose to 2.58 ⫾ 1.64 (minimum 0 sounds, maximum 7 sounds), with 20 categories perceived (plus the “other” category). The most common types of sounds did not change. Table 3 shows the ranking list of the sounds perceived. Three subjects never heard anything (in either situation), six subjects who did not hear anything in the empty soundproof room reported the perception of one to four sounds in the loudspeaker condition (two subjects reported one sound, one subject reported two sounds, and three subjects reported four sounds). Only one subject who reported a sound (buzz) in the empty soundproof room did not perceive any sound in the presence of the loudspeaker. Neither the differences in the portion of participants perceiving sounds (P ⫽ NS) nor in the number of sound perceived (P ⫽ NS) were statistically significant. There was no correlation between the number of perceived sounds and DPOAE average amplitudes (Pearson 2: 0.157; P ⫽ NS), nor did the number of reported sounds and the mean values of the DPOAE amplitude level at every f2 primary frequency result in any significant correlations.
DISCUSSION Our study demonstrates that a period of sustained silence combined with auditory attention leads a high percentage of normal listeners to experience tinnitus, thus further confirming the results of Heller and Bergman’s4 classic experiment.
To avoid subliminal hearing loss as a potential confounding factor, we chose very restrictive criteria for normal hearing. The observed incidence of sound perception under the two investigated conditions was 83 percent and 92 percent, respectively, only slightly lower than the 94 percent observed by Heller and Bergman in 1953. Because one of the main criticisms of Heller and Bergman’s study was that the hearing status of participants was not systematically investigated, our results now demonstrate that the incidence of sound perception is equally high in a thoroughly audiometrically tested population sample, further indicating that the occurrence of tinnitus in subjects with normal hearing under acoustic deprivation represents a very stable phenomenon. Additional support for the robustness of this phenomenon comes from the fact that the quality of sound reported in our sample was very similar to the results of Heller and
Table 3 Reported sounds under two conditions: in an empty anechoic chamber and in an anechoic chamber with a loudspeaker
Sound Buzz Hum Acute sound (chalk on the blackboard) Whir (personal computer fan) Sound of ocean waves Whistle Heartbeat Compressor Click Flowing water Cricket Cicada Pressure cooker Waterfall Bell Roar Deflating tire Frying Sandpaper Other*
Empty Soundproof soundproof room with room loudspeaker 16 15
17 19
10
12
9 9 6 5 5 5 5 4 3 3 3 2 2 2 1 1 9
5 8 8 6 8 5 9 11 5 2 3 0 1 0 5 6 9
*Contains every sound reported from only one subject.
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Bergman. Compared with two other recent studies,7-9 the incidence of tinnitus in our study was slightly higher. The lower rates reported by Tucker et al7 (64% of listeners overall) and by Knobel and Sanchez9 (68.2% overall) might be due to differences in age and race between the investigated samples. Our study was the first to investigate the relationship between amplitude of DPOAEs and the perception of tinnitus in silence. The lack of a correlation between DPOAEs suggests that the mechanisms involved in the generation of DPOAEs do not play a decisive role in the occurrence of tinnitus in silence. Interestingly, the presence of a loudspeaker in the soundproof chamber resulted in only a slight increase in the number of perceived sounds, a result that did not reach significance. This finding that suggestive mechanisms do not seem to play a major role in the phenomenon of sound perception in silence seemingly contrasts with the recent results of Knobel and Sanchez,9 who demonstrated the importance of attentional mechanisms. However, even if both anticipation and attention are higher-order mechanisms involved in the top-down regulation of sensorial perception, they represent neurobiologically different mechanisms. Thus, it might be conceivable that, even if attention deviation on other sensory systems or cognitive tasks results in reduction of tinnitus perception, anticipatory mechanisms do not increase the perception of sound in silence. We are also aware that the lack of an effect of suggestion in our study might be due to methodological limitations. It might be possible that the presence of the loudspeaker exerted only a weak influence on anticipation or that the relative low increase in sound perception was due to a ceiling effect. Another methodological limitation was that we did not control for order effects. However, the only other study in which subjects were tested repeatedly9 did not show any order effect. For clarification of these issues, additional studies are needed to investigate different attentional and suggestive influences in the same sample.
CONCLUSION In an empty anechoic chamber, a high percentage of participants reported the experience of sounds. The number of sounds perceived did not increase significantly with the presence of a loudspeaker as a suggestive factor. These results further confirm the emergence of tinnituslike perceptions in a nonclinical population in a silent environment and indicate that suggestive mechanisms play only a minor role in their generation.
ACKNOWLEDGEMENTS The anechoic sound chamber was offered by Faital S.p.a., and the phonometric measures were performed by Mr Ruggero Chiavallotti.
AUTHOR INFORMATION From the Fondazione Ascolta e Vivi (Drs Del Bo, Costanzo, and Ugazio); the Department of ORL and Ophthalmology (Dr Ambrosetti), and the Audiology Unit (Dr Forti), University of Milan, Fondazione IRCCS Ospedale Maggiore Policlinico, Mangiagalli and Regina Elena; the Department of Information Technology and Communication (Drs Ambrosetti, Mauro, and Mancuso), University of Milan; and the Department of Psychiatry, University of Regensburg (Dr Langguth), Germany. Corresponding author: Luca Del Bo, MSc, Fondazione Ascolta e Vivi, Via Foppa, 15 - 20144 Milan, Italy. E-mail address:
[email protected];
[email protected].
AUTHOR CONTRIBUTIONS Luca Del Bo: study design, supervision of experiments, interpretation of data, writing of the manuscript, final approval of the manuscript; Stella Forti: interpretation of data, statistics, writing of the manuscript, interpretation of data, final approval of the manuscript; Umberto Ambrosetti: audiological visits, phonological measurements, writing of the manuscript, interpretation of data, final approval of the manuscript; Serena Costanzo: audiological examinations, interpretation of data, final approval of the manuscript; Davide Mauro: experiments, interpretation of data, final approval of the manuscript; Gregorio Ugazio: audiological visits, interpretation of data, final approval of the manuscript; Berthold Langguth: study design, interpretation of data, writing of the manuscript, final approval of the manuscript; Antonio Mancuso: study design, supervision of experiments, interpretation of data, final approval of the manuscript.
FINANCIAL DISCLOSURE None.
REFERENCES 1. Moller AR. Tinnitus: presence and future. Prog Brain Res 2007;166: 3–16. 2. Seidman MD, Jacobson GP. Update on tinnitus. Otolaryngol Clin North Am 1996;29:455– 65. 3. Humes LE, Joellenbeck LM, Durch JS. Noise and military service: implications for hearing loss and tinnitus.Washington: National Academies Press; 2006:320. 4. Heller MF, Bergman M. Tinnitus aurium in normally hearing persons. Ann Otol Rhinol Laryngol 1953;62:73– 83. 5. Jastreboff MM. Sound therapies for tinnitus management. Prog Brain Res 2007;166:435– 40. 6. Tyler RS, Gogel SA, Gehringer AK. Tinnitus activities treatment. Prog Brain Res 2007;166:425–34. 7. Tucker DA, Phillips SL, Ruth RA, et al. The effect of silence on tinnitus perception. Otolaryngol Head Neck Surg 2005;132:20 – 4. 8. Sanchez TG, Medeiros IR, Levy CP, et al. Tinnitus in normally hearing patients: clinical aspects and repercussions. Rev Bras Otorrinolaringol (English edition) 2005;71:427–31. 9. Knobel KA, Sanchez TG. Influence of silence and attention on tinnitus perception. Otolaryngol Head Neck Surg 2008;138:18 –22. 10. Cooper JCJ. Health and Nutrition Survey of 1971–75, part ii: tinnitus, subjective hearing loss and well being. JAAA 1994;5:37– 43. 11. Hoffman HJ, Reed GW. Epidemiology of tinnitus. In: Snow JB, editor. Tinnitus: theory and management. London: BC Decker; 2004. p. 16 – 41.