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842577

review-article2019
AORXXX10.1177/0003489419842577Annals of Otology, Rhinology & LaryngologyOmidvar and Jafari

Review Article
Annals of Otology, Rhinology & Laryngology

Association Between Tinnitus and


1­–14
© The Author(s) 2019
Article reuse guidelines:
Temporomandibular Disorders: A sagepub.com/journals-permissions
DOI: 10.1177/0003489419842577
https://doi.org/10.1177/0003489419842577

Systematic Review and Meta-Analysis journals.sagepub.com/home/aor

Shaghayegh Omidvar, PhD1,2 and Zahra Jafari, PhD3

Abstract
Objectives: Tinnitus is one of the most common otological symptoms in patients with temporomandibular disorders.
This study aimed to investigate the possible association between tinnitus and temporomandibular disorders.
Methods: The online databases of PubMed, Ovid, ScienceDirect, and Web of Science were explored for all English articles
published until September 2018 using the combined keywords tinnitus and temporomandibular. Cross-sectional, cohort, or
case-control studies that investigated the association between tinnitus and temporomandibular disorders (TMDs) were
considered. The quality of the included papers was assessed by the Crowe Critical Appraisal Tool.
Results: Twenty-two papers met the eligibility criteria and were included in the systematic review. Meta-analysis was
performed on 8 papers to investigate the possible relationship between tinnitus and TMDs by calculating the odds ratios.
Odds ratios ranged from 1.78 to 7.79 in the studies related to tinnitus frequency in temporomandibular disorders and from
1.80 to 7.79 in the papers linked to temporomandibular disorder frequency in tinnitus, indicating a significant association
between tinnitus and temporomandibular disorders.
Conclusions: There was a strong relationship between tinnitus occurrence and TMDs. The findings implied the significance
of exploring the signs of TMDs in patients with tinnitus as well as tinnitus in those who complain from temporomandibular
disorders.

Keywords
tinnitus, temporomandibular disorder, hearing loss, systematic review, meta-analysis

Introduction related structures.7 All of these disorders share a group of


symptoms, including (a) ear symptoms such as hearing loss,
Tinnitus is a phantom auditory experience in the absence of otalgia, tinnitus, and vertigo8; (b) pain, originated from
external auditory stimuli.1 It is estimated that 10% to 15% of either macular or articular conditions,9 in the form of head-
the adult population suffers from tinnitus.2,3 In addition to ache about the vertex, occiput, and behind the ears, and a
the auditory system that is commonly associated with this burning sensation in throat, tongue, and side of the nose8; (c)
phantom auditory perception,4 the somatosensory system miscellaneous symptoms such as dryness of the mouth, her-
also appears to contribute to tinnitus resulting from the pes of the external ear canal, buccal mucosa8; and limited
somatosensory-auditory interactions in the central nervous mouth opening.10
system.5 The somatic involvement of the structures outside Approximately 60% to 70% of the general population
of the ear, for example, the temporomandibular joint (TMJ) suffers from at least 1 symptom of TMDs; however, 1 out of
and masculatory muscles, may also interfere in tinnitus 4 of these individuals is aware of the signs and reports them.
(somatic tinnitus) perception.5 Various cranial nerves,
including the trigeminal (V), facial (VII), glossopharyngeal
(IX), vagus (X), and autonomic nerves, innervate the ear. 1
Department of Audiology, School of Rehabilitation Sciences, Shiraz
The TMJ is likewise innervated by cranial nerves V and VII University of Medical Sciences, Shiraz, Fars, Iran
2
with communicating branches like the chorda tympani, Rehabilitation Sciences Research Center, Shiraz University of Medical
Sciences, Shiraz, Fars, Iran
which are close to the ear structures. Due to the common 3
Department of Neuroscience, Canadian Center for Behavioral
cranial nerves between the ear and TMJ, ear difficulties like Neuroscience (CCBN), University of Lethbridge, Lethbridge, AB, Canada
tinnitus, otalgia, and vertigo have been postulated to be con-
Corresponding Author:
nected to temporomandibular disorders (TMDs).6 TMDs is a Zahra Jafari, PhD, Department of Basic Sciences in Rehabilitation, School of
collective term used to demonstrate a number of associated Rehabilitation Sciences, Iran University of Medical Sciences, Tehran, Iran.
disorders involving the TMJ, masticulatory muscles, and Emails: jafari.z@iums.ac.ir, zahra.jafari@uleth.ca
2 Annals of Otology, Rhinology & Laryngology 00(0)

Approximately 5% of individuals with 1 or more TMD criteria for TMDs were applied: (1) the research diagnostic
symptoms also seek for treatment.10 criteria for temporomandibular joint disorder (RDC/
Although tinnitus and TMDs are 2 common complaints TMD),20 (2) the revised versions of the RDC/TMD,21,22 and
in every society, the incidence of each one in patients with (3) complain of TMJ noise (like clicking), mouth opening
the other complaint does not necessarily suggest a causal limitation, or both that were evaluated by asking questions
relation. Tinnitus has been shown to be more frequent in and/or clinical examinations.
individuals with TMDs (36.6%) compared to the controls RDC/TMD incorporates 2 axes. Axis I demonstrates
(4.4%).11 Patients with tinnitus also display a significantly the clinical condition, and Axis II includes the psycho-
higher frequency of TMDs (85%) compared with the indi- social status and pain-related disability given the bio-
viduals without tinnitus (55%).12 In 1934, Costen described psychosocial model of chronic pain.20 Axis I diagnoses
the relationship between otologic symptoms and TMDs and are based on the following diagnostic groups: group I
attributed it to a misdisplacement of mandibular condyle, ([a] myofascial pain, [b] myofascial pain with limitation
causing pressure on ear structures.13 Thereafter, diverse in mouth opening), group II ([a] disk displacement with
hypotheses were presented to explain the underlying rea- reduction, [b] disk displacement without reduction with
sons for reporting otologic signs in TMDs,13 for instance, limited opening, [c] disk displacement without reduc-
the similar embryonical origin of the middle ear and chew- tion without limited opening), and group III ([a] arthral-
ing muscles; compression of vessels, nerves, and ligaments gia, [b] osteoarthritis, [c] osteoarthrosis). Axis II
of the middle and inner ear regions following the transloca- diagnoses are also according to the scores of the follow-
tion of articular head of the mandible13,14; middle ear dis- ing instruments: chronic pain grades, based on graded
eases subsequent to an Eustachian tube dysfunction15; and a chronic pain scale (GCPS) (0, no disability; I, low dis-
neuroanatomical interaction between the neural input from ability, low intensity; II, low disability, high intensity;
trigeminal system and dorsal cochlear nucleus (DCN).16,17 III, high disability, moderately limiting; and IV, high
A great amount of uncertainty, however, still exists about disability, severely limiting)23; depression levels, based
the biological origin of the relationship between TMDs and on the depression scale of the symptoms-checklist-90R
tinnitus.18 (SCL-90R) (normal, moderate, severe depression)24;
This topic, namely, “exploring the association between and nonspecific physical symptoms levels based on the
tinnitus and TMDs,” contains major clinical implications somatization scale (SOM) of the SCL-90R (normal,
for a diverse spectrum of health care professionals, which
moderate, severe somatization). The DC/TM22 and
impacts both levels of clinical practice and future research.
expanded DC/TMD21 are the revised versions of the
It also indicates taking advantage of specific multidisci-
RDC/TMD. The main discrepancy between DC/TMD
plinary clinical assessments and therapeutic approaches in
and RDC/TMD is that DC/TMD confirms pain and/or
the management of patients with tinnitus with underlying
headache locations as it separately examines each side
TMJ dysfunction. The present study aimed to systemati-
cally investigate and quantitatively analyze the association of the head.22 In the expanded DC/TMD, a set of uncom-
between tinnitus and TMDs. mon nonoverlapping TMDs with realizable criteria are
included to achieve high interexaminer reliability and
diagnostic validity.21
Methods
Exclusion criteria. Reviews, letters, case reports, conference
Systematic Search Strategy
abstracts, books, and studies that did not investigate the
This systematic review was conducted based on the guide- association between TMDs with tinnitus; non-English
lines of the Preferred Reporting Items for Systematic papers; and studies without an accessible full text were
Reviews and Meta-Analysis (PRISMA).19 A comprehen- excluded.
sive systematic search was conducted on January 7, 2018, The duplicates were removed using Endnote software
updated September 2018, in PubMed, Ovid, ScienceDirect, (Thomson Reuters, Philadelphia, Pennsylvania, USA, ver-
and Web of Science databases. The searched terms were tin- sion X7). The final papers were included through a 3-stage
nitus and temporomandibular. They were always combined, process: title screening, abstract screening, and full-text
thus papers with both keywords in the title and/or abstract screening. In each section, the papers that did not meet the
were extracted regardless of whether they focused on the inclusion criteria were excluded. In the cases of uncertainty,
association between tinnitus and TMDs. first the abstracts and then the full texts were screened. All
3 stages were independently conducted by 2 reviewers
Inclusion criteria. Cross-sectional, cohort, or case-control (S.O., Z.A.). If there was any disagreement, the authors dis-
studies in individuals with TMDs or tinnitus and their asso- cussed to reach a consensus.25 Overall, there was a com-
ciation were considered for the review. Three inclusion plete agreement between the reviewers.
Omidvar and Jafari 3

Quality Assessment individuals with and without tinnitus (Table 2), 4 cross-sec-
tional studies on TMD frequency in tinnitus without a con-
Because of the heterogeneity of the studies, the Crowe trol group (Table 2), and 6 cross-sectional studies related to
Critical Appraisal Tool (CCAT)26 was applied as the quality both tinnitus frequency in individuals with TMDs and vice
measurement tool in this systematic review. This instrument versa (Table 1 and 2). One paper consisted of 2 parts, a
is one of the few instruments that has undergone both reli- case-control study and a cross-sectional study.28 The refer-
ability and validity evaluations26,27 and is able to appraise ence lists for the selected publications were hand-searched;
different research study designs. The CCAT permits assess- no additional related article, however, was found. The bias
ments of the following aspects of each paper using a 6-point resulting from only searching databases in the English lan-
scale (from 0 to 5 for each category): permeable, introduc- guage (language bias) is acknowledged. All steps of the
tion, design, sampling, data collection, ethical issues, screening procedure are illustrated in Figure 1.
results/findings, and discussion, with a total potential score
of 40.
The strength of the Evidence
Synthesis of Results The included studies were assessed for methodological
quality using CCAT.26,27 The final CCAT scores (after an
A meta-analysis was carried out to investigate the possible agreement between authors) are reported in Table 3.
relationship between tinnitus and TMDs by calculating the According to CCAT recommendations, the scores are
odds ratios (ORs). Therefore, the studies without a convenient reported as both a total score and a percentage. There was
control group were excluded from the analysis. To prevent extreme variability in the quality of the studies, with a rat-
confounding bias resulting from low sample sizes, the papers ing of 35% to 80% (mean = 65.57%). Overall, only 5
with a sample size less than 100 subjects were not considered studies12,29-32 contained scores above 75%. The majority of
in the analysis. The papers were first classified into 2 groups, studies were deficient in several aspects, including the
the first group including papers associated with tinnitus fre- unclear definition of the assessment tools and potential bias,
quency in TMDs and the second group containing papers application of invalid and unreliable tools, and little or no
linked to TMD frequency in tinnitus. Then the papers of each mention of ethnical matters, for example, ethical approvals,
group were separated based on the study type (cross-sectional, funding sources, or potential conflict(s) of interest. Most
cohort, or case-control), and meta-analysis was conducted for papers provided minimal details regarding sample size cal-
each subgroup. The metan procedure in STATA software (Stata culations, inclusion and exclusion criteria, as well as non-
Corp., College Station, Texas, USA) version 14 was employed participation, withdrawal, and other incomplete/lost data.
for meta-analysis of ORs. Heterogeneity was assessed by The external validity of the studies, their particular strengths
Q-Cochrane test and I-squared statistic. Whenever heterogene- and limitations, and suggestions for future investigations
ity was confirmed (I2 value >0.75 and P value <0.1 by were also less described.
Q-Cochrane test), a random-effect meta-analysis with 95%
confidence intervals (CIs) was performed; otherwise, a fixed-
effect meta-analysis was applied. Forest plots were used to
Findings From the Systematic Review
present the pooled estimates of ORs and the 95% CIs. Demographic Characteristics of the Included
Papers
Results Tables 1 and 2 demonstrate the characteristics of the
The database search yielded 620 papers that were screened. included studies such as sample size, age, gender, and
Duplicated papers (n = 396), non-English papers (n = 17), assessment tools used for diagnosing tinnitus and TMDs and
case report studies (n = 28), animal studies (n = 1), and investigating the outcome. Sample size varied between 5933
titles out of the study scope (n = 60) were removed. This and 17 01732 in the studies focusing on tinnitus frequency in
initial screening resulted in a set of 118 papers. The co- individuals with TMDs. In the studies investigating TMDs
authors evaluated the 118 abstracts to extract those items in patients with tinnitus, the sample size was from 2034,35 to
corresponding to the inclusion criteria, allowing the authors 17 017.32 Song et al32 investigated both the frequency of tin-
to determine the levels of evidence available. Of the 37 nitus in TMDs and vice versa. Both genders (male and
studies extracted for the full review, 22 studies were identi- female) were considered in approximately all papers, except
fied and selected for final inclusion: 2 cohort and 3 case- 3 that assessed only females.33,36,37 Different age ranges
control studies related to tinnitus frequency in individuals were studies in the included papers; the youngest person
with and without TMDs (Table 1), 7 cross-sectional papers was 10 years,7 and the oldest was 84 years old.16
on tinnitus frequency in TMD patients without a control Demographic information of the participants, namely, age
group (Table 1), 1 case-control study related to TMDs in and gender, was not mentioned in 2 papers.18,32
4
Table 1. Summary of Characteristics of the Included Studies Reporting the Frequency of Tinnitus in Individuals With and Without TMDs.
Study Characteristics Population Characteristics Assessment Tool Outcome

Tinnitus
Gender Frequency
Author Year Study Design Subjects (n) Age (y) Female/Male Tinnitus Evaluation TMJ Evaluation (%)

Ciancaglini et al 1994 Cross-sectional Case = 797 37.4 ± 8.3 (15-60) 534/263 Asking questions -Clinical examinations 6.4
-CT
Tuz et al 2003 Case-control 250 *29.6 *165/35 Asking questions RDC/TMD *45.5
(*case = 200, **control = 50) **37.2 ** **26
27/23
Bernhardt et al 2004 Cross-sectional 4228 20-79 NR Asking questions Clinical examinations *5.77
(*case = 745, **control = 3483) **2.76
Bernhardt et al 2011 Cohort 3134 (*case = 191; **control = 20-81 1628/1506 Asking questions Clinical examinations *12.6
2643) **5.8
Calderon et al 2012 Cross-sectional Case = 59 35.25 (17-52) 59 F Asking a question -RDC/TMD 54.24
-VAS
Saldanha et al 2012 Cross-sectional 200 (*case = 140, **control = 60) 36.7 149/51 -Asking a question -RDC/TMD *60.71
-VAS -PPT **25
-VAS
Fernandes et al 2013 Case-control 224 37.7 (18-76) 184/40 A question in RDC/TMD RDC/TMD *70.37
(*case = 162, **control = 62) questionnaire **24.19
Fernandes et al 2014 Cross-sectional 261 37.0 (18-76) 261 F A question in RDC/TMD RDC/TMD *70.37
(*case = 216, **control = 45) questionnaire **24.44
Ferendiuk et al 2014 Cross-sectional Case = 1209 19-50 952/256 Medical interview Clinical examinations 3.72
Buergers et al 2014 Cross-sectional 951 54.1 ± 17.1 478/473 -Asking question RDC/TMD *36.6
(*case = 82, **control = 869) -THI **4.4
Manfredini et al 2014 Cross-sectional Case = 238 49.3 ± 13.5 58/192 Asking questions An executive summary of the 30.4
DC/TMD
Algieri et al 2016 Cross-sectional Case = 200 44.10 (13-79) 168/32 THI -Clinical examinations 60
MRI
-Wilkes classification
Effat 2016 Case-control 214 *35.3 ± 12.1 (10-59) *84/20 Asking questions -History taking *52
(*case = 104, **control = 110) **30.9 ± 8.1 (14-53) **66/44 -The expanded DC/TMD **12
de-Pedro-Herráez et al 2016 Cohort 62 (*case = 31, **control = 31) 24-58 62 F An item in a health RDC/TMD *51.6
questionnaire **9.7
Vasconcelos et al 2016 Cross-sectional Case = 100 13-70 80/20 Asking questions The simplified Fonseca 64
anamnestic questionnaire
Maciejewska-Szaniec et al 2017 Cross-sectional Case = 246 40.08 ± 11.12 147/99 Asking questions RDC/TMD 14.63
Kim et al 2018 Cross-sectional 11 745 NR 5967/5778 Asking questions -A questionnaire *27.38
(*case = 924, **control = 10 821) -Clinical examinations **21.27
Song et al 2018 Cross-sectional 17 017 (*case = 2003, **control = NR NR Asking questions Asking questions *32.65
15 014) **21.39

Abbreviations: Case, subjects with temporomandibular joint disorders; control, subjects without temporomandibular joint disorders; CT, computed tomography; F, female; MRI, magnetic resonance imaging; NR, not reported;
PPT, pain pressure threshold; RDC/TMD, research diagnostic criteria for temporomandibular joint disorder; THI, tinnitus handicap inventory; TMD, temporomandibular disorders; TMJ, temporomandibular joint; VAS, visual
analog scale
Table 2. Summary of Characteristics of the Included Studies Reporting TMD Frequency in Individuals With and Without Tinnitus.

Study Characteristics Population Characteristics Assessment Tool Outcome

Gender TMD
Author Year Study Design Subjects (n) Age (y) Female/Male Tinnitus Evaluation TMJ Evaluation Frequency (%)
Morgan 1992 Cross-sectional Case = 20 55.3 (22-74) 4/16 NR -*Clinical examinations *95
-**Mandibular scan and EMG **20
Lam et al 2001 Cross-sectional Case = 192 NR NR Asking questions RDC/TMD 64.1
Rubinstein 1993 Cross-sectional Case = 102 56 (15-84) 40/62 NR -*Clinical examinations *84
et al. -**A questionnaire **46
Bernhardt et 2004 Cross-sectional 4228 (*case = 139, **control = 20-79 *67/72 Asking questions Clinical examinations *30.93
al (Phase I) 4089) **2092/1997 **17.17
Bernhardt et 2004 Case-control 1937 *18-71 *13/17 Asking questions Clinical examinations *60
al (Phase II) (*case = 30; **20-79 **992/915 **36.5
**control = 1907)
Morais and Gil 2012 Cross-sectional Case = 20 32.1 (20-55) 14/6 -Asking question Asking questions 90
-THI
Saldanha et al 2012 Cross-sectional 200 (*case = 100, **control = *39.16 ± 12.01 *84/16 -Asking a question -RDC/TMD * 85
100) **34.33 ± 10.72 **65/35 -VAS -PPT **55
-VAS
Buergers et al 2014 Cross-sectional 951 54.1 ± 17.1 478/473 -Asking question RDC/TMD *44.12
(*case = 68, **control = 883) -THI **5.89
Fernandes 2014 Cross-sectional 261 37.0 (18-76) 261 F A question in RDC/TMD *93.25
et al (*case = 163, **control = 98) RDC/TMD **65.31
questionnaire
Kim et al 2018 Cross-sectional 11 745 (*case = 2555, **control *49.1 ± 0.6 *1436/1119 Asking questions -Asking questions *9.9
= 9190) **44.5 ± 0.3 **4531/4659 -Clinical examination **7.3
Song et al 2018 Cross-sectional 17 017 NR NR Asking questions Asking questions *16.92
(*case = 3866, **10.26
**control = 13 151)

Abbreviations: Case, subjects with tinnitus; control, subjects without tinnitus; EMG, electromypgraphy; F, female; NR, not reported; PPT, pain pressure threshold; RDC/TMD, research diagnostic
criteria for temporomandibular joint disorder; THI, tinnitus handicap inventory; TMD, temporomandibular disorders; TMJ, temporomandibular joint; VAS, visual analog scale

5
6 Annals of Otology, Rhinology & Laryngology 00(0)

Figure 1. Flow diagram of literature search and selection criteria corresponding with the Preferred Reporting Items for Systematic
Reviews and Meta-Analyses (PRISMA) statement 2009.

Tinnitus Frequency in Individuals With TMDs a stronger predictor for the development of tinnitus than
tenderness or pain in the masticatory muscles.29 There was
Table 1 presents the frequency of tinnitus in individuals no significant difference between the prevalence of tinnitus
with TMDs in 18 included publications. Tinnitus frequency in different TMD subgroups in 2 studies.31,40 In Calderon
varied between 3.72%38 and 70.37%36,39 in the patients with et al’s33 (2012) study, approximately 68% of patients with
TMDs (total sample = 7647) and 2.76%28 and 26%40 in the tinnitus suffered both muscular and articular TMDs. In
controls (total sample = 33 188). another study, 75% of patients with tinnitus complained of
some soreness or pain to palpation in the TMJ.35 The asym-
TMD Frequency in Individuals With Tinnitus metrical opening movement was the most frequent TMD
sign reported by individuals with tinnitus in 1 study.34
Among the included studies, 11 papers investigated TMD
frequency in patients with tinnitus (Table 2). TMD fre-
quency was reported between 9.9%30 and 95%35 in the tin- Tinnitus Characteristics in TMDs
nitus group (total sample = 7255) and 5.89%11 and 65.31%36 In a population with both tinnitus and TMDs (n = 30), all
in the subjects without tinnitus (total sample = 29 418). patients with unilateral TMDs and simultaneous unilateral
tinnitus demonstrated both symptoms on the same side
The Relationship Between the Type of TMDs (8/8), and participants with bilateral TMDs complained
from either bilateral (14/17) or unilateral (3/17) tinnitus.11
and Tinnitus In another study, unilateral tinnitus (n = 26) was more fre-
Among the included papers, 8 studies reported the effect of quent than bilateral tinnitus (n = 19) in participants with
TMD type on the prevalence of tinnitus,12,28,29,31,33-35,40 In 2 both TMDs and tinnitus (n = 45).38 The frequency of bilat-
studies, patients with tinnitus and TMDs perceived tender- eral tinnitus (n = 83/200) in TMD patients was higher than
ness of the masticatory muscles and TMJ significantly more unilateral tinnitus (n = 37/200) in 1 study.41 In 2 later stud-
often than subjects with dysfunctions but without tinni- ies, the laterality of TMDs was not reported.38,41 Other
tus.12,28 In another study, tenderness or pain in the TMJ was characteristics of tinnitus (eg, its pitch, loudness, duration,
Table 3. Quality Assessment of the Included Papers With CCAT Ratings.

Data Ethical
Author Year Preamble Introduction Design Sampling Collection Matters Results Discussion Total/40 Total (%)
Rubinstein et al 1990 5 4 2 3 3 0 3 3 23 57.5
Morgan 1992 3 3 1 1 2 0 3 1 14 35
Ciancaglini et al 1994 5 3 4 4 3 0 4 4 27 67.5
Tuz et al 2003 4 5 3 3 3 0 3 2 23 57.5
Bernhardt et al 2004 4 5 4 4 3 1 3 3 27 67.5
Bernhardt et al 2011 4 5 4 4 3 3 4 4 31 77.5
Lam et al 2011 5 5 4 2 3 1 3 5 28 70
Calderon et al 2012 5 5 1 1 4 3 3 4 26 65
Morais and Gil 2012 3 3 2 1 2 3 2 1 17 42.5
Saldanha et al 2012 5 5 4 3 4 3 4 3 31 77.5
Fernandes et al 2013 5 5 4 3 3 2 3 4 29 72.5
Buergers et al 2014 5 5 4 2 5 1 3 4 29 72.5
Fernandes et al 2014 5 5 3 2 3 3 3 4 28 70
Ferendiuk et al 2014 4 5 3 3 3 3 3 2 26 65
Manfredini et al 2014 5 5 3 3 4 3 4 4 31 77.5
de-Pedro-Herráez et al 2016 2 5 1 1 2 3 2 3 19 47.5
Effat 2016 3 5 3 4 4 2 3 3 27 67.5
Vasconcelos et al 2016 5 5 2 2 2 1 4 3 24 60
Algieri et al 2017 5 5 3 3 3 0 4 2 25 62.5
Maciejewska-Szaniec et al 2017 4 5 4 3 4 4 3 2 29 72.5
Song et al 2018 5 5 3 5 3 3 3 5 32 80
Kim et al 2018 5 5 2 5 3 3 4 4 31 77.5

Abbreviation: CCAT, Crowe critical appraisal tool.

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8 Annals of Otology, Rhinology & Laryngology 00(0)

and continuity) in TMDs were not reported in the included The Relationship Between Tinnitus and TMDs
papers.
Table 4 indicates the results of the meta-analysis for the
association between tinnitus and TMDs in the included
Instrumentation case-control, cohort, and cross-sectional studies. ORs
The method of classifying individuals as those with and (95% CI) ranged from 1.78 (1.61-1.97) to 7.80 (2.93-
without tinnitus and with and without TMDs was quite dif- 20.78) in the studies related to tinnitus frequency in TMDs
ferent. To diagnose patients with TMDs, 1 papers used and from 1.81 (1.64-1.99) to 7.80 (2.93-20.78) in the
RDC/TMD11,12,18,33,36,37,39,40,42 or its revised versions,7,31 6 papers related to TMD frequency in tinnitus, all implying
papers did clinical examinations,28,29,35,38,41,43 3 asked that tinnitus was significantly related to TMDs. The papers
some questions,32,34,44 and 2 used both clinical examina- were classified into 2 groups, namely, those with samples
tions and asking questions.16,30 The method of labeling derived from health studies (public population) and those
patients as those suffering from TMDs was summarized in with samples selected from people seeking dental care
Tables 1 and 2. (specific population). The connection between tinnitus
To evaluate the presence or absence of tinnitus, various and TMDs was significantly stronger in the papers linked
methods were used in the included papers. Two publica- to specific populations compared to the papers associated
tions used a question in RDC/TMD questionnaire.36,39 Other with public populations. The results of the meta-analysis
studies asked 1 or more questions,7,11,12,18,28-34,37,38,40,42-44 but are also summarized in the forest plots (Figures 2A-2C).
the applied questions were only mentioned in 4.28-30,33 The Forest plots provide a simple visual representation of the
tinnitus handicap inventory (THI) questionnaire was used amount of variation across studies as well as an estimate
in 3 papers.11,34,41 of the overall result of all studies together.45 In the current
study, the forest plots were demonstrated when there was
more than 1 study in each investigated category, namely,
Results of the Meta-Analysis tinnitus occurrence in TMDs and vice versa in cross-sec-
Eleven papers including a control group for comparison tional studies among people seeking dental care (Figure
were considered for the analysis. One of the papers was 2A), TMD occurrence in tinnitus in cross-sectional popu-
excluded given a sample size of less than 100.37 Fernandes lation-based studies (Figure 2B), and tinnitus occurrence
et al36,39 investigated tinnitus frequency in the individuals in TMDs in case-control studies among people seeking
with and without TMDs in 2 papers. One study was excluded dental care (Figure 2C). In each forest plot, the horizontal
from the analysis as all subjects displayed a chief complain axis represents the odds ratios, and the vertical line (dis-
of orofacial pain leading to a high frequency of TMDs both played at the value of 1) is known as the “line of null
in the individuals with tinnitus and the control group.36 effect,” where no association is expected between tinnitus
Bernhardt et al also published 2 papers. The later one was a and TMDs. Each horizontal line put onto a forest plot
cohort study on tinnitus frequency in TMD study,29 and the demonstrates a separate study being analyzed. Each study
former paper contained 2 studies consisting of a case-con- “result” has 2 components comprising: (1) a black box
trol study on TMD frequency in subjects with and without indicating both a point estimate of the study result and the
tinnitus and a cross-sectional study investigating TMD fre- size of the stud 45,46 (the largest sample size in Song et al,32
quency in tinnitus and vice versa.28 The main population 2018) and (2) a horizontal line representing the 95% con-
had overlap among these 3 studies. The cohort study29 (the fidence intervals of the study result.45,46 For example, the
later one) therefore was considered to investigate tinnitus point estimate of Buergers et al11 study was 12.62, and its
frequency in TMDs, and the second part of the former confidence interval was 7.25 to 21.97. Since none of the
study,28 with a higher sample size relative to the first part, study lines crossed the line of null effect, they all indi-
was analyzed for exploring TMD frequency in tinnitus. cated a statistically significant result.46 The weight (%)
Song et al32 (2018) and Kim et al30 (2018) also published 2 exhibits the impact of each individual study on the pooled
papers on the same population. The paper with a larger sam- result. Among all included studies for drawing forest
ple size32 was included for the analysis. Thus, eventually 8 plots, the Song et al32 study had the highest weight (92.99)
papers were included for the meta-analysis: 3 case- and Bernhardt et al28 had the lowest one (7.01). A dia-
control7,39,40 and 1 cohort29 papers on tinnitus frequency in mond in each figure presents the overall point estimate
subjects with and without TMDs, 1 cross-sectional study on from the meta-analysis and its confidence interval. The
TMD frequency in individuals with and without tinnitus,28 center of the diamond displays the pooled point estimate,
and 3 cross-sectional papers (1 on public population32 and 2 and its horizontal tips represent the 95% confidence
on individuals seeking dental care11,12) both on tinnitus fre- interval.45 Because the diamonds did not cross the line of
quency in subjects with and without tinnitus as well as null effect, the combined result was potentially statisti-
TMD frequency in individuals with and without tinnitus. cally significant.
Omidvar and Jafari 9

Table 4. Summary ORs Estimates and 95% CIs for Case-Control, Cross-Sectional, and Cohort Studies of the Association Between
Tinnitus and TMDs.

Within Hetro

Groups Author Type of Studies Study Design No. ORs 95% CI I2 (%) P
Tinnitus Buergers et al, 2014 Specific population Cross-sectional 2 7.798 2.926-20.782 80.1 .025
occurrence Saldanha et al, 2012 Specific population Cross-sectional
in individuals Effat, 2016 Specific population Case-control 3 5.229 2.422-11.291 73.5 .023
with TMDs Fernandes et al, 2013 Specific population Case-control
Tuz et al, 2003 Specific population Case-control
Song et al, 2018 Public population Cross-sectional 1 1.7813 1.6099-1.9711 — —
Bernhardt et al, 2011 Public population Cohort 1 2.5312 1.5978-4.0098 — —
TMD Buergers et a, 2014 Specific population Cross-sectional 2 7.798 2.926-20.782 80.1 .025
occurrence Saldanha et al, 2012 Specific population Cross-sectional
in individuals Song et al, 2018 Public population Cross-sectional 2 1.806 1.638-1.991 0.0 .322
with tinnitus Bernhardt et al, 2004 Public population Cross-sectional

Abbreviations: CI, confidence interval; hetero, heterogeneity; I2, inconsistency index; No., number of studies; ORs, odds ratios; TMDs,
temporomandibular joint disorders; —, indicates that it was incalculable.

Discussion or constant contraction of the masticatory muscles might


affect middle ear muscle tension or ventilation. This can
Our study on the relationship between tinnitus and TMDs generate afferent signals that influence the auditory path-
demonstrated that (1) TMDs led to ORs of 1.78 to 7.79 for ways via cochlear nerve.6 It, however, cannot be the only
diagnosed tinnitus and tinnitus perception resulted in ORs explanation because tinnitus and its somatosensory modula-
of 1.80 to 7.79 for TMDs, suggesting that (2) the signs of tion can persist even after the 8 nerve excision.47 Recently,
TMDs can enhance the development of tinnitus and percep- neuroanatomical and experimental studies imply anatomic
tion of tinnitus can be considered as a risk for presenting and topographic associations between the trigeminal nerve
TMDs. (3) The link between tinnitus and TMDs was stron- and TMJ capsule and between the trigeminal ganglion and
ger in the population with dental complaints. cochlear nucleus (CN).48,49 As indicated in Figure 3, sen-
The ORs of 1.78 to 7.79 for diagnosed tinnitus in patients sory inputs from the face via the trigeminal (V) nerve in the
with TMDs revealed their higher risk of developing tinnitus spinal trigeminal tract, the neck via the C2 dorsal spinal
rather than those without TMDs. A few studies determined root, and the external and middle ears via the common spi-
the ORs for tinnitus prevalence in TMD patients.30,37 In a nal tract of the facial (VII), glossopharyngeal (IX), and
study on a low number of patients with (n = 31) and with- vagus (X) cranial nerves converge to a common region in
out (n = 31) TMDs, the ORs of tinnitus prevalence was the lower part of the medulla (the medullary somatosensory
9.96.37 A health study on a large population reported that nucleus). These fibers then project to the ipsilateral dorsal
subjects with TMDs suffered tinnitus 1.6 times more than cochlear nucleus (DCN). The modulation of activity in the
subjects without TMDs.30 medullary somatosensory nucleus to the DCN pathway dis-
In our study, tinnitus perception also caused ORs of 1.80 inhibits the DCN. Projections from the DCN to the higher
to 7.79 in patients with TMDs, which means tinnitus func- centers lead to hyperactivity of the central auditory system
tions as a risk for TMDs. This finding was consistent with a and finally, tinnitus perception.5,17 The interaction between
few previous studies.28,32 The study of health in Pomerania the auditory and somatosensory systems might explain why
on a large population (n = 4228) reported the ORs of 2.99 tinnitus sufferers can modulate the loudness and pitch of
for TMD prevalence in tinnitus.28 In the other health study, their tinnitus.50,51
participants with tinnitus showed ORs of 1.97 for TMD The prevalence of tinnitus in patients with TMDs was
prevalence.32 This relationship demonstrates an important significantly higher than those without TMDs. Similarly,
clinical implication for diverse health care professionals, the prevalence of TMDs was higher in patients with tinnitus
especially in patients requiring dental cares. compared with those without tinnitus. Reports of tinnitus
One common explanation for tinnitus perception in and TMD frequencies, however, widely differed among the
TMDs is attributed to an anatomical connection (eg, the included studies. This can be attributed to differences in
tensor veli palatini, the eustachian tube, or several liga- their methodology, including the methods of dividing indi-
ments) between a TMJ or the masticatory muscles and mid- viduals into the case and control groups, sample sizes,
dle ear muscles. A disorder in TMJ (eg, disc displacement) demographic data, and differences in the study design and
10 Annals of Otology, Rhinology & Laryngology 00(0)

Figure 2. Forest plots for the relationship between tinnitus and temporomandibular disorders (TMDs) with the use of fixed- and
random-effects models. (A) Tinnitus occurrence in TMDs as well as TMD occurrence in tinnitus in cross-sectional studies on people
seeking dental cares. (B) TMD occurrence in tinnitus in cross-sectional population-based studies. (C) Tinnitus occurrence in TMDs in
case-control studies on people seeking dental cares. CI, confidence interval; OR, odds ratio; square, study-specific OR estimate (size
of square indicates the study specific statistical weight, ie, the inverse of the variance); horizontal line, 95% CI; diamond, summarize
OR estimate and its corresponding 95% CI. All statistical tests were 2-sided. Statistical heterogeneity between studies was assessed
with the I-squared test.

the procedures for diagnosis of tinnitus and TMDs. For no significant difference.31,40 It appears that tinnitus is a
instance, the TMD frequency in the individuals with and with- chronic stressor that increases masticatory muscle and TMJ
out tinnitus was reported 93.25% and 65.31%, respectively.36 activities leading to pain. It is, however, not clear whether
These high percentages might be created by selecting both the relationship between TMDs and tinnitus might consist
case and control groups from the subjects with the chief com- of a response to emotional stress yet.28,29,52 Alteration in the
plain of orofacial pain.36 If samples were selected without neuromuscular coordination of the craniomandibular, which
any bias, TMD prevalence was likely lower in these sub- can be considered as one of the possible causes of otogenic
jects. Further studies thus are required to draw a more pre- symptoms including tinnitus, might also result in a higher
cise conclusion in this area. tenderness of masticatory muscles.53 In a longitudinal study,
Effect of the TMD type on the prevalence of tinnitus had the prevalence of tinnitus in patients with palpation pain in
been examined in a few studies.12,28,29,31,33-35,40 Most studies the TMJs was higher than those with tenderness or pain in
suggested a higher prevalence of muscular and/or articular the masticatory muscles. The authors, however, argued that
TMDs in patients with tinnitus,12,28,29,33,35 and some reported as the small sample of subjects with palpation pain in the
Omidvar and Jafari 11

Figure 3. Disinhibition of the dorsal cochlear nucleus (DCN) as a possible hypothesis for somatic tinnitus.
Adapted with permission from Levine et al (2007).

TMJs, it was not possible to infer that TMJ palpation pain diminish the likelihood of false positive or false negative
could be a prognostic factor for tinnitus.29 Due to inconsis- patient selection and increase the accuracy of the results.
tencies and lack of information in the literature, further Tinnitus is often imperceptible or inaudible to others, and
investigations are suggested to clarify the effects of the it is objectively hard to confirm patients’ statements about
types of TMDs on tinnitus. tinnitus.56 In almost all included papers, except 3,11,34,41
Among the included papers, just 1 reported the relation- tinnitus was only examined by asking 1 or more questions,
ship between the laterality of tinnitus and the laterality of and no detailed information was given regarding other char-
TMDs. In this study,11 all subjects with simultaneous unilat- acteristics of tinnitus, even clinical specifications like tinni-
eral TMDs and unilateral tinnitus had both symptoms on the tus quality and continuity.7,11,12,18,28-34,36-40,43,44 The THI
same side, and almost all individuals with bilateral TMDs questionnaire was the validated tool used in 3 papers.11,34,41
(except 3 subjects) had tinnitus on both sides. This finding The THI, however, was applied to evaluate the severity of
also was reported in other investigations,16,54 which may be handicap resulting from the tinnitus than to identify tinnitus
associated with the DCN as a possible site of hyperactivity appearance.57-61 In future studies, applying well-defined,
in somatic tinnitus. As the projections from the somatosen- detailed questionnaires as well as psychoacoustic measure-
sory nuclei (nucleus cuneatus/medullary somatosensory ments of tinnitus are suggested to obtain accurate findings
nucleus) to the DCN are only ipsilateral, somatic tinnitus is regarding the tinnitus characteristics in TMD patients.
perceived ipsilaterally.5 Other characteristics of tinnitus like The study design of almost 80% of included papers was
its continuity, pitch, and loudness were not explained in any cross-sectional,11,12,16,18,28,30-36,38,41-44 and the others con-
of the included papers, suggesting further studies to define tained a case-control7,28,39,40 or a cohort design.29,37 Cross-
the attributes of tinnitus in subjects with TMDs clearly. sectional studies are primarily used to determine the
There are different methods for TMD diagnosis. In the prevalence and identify associations. This type of study
current review, almost half of the papers used RDC/ cannot distinguish between cause and effect. Case-
TMD11,12,18,33,36,37,39,40,42 or the revised versions of this controlled studies compare people with the outcome of
criteria7,31 for diagnosing TMDs. RDC/TMD is a reliable interest and a control group who do not. They are retrospec-
and valid protocol for diagnosing and grouping the prevalent tive and cannot be applied to calculate the relative risk.
forms of TMDs using a questionnaire and clinical examina- Nevertheless, they can be used to calculate ORs. Cohort
tions.55 It is more likely that individuals classified into the studies are the best way to discriminate between cause and
TMD groups in these studies truly suffered from it. The effect due to evaluating events in chronological order.62 A
other half, however, asked some questions and/or applied few cohort studies had evaluated the risk of tinnitus occur-
different methods of clinical examinations without reporting rence in patients with TMDs and reported that signs of
their validity or reliability.16,28-30,32,34,35,38,41,43,44 This TMDs were a risk factor for the development of tinni-
approach might lead to underestimating or overestimating tus.29,37,63 No cohort study, however, investigated the risk of
the presence of TMDs. Applying reliable and valid tools can TMDs occurrence in individuals with tinnitus. Given a low
12 Annals of Otology, Rhinology & Laryngology 00(0)

number of cohort studies, future researches with a cohort ORCID iD


design are suggested to identify a likely cause-and-effect Zahra Jafari https://orcid.org/0000-0002-0485-2003
relationship between tinnitus and TMDs.
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