Innovations in Tinnitus Research: Review

Trends in Hearing
Volume 22: 1–15
Association Between Subjective Tinnitus ! The Author(s) 2018
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DOI: 10.1177/2331216518800640

Disorders: A Systematic Review journals.sagepub.com/home/tia

E. J. Bousema1,2 , E. A. Koops1,3, P. van Dijk1,3 and P. U. Dijkstra4,5

Abstract
Movements of the neck and jaw may modulate the loudness and pitch of tinnitus. The aim of the present study was to
systematically analyze the strength of associations between subjective tinnitus, cervical spine disorders (CSD), and temporo-
mandibular disorders (TMD). A systematic literature search of the Medline, Embase, and Pedro databases was carried out on
articles published up to September 2017. This covered studies in which tinnitus and CSD or TMD were studied as a primary
or a secondary outcome and in which outcomes were compared with a control group. Included articles were evaluated on
nine methodological quality criteria. Associations between tinnitus and CSD or TMD were expressed as odds ratios. In total,
2,139 articles were identified, of which 24 studies met the inclusion criteria. Twice, two studies were based on the same data
set; consequently, 22 studies were included in the meta-analysis. Methodological quality was generally limited by a lack of
blinding, comparability of groups, and nonvalidated instruments for assessing CSD. Results indicated that patients with
tinnitus more frequently reported CSD than subjects without tinnitus. The odds ratio was 2.6 (95% CI [1.1, 6.4]). For
TMD, a bidirectional association with tinnitus was found; odds ratios ranged from 2.3 (95%CI [1.5, 3.6]) for arthrogenous
TMD to 6.7 (95%CI [2.4, 18.8]) for unspecified TMD. Funnel plots suggested a publication bias. After adjusting for this, the
odds ratios decreased, but associations persisted. There is weak evidence for an association between subjective tinnitus and
CSD and a bidirectional association between tinnitus and TMD.

Keywords
subjective tinnitus, systematic review, neck pain, temporomandibular disorder

Date received: 5 February 2018; revised: 23 July 2018; accepted: 9 August 2018

majority of tinnitus sufferers, the sound is audible only

Introduction
to the patient and is called subjective tinnitus (Ward,
Tinnitus is a sound that is perceived in the absence of an Vella, Hoare, & Hall, 2015).
acoustic event occurring external to the listener’s body. It Numerous studies suggest that subjective tinnitus
is commonly described as the sound of, for example, arises in the central auditory system due to neuroplastic
crickets, winds, falling tap water, grinding steel, escaping adaptations that occur in response to changes in the
steam sound, or as a combination of sounds (Han, Lee,
Kim, Lim, & Shin, 2009). Tinnitus can be perceived in 1
Department of Otorhinolaryngology, Head & Neck Surgery, University
one ear, both ears, or more centrally located ‘‘in the Medical Center Groningen, University of Groningen, the Netherlands
2
head’’ (Heller, 2003). In adults of the general population, Fysiotherapie Sittard Oost, the Netherlands
3
the prevalence of tinnitus ranges between 10% and 15% Research School of Behavioral and Cognitive Neurosciences, Graduate
School of Medical Sciences, University of Groningen, the Netherlands
(D. Baguley, McFerran, & Hall, 2013). In people older 4
Department of Oral and Maxillofacial Surgery, University Medical Center
than 60 years of age, the prevalence of tinnitus increases Groningen, University of Groningen, the Netherlands
to about 18% (Davis & El Rafaie, 2000). 5
Department of Rehabilitation Medicine, University Medical Center
In a minority of people with tinnitus, the sound is Groningen, University of Groningen, the Netherlands
audible to an observer and is therefore called objective Corresponding author:
tinnitus. In most of these patients, it is possible to deter- E. J. Bousema, Bachstraat 103, Sittard, 6137 RX, the Netherlands.
mine the underlying etiology. However, in the vast Email: [email protected]

Creative Commons Non Commercial CC BY-NC: This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License (http://www.
creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work
is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage).
2 Trends in Hearing

peripheral auditory system (Eggermont & Roberts, 2004; Facial Muscles or Neck Pain or Masticatory Muscles
Kaltenbach, 2011; Moller, 2007; Norena & Farley, 2013; or Musculoskeletal or Trigger point or ((Head or
Roberts et al., 2010). Animal studies indicate that per- Jaw or Neck or Shoulder) and (Muscle or Pain or
ipheral damage, for example, noise trauma, results in Trauma or injuries))) (Appendix 1: electronic search
changes in spontaneous neural activity (Eggermont, strategy).
2005). The central auditory system is thought to com- Titles and abstracts were assessed for their relevance
pensate for the reduced input by upregulating the excit- by the first author (E. J. B.). In the next round, selected
ability of the central auditory neurons (Eggermont & full-text articles were retrieved and their relevance inde-
Roberts, 2012; Knipper, Van Dijk, Nunes, Ruttiger, & pendently assessed by two observers (E. J. B. and P. D.).
Zimmermann, 2013; Tyler, 1984). Interobserver agreements were expressed as Cohen’s
Two thirds of patients may experience modulations to kappa. Inclusion criteria were a cross-sectional or longi-
their subjective tinnitus through somatosensory system tudinal cohort design in which tinnitus and CSD or TMD
effects in addition to those associated with central audi- were treated as either primary or secondary outcomes
tory neurons. These patients are able to modulate the and that this group was compared with a control
loudness and pitch by muscle contractions of the neck, group. Exclusion criteria were reviews, letters to the
head, or jaw (Bjorne, 2007; Bonaconsa, Mazzoli, editor, animal studies, number of patients <10, and art-
Magnano, Milanesi, & Babighian, 2010; Levine, 1999; icles describing neck or jaw disorders caused by a
Pinchoff, Burkard, Salvi, Coad, & Lockwood, 1998; trauma. The term trauma was used as part of the
Rocha & Sanchez, 2007; Rubinstein, 1993; Sanchez, search strategy to avoid missing possibly relevant art-
Yupanque Guerra, Lorenzi, Brandao, & Bento, 2002; icles. No language restrictions were applied. In case the
Vernon, Griest, & Press, 1992). To indicate this type of authors were not able to understand an article for lan-
tinnitus, the term somatosensory tinnitus has been pro- guage reasons, it was translated. References of the stu-
posed (Levine, Abel, & Cheng, 2003). Moreover, cervical dies included were checked for relevant studies that had
spine disorders (CSD; e.g., pain, tenderness; Abel & been missed in the database searches.
Levine, 2004; Bjorne, 2007; Folmer & Griest, 2003;
Michiels, De Hertogh, Truijen, & Van de Heyning,
2015; Oostendorp et al., 2016; Reisshauer et al., 2006;
Assessment of Characteristics of Studies
Sahin, Karatas, Ozkaya, Cakmak, & Berker, 2008) or The methodological quality of the studies included was
temporomandibular disorders (TMD; Ramirez, independently judged by two observers (E.J. B. and E. A.
Ballesteros, & Sandoval, 2008) are frequently associated K.) according to nine criteria of a modified version of
with tinnitus. However, in most of these studies, the Quality Assessment of Case-Control Studies (2014). The
prevalence data are not compared with a control criteria were (1) ‘‘Was the research question or objective
group, and the strength of the association between tin- in this article clearly stated and appropriate?’’ (2) ‘‘Was
nitus and CSD or TMD remains unclear. the study population clearly specified and defined?’’ (3)
To the best of our knowledge, a systematic review of ‘‘Were controls selected or recruited from the same or
studies on the association between subjective tinnitus similar population that gave rise to the patients
and CSD or TMD has not yet been carried out. As (including the same timeframe)?’’ (4) ‘‘Were the defin-
movements of the neck and jaw may increase or decrease itions and inclusion and exclusion criteria used to iden-
the loudness and pitch of tinnitus, understanding the tify or select patients and controls valid, reliable, and
association between tinnitus and CSD or TMD is implemented consistently across all study participants?’’
important because in the future, treatment of CSD or (5) ‘‘Were the patients clearly defined and differentiated
TMD might be used to reduce tinnitus. The aim of the from controls?’’ (6) ‘‘Were the patients and controls ran-
present study was to systematically analyze the level of domly selected?’’ (7) ‘‘Were controls matched to patients
evidence for a bidirectional association between subject- on one or more attributes?’’ (8) ‘‘Were the measures of
ive tinnitus and symptoms of CSD or TMD. exposure clearly defined, valid, reliable, and imple-
mented consistently across all study participants?’’ and
(9) ‘‘Were the assessors blinded to the patient or control
Methods status of participants?’’ Criteria were scored: [þ] ¼ Yes,
[–] ¼ No, [?] ¼ Cannot be determined/unclear/ not
Identification and Selection of Studies reported. Each quality item addresses a different source
A database search was performed in Medline, Embase, of potential bias and can impact study results dispropor-
and Pedro to identify articles published within the time tionately. If, for example, only one quality item is not
period of 1966 to September 2017. The following search fulfilled, it does not mean that the study has a better
terms were used: Tinnitus and (Temporomandibular quality than a study with two quality items not fulfilled.
Joint or Jaw or Cervical Vertebrae or Neck Muscles or Therefore, the results of methodological quality
Bousema et al. 3

assessment will be described per item, without summing reference lists of the articles (Figure 1). No articles sur-
across items (see Table 2). faced in our search strategy that needed translation.

Data Synthesis and Analysis Data Extraction and Quality Assessment

Data were entered in the program Comprehensive Meta- Study characteristics. Almost all studies were cross-sec-
Analysis V3 (Biostat, Englewood, NJ, USA). If odds tional (n ¼ 20) in design. Data of two longitudinal studies
ratios were provided in the original article, then they were extracted from baseline measurements (Table 1;
were entered into the database. When odds ratios were Bonaconsa et al., 2010; Lee et al., 2016). Twelve studies
not reported, the data were entered into the database as investigated the presence of CSD or TMD in patients
they were reported in the article (Borenstein, Hedges, with and without tinnitus. Ten studies examined the
Higgins, & Rothstein, 2009). Meta-analyses were per- presence of tinnitus in patients with and without TMD
formed assuming a random-effects model. The summary only. No studies were found in which tinnitus was
statistic of the association between tinnitus and CSD or explored in patients with and without CSD. Of the stu-
TMD was expressed as odds ratios. To explore publica- dies investigating the association between tinnitus and
tion bias for each association, funnel plots were made. TMD, three studies examined patients with and without
To adjust for potential publication bias, Duval and tinnitus, wherein both groups also complained about
Tweedie’s (2000) nonparametric trim-and-fill approach bruxism (Camparis et al., 2005), disc displacements of
to impute theoretical missing studies was applied. the temporomandibular joint (TMJ; Ren & Isberg,
1995), or headache or facial pain (Pezzoli et al., 2015).
Most patients were recruited from general or specialized
Results hospitals/ENT departments. Almost all studies included
adult patients and controls of all ages. However, in one
Search Strategy and Study Selection
study, patients and controls were students less than 21
A total of 2,139 records were found: in PubMed, 1,069; years old (Akhter et al., 2013), and in another study,
in Embase, 1,053; and in Pedro, 17. After removing patients and controls were exactly 70 or 76 years old
duplicates, 1,581 articles remained. In 1,517 of these, (Rubinstein et al., 1993). In four studies, patients and
the association between tinnitus and CSD or TMD had controls were recruited from a community database
not been studied. Two observers assessed the full text of (Table 1; Khedr et al., 2010; Kuttila et al., 2005; Park
64 articles, of which 24 met the inclusion criteria. & Moon, 2014; Rubinstein et al., 1993).
Interobserver agreement expressed as Cohen’s kappa Several studies also reported TMD symptoms of
was 0.70 (absolute agreement: 86%). Two of these art- arthrogenous (TMDa) or myogenous origin (TMDm).
icles, Saldanha, Hilgenberg, Pinto, and Conti (2012) and If, in addition to an overall outcome for TMD, a
Chole and Parker (1992) were based on the same data set TMDa or TMDm symptom was also reported, then
as Hilgenberg, Saldanha, Cunha, Rubo, and Conti these specified outcomes instead of TMD (not specified)
(2012) and Parker and Chole (1995), respectively. Only were used in the meta-analyses. The following strategy
the latter articles were included, as they contained was applied to decide whether TMDa was investigated in
the most relevant information for this review. a study: (a) the authors of the study reported it; (b) if it
Consequently, a total of 22 independent articles were was not reported, then data regarding disc derangement
included in this study (Akhter et al., 2013; Bernhardt were used; (c) if these were not reported, then data
et al., 2004; Bonaconsa et al., 2010; Buergers, regarding pain in temporomandibular joint were used;
Kleinjung, Behr, & Vielsmeier, 2014; Camparis, and (d) if these were missing, then data regarding joint
Formigoni, Teixeira, & De Siqueira, 2005; De Felicio, sounds were used. For TMDm, (a) data regarding myo-
Melchior, Ferreira, & Rodrigues Da Silva, 2008; de- fascial pain (dysfunction) were used; (b) if this was not
Pedro-Herraez, Mesa-Jimenez, Fernandez-de-Las- reported, then Diagnosis Group I.a and I.b of the
Penas, & de-la-Hoz-Aizpurua, 2016; Effat, 2016; Research Diagnostic Criteria for Temporomandibular
Fernandes, de Godoi Goncalves, de Siqueira, & Disorders (RDC/TMD) were used (Dworkin &
Camparis, 2013; Hilgenberg et al., 2012; Khedr et al., LeResche, 1992); (c) if these were not reported, then
2010; Kuttila, Kuttila, Le Bell, Alanen, & Suonpaa, data regarding pain/tenderness on palpation of mastica-
2005; Lee et al., 2016; Park & Moon, 2014; Parker & tory muscles were used; and (d) if these were not
Chole, 1995; Pekkan, Aksoy, Hekimoglu, & Oghan, reported, then data regarding pain in the lower lateral
2010; Peroz, 2003; Pezzoli et al., 2015; Ren & Isberg, face were used.
1995; Rocha & Sanchez, 2007; Rubinstein, Osterberg, Studies were grouped into one of five categories: (a)
Rosenhall, & Johansson, 1993; Tuz, Onder, & Kisnisci, The association between tinnitus and CSD was analyzed
2003). No additional articles were identified from the in five studies (Khedr et al., 2010; Kuttila et al., 2005;
4 Trends in Hearing

Papers retrieved by
database search (n=2139)

Duplicates (n=558)

Total aer duplicates

removed (n=1581)

Excluded on tle/abstract (n=1517)

- No associaon between nnitus and
CSD or TMD was studied

Total eligible for full text

evaluaon (n=64) Excluded on full text evaluaon (n=42)
- No (appropriate) control group (n=24)
- Review /descripve paper (n=7)
- Intervenon study (n=5)
- Too diverse research populaon
(Whiplash trauma, Meniere disease,
different aural symptoms, n=3)
- Duplicate publicaons (n=2)
Studies included (n=22) - Exclusion criteria: trauma (n=1)

Figure 1. Flow chart of study selection.

CSD ¼ cervical spine disorders; TMD ¼ temporomandibular disorders.

Pezzoli et al., 2015; Ren & Isberg, 1995; Rubinstein et al., studies. Random selection of patients and controls was
1993); (b) the association between tinnitus and disorders applied in three studies. In five studies, participants were
in both neck and jaw (CSD plus TMD) in three studies matched for gender and age. In two studies, assessors
(Bonaconsa et al., 2010; Peroz, 2003; Rocha & Sanchez, were blinded. Patients and controls were recruited from
2007); (c) the association between tinnitus and TMD the same population in 16 studies.
(not specified) in six studies (Buergers et al., 2014; De Instruments to assess tinnitus, CSD, or TMD were
Felicio et al., 2008; Effat, 2016; Fernandes et al., 2013; well described in eight studies. In all eight studies, the
Park & Moon, 2014; Pekkan et al., 2010); (d) the asso- RDC/TMD (Dworkin & LeResche, 1992) was applied
ciation between tinnitus and TMDa in 11 studies (Akhter (Buergers et al., 2014; Camparis et al., 2005; De Felicio
et al., 2013; Bernhardt et al., 2004; Camparis et al., 2005; et al., 2008; de-Pedro-Herraez et al., 2016; Fernandes
Hilgenberg et al., 2012; Khedr et al., 2010; Kuttila et al., et al., 2013; Hilgenberg et al., 2012; Pekkan et al.,
2005; Parker & Chole, 1995; Peroz, 2003; Pezzoli et al., 2010; Tuz et al., 2003). Tinnitus was assessed with a
2015; Rubinstein et al., 1993; Tuz et al., 2003); and (e) single question in most of the studies (n ¼ 16). In six
the association between tinnitus and TMDm in seven studies, this question was part of the RDC/TMD
studies (Bernhardt et al., 2004; Camparis et al., 2005; (Buergers et al., 2014; Camparis et al., 2005; De Felicio
Hilgenberg et al., 2012; Peroz, 2003; Pezzoli et al., et al., 2008; Fernandes et al., 2013; Pekkan et al., 2010;
2015; Ren & Isberg, 1995; Tuz et al., 2003). Some studies Tuz et al., 2003). In all other studies (n ¼ 10), tinnitus
considered multiple associations and, as a consequence, was assessed by a single question as part of author-
belonged to more than one category (Table 1). designed questionnaires (nonvalidated). In six studies, a
physician assessed tinnitus. No information about sever-
Quality assessment. The number of quality criteria met by ity of tinnitus was reported.
the studies ranged from 1 to 7 (Table 2). The interobser- Participants were asked to report the presence of pain
ver agreement expressed as Cohen’s kappa was 0.33 in the jaw, neck, and shoulder region by means of
(absolute agreement: 64%). Criteria for study objective, author-designed (nonvalidated) questionnaires in five
population, and group discrimination were fulfilled in 21 studies (Khedr et al., 2010; Kuttila et al., 2005; Peroz,
 Table 1. Overview of Studies Analysing the Association Between Tinnitus and Complaints of Neck, Shoulders, or Temporomandibular Joint in Patients and Controls.
Patients Patients Controls Controls Controls Recruitment Assessment
Author Patientsa recruitedb Patients N (,) age M (SD) Controlsa recruitedb N (,) age M (SD) methodc methodd Outcomea,e Casef Control

Association between tinnitus and CSD

Tinnitus vs. no tinnitus
Rubinstein et al., Tinnitus Community 166 (–) – No tinnitus Community 592 (–) – Quest/Phys Quest/Phys MP in neck 24% –
1993g database database
Ren and Isberg, Tinnitus þ DD Specialized 53 (70%) – No tinnitus þ Specialized 82 (60%) – Quest Quest MP in neck 55% 24%
1995 ipsilateral DD ipsilateral
Kuttila et al., 2005 Tinnitus Community 126 (–) – Tinnitus Community 132 (–) – Quest Quest MP in neck 52% 5%
(>1/month) database (<1/month) database
Khedr et al., 2010 Tinnitus Community 439 (46%) – No tinnitus Community 96 (–) – Quest Quest MP in neck 37% 33%
database database
Pezzoli et al., 2015 Tinnitus þ Specialized 334 (84%) 42 (16) No tinnitus þ Specialized 917 (85%) 48 (16) Quest Palpation MP in neck – –
headache headache or
or facial pain facial pain

CSD vs. No CSD

No studies included
Association between tinnitus and CSD þ TMD
Tinnitus vs. no tinnitus
Peroz, 2003 Tinnitus Specialized 40 (53%) 52 (14) No tinnitus Specialized 35 (60%) 50 (15) Phys Quest Muscle hypertonia 67% 22%
in head, neck or
shoulders
Rocha and Sanchez, Tinnitus Specialized 94 (58%) 53 (–) No tinnitus Peer 94 (58%) 53 (–) Phys Palpation MP in head, jaw, 72% 36%
2007 accompanying neck, or
cases shoulders
Bonaconsa et al., Tinnitus Specialized 40 (25%) 48 (–) No tinnitus Specialized 40 (73%) 43 (–) Quest Palpation MP in head, jaw, 83% 45%
2010 neck, or
shoulders
CSD þ TMD vs. No CSD þ TMD
No studies included
Association between tinnitus and TMD
Tinnitus vs. no tinnitus
Hilgenberg et al., Tinnitus Specialized 100 (84%) 39 (12) No tinnitus Specialized 100 (65%) 34 (10) Phys Phys TMD 85% 55%
2012g (RDC/TMD)
Park and Moon, Tinnitus Community 2,149 (60%) 50 (16)h No tinnitus Community 10,061 (57%) 50 (16)h Quest Quest TMD ?i ?i
2014 database database
TMD vs. No TMD
Tuz et al., 2003g TMD Specialized 200 (83%) 30 (–) No TMD Specialized 50 (54%) 37 (–) Phys Quest Tinnitus 46% 26%
(RDC/TMD) (RDC/TMD)
De Felicio et al., TMD Specialized 20 (100%) 31 (–)h No TMD – 8 (100%) 31 (–)h Phys Quest Tinnitus 60% 25%
2008 (RDC/TMD) (RDC/TMD)
Pekkan et al., 2010 TMD Specialized 25 (16%) 28 (–) No TMD Specialized 20 (15%) 28 (–) Phys/Quest Phys/Quest Tinnitus 52% 0%
(RDC/TMD) (RDC/TMD)
Akhter et al., 2013g TMD Students 543 (28%) 19 (2)h No TMD Students 1,387 (72%) 19 (2)h Quest Quest Tinnitus 39% 6%
<22 years <22 years
Fernandes et al., Painful TMD Specialized 162 (–%) 38 (13)h No TMD nor Specialized 62 (–%) 38 (13)h Quest Quest Tinnitus 88% 12%
2013 painful TMD (RDC/TMD) (RDC/TMD)

5
(continued)
 Table 1. Continued

6
Patients Patients Controls Controls Controls Recruitment Assessment
Author Patientsa recruitedb Patients N (,) age M (SD) Controlsa recruitedb N (,) age M (SD) methodc methodd Outcomea,e Casef Control
h h
Buergers et al., 2014 TMD Specialized 82 (68%) 54 (17) No TMD Specialized 869 (49%) 54 (17) Phys Phys Tinnitus 37% 4%
(RDC/TMD)
Lee et al., 2016g TMD Insurance 7,585 (66%) 45 (16) No TMD General/ 30.340 (66%) 45 (16) Phys Phys Tinnitus ?j ?j
Specialized
Effat, 2016 TMD Specialized 104 (81%) 35 (12) No TMD General 110 (60%) 31 (8) Phys Quest Tinnitus 52% 12%

Association between tinnitus and TMDa

Tinnitus vs. no tinnitus
Rubinstein et al., Tinnitus Community 166 (–) – No tinnitus Community 592 (–) – Quest/Phys Quest/Phys Noises in TMJk 11% –
1993 database database
Peroz, 2003 Tinnitus Specialized 40 (53%) 52 (14) No tinnitus Specialized 35 (60%) 50 (15) Phys Phys Noises in TMJk 23% 1%
Bernhardt et al., Tinnitus Specialized 30 (43%) 41 (–) No tinnitus Community 1,907 (52%) 49 (–) Quest Palpation Pain in TMJ 34% 5%
2004 database
Phys Noises in TMJk 37% 28%
Camparis et al., 2005 Tinnitus þ Specialized 54 (83%) 38 (–) No tinnitus þ Specialized 46 (76%) 34 (–) Quest Phys Pain in TMJ 70% 39%
bruxism bruxism (RDC/TMD) (RDC/TMD)
DD 20% 17%
Kuttila et al., 2005 Tinnitus Community 126 (–%) – Tinnitus Community 132 (–%) – Quest Quest Pain in TMJ 48% 5%
(>1/month) database (<1/month) database

Khedr et al., 2010 Tinnitus Community 439 (46%) – No tinnitus Community 96 (–) – Quest Quest Pain in TMJ 21% 12%
database database
Hilgenberg et al., Tinnitus Specialized 100 (84%) 39 (12) No tinnitus Specialized 100 (65%) 34 (10) Phys Phys Pain in TMJ 53% 24%
2012 (RDC/TMD)
DD þ Clickingk 43% 30%
DD þ No Clicking þ 0% 1%
LMO
DD þ No Clickingk 6% 4%
Arthritis 3% 0%
Arthrosis 1% 1%
Pezzoli et al., 2015 Tinnitus þ Specialized 334 (84%) 42 (16) No tinnitus þ Specialized 917 (85%) 48 (16) Quest Phys DD ?i ?i
headache headache or
or facial pain facial pain
TMD vs. No TMD
Parker and Chole, Pain in Specialized 200 (87%) – No TMD nor General 649 (61%) – Phys Quest Tinnitus 59% 24%
1995 TMJ þ DD pain in TMJ þ DD
Tuz et al., 2003 MP in jaw þ DD Specialized 200 (83%) 30 (–) No TMD Specialized 50 (54%) 37 (–) Phys Quest Tinnitus 42% 26%
(RDC/TMD) (RDC/TMD)
DD 44% 26%
Akhter et al., 2013 Pain in TMJ Students 543 (28%) 19 (2)h No TMD Students 1,387 (72%) 19 (2)h Quest Quest Tinnitus 48% 6%
<22 years <22 years
DD 6% 6%
DD þ Pain in TMJ 55% 6%
DD þ LMO 4% 6%
Pain in 9% 6%
TMJ þ LMO
DD þ Pain in 4% 6%
TMJ þ LMO
(continued)
 Table 1. Continued
Patients Patients Controls Controls Controls Recruitment Assessment
Author Patientsa recruitedb Patients N (,) age M (SD) Controlsa recruitedb N (,) age M (SD) methodc methodd Outcomea,e Casef Control

Association between tinnitus and TMDm

Tinnitus vs. No tinnitus
Ren and Isberg, Tinnitus þ DD General 53 (70%) – No tinnitus þ General 82 (60%) – Quest MP lower lateral 79% 56%
1995g ipsilateral DD ipsilateral face
Peroz, 2003 Tinnitus Specialized 40 (53%) 52 (14) No tinnitus Specialized 35 (60%) 50 (15) Phys Palpation MP in jaw 93% 71%
Bernhardt et al., Tinnitus Specialized 30 (43%) 41 (–) No tinnitus Community 1,907 (52%) 49 (–) Quest Palpation MP in jaw 50% 16%
2004 database
Camparis et al., 2005 Tinnitus þ Specialized 54 (83%) 38 (–) No tinnitus þ Specialized 46 (76%) 34 (–) Quest Phys MP in jaw 85% 48%
bruxism bruxism (RDC/TMD) (RDC/TMD)
Hilgenberg et al., Tinnitus Specialized 100 (84%) 39 (12) No tinnitus Specialized 100 (65%) 34 (10) Phys Phys MP in jaw 32% 22%
2012 (RDC/TMD)
MP in jaw þ LMO 39% 16%
Pezzoli et al., 2015 Tinnitus þ Specialized 334 (84%) 42 (16) No tinnitus þ Specialized 917 (85%) 48 (16) Quest Phys MP in facial or ?i ?i
headache headache or masticatory
or facial pain facial pain muscles
TMD vs No TMD
Tuz et al., 2003 MP in jaw Specialized 200 (83%) 30 (–) No TMD Specialized 50 (54%) 37 (–) Phys Quest Tinnitus 59% 26%
(RDC/TMD) (RDC/TMD)
de-Pedro-Herraez MP in jaw Specialized 31 (100%) 39 (–) No MP in jaw Specialized 31 (100%) 41 (–) Quest Quest Tinnitus 52% 10%
et al., 2016 (RDC/TMD)

Note. CSD ¼ cervical spine disorders; TMJ ¼ temporomandibular joint.

a
TMD ¼ temporomandibular disorder not specified; DD ¼ temporomandibular disc displacements; LMO ¼ limited mouth opening.
b
Recruitment setting: General ¼ general hospital/ENT department; Specialized ¼ specialized tinnitus or TMD clinic/department.
c
Recruitment method: Quest ¼ by questionnaire; Phys ¼ by a physician.
d
Assessment method: RDC/TMD ¼ research diagnostic criteria for temporomandibular disorders (Dworkin & LeResche, 1992).
e
Assessment outcome: MP ¼ myofascial pain.
f
TMDa ¼ TMD arthrogenous; TMDm ¼ TMD myogenous. Peroz (2003) reported ‘‘Verspannungen im hals-, schulter- und oberarm bereich und kaumuskeln’’ (we grouped this under ‘‘hypertonia in head, neck, and
shoulder muscles’’).
g
Not included in meta-analysis as explained in methods and results.
h
Value ¼ overall mean age cases þ controls.
i
Unknown percentage, odds ratios as a result of multivariable logistic regression analyses were presented.
j
Incidence study: In the TMD group (n ¼ 7,585), 362 developed tinnitus, and in the control group (n ¼ 30,340), 530 developed tinnitus; Parker and Chole (1995) analyzed two control groups. We combined the groups.
k
Regarding ‘‘Noises in TMJ’’ and clicking, we assume that the subjects heard subjective tinnitus in addition to sound that the jaw joint might produce, as the authors distinguish between these two percepts in their
discussion; [–] not reported (Dehmel et al., 2008).

7
8 Trends in Hearing

Table 2. Quality Assessment of the Studies.

Quality criteria

Author Year 1 2 3 4 5 6 7 8 9

Rubinstein 1993 þ þ þ þ þ þ – – ?
Parker and Chole 1995 þ – – ? ? ? – – ?
Ren and Isberg 1995 þ þ þ þ þ – – – ?
Peroz 2003 þ þ – þ þ ? – – ?
Tuz et al. 2003 þ þ þ þ þ – – þ ?
Bernhardt et al. 2004 þ þ þ – þ – – þ ?
Camparis et al. 2005 þ þ þ þ þ ? – þ ?
Kuttila et al. 2005 þ þ þ þ þ þ – – ?
Rocha and Sanchez 2007 þ þ þ þ þ – þ þ –
De Felicio et al. 2008 þ þ ? þ þ ? – þ ?
Bonaconsa et al. 2010 – þ ? þ þ ? þ þ –
Khedr et al. 2010 þ þ þ þ þ – þ þ ?
Pekkan et al. 2010 þ þ – þ þ ? – þ ?
Hilgenberg et al. 2012 þ þ þ þ þ ? – þ þ
Akhter et al. 2013 þ þ þ þ þ – – – ?
Fernandes et al. 2013 þ þ þ þ þ – – þ þ
Buergers et al. 2014 þ þ þ – þ – – þ ?
Park and Moon 2014 þ þ þ þ þ – – þ ?
Lee et al. 2016 þ þ þ þ þ þ þ ? ?
Pezzoli et al. 2015 þ þ þ þ þ – – þ ?
de-Pedro-Herraez et al. 2016 þ þ þ þ þ – þ ? ?
Effat 2016 þ þ – þ þ – – – ?
Note. 1. Was the research question or objective in this article clearly stated and appropriate? 2. Was the study population clearly specified and defined? 3.
Were controls selected or recruited from the same or similar population that gave rise to the cases (including the same timeframe)? 4. Were the definitions,
inclusion, and exclusion criteria used to identify or select cases and controls valid, reliable, and implemented consistently across all study participants? 5.
Were the cases clearly defined and differentiated from controls? 6. Were the cases and controls randomly selected? 7. Were controls matched to cases on
one or more attributes? 8. Were the measures of exposure clearly defined, valid, reliable, and implemented consistently across all study participants? 9.
Were the assessors blinded to the case or control status of participants? [þ] Yes, [–] No, [?] cannot be determined/unclear/not reported (modified version
of Quality Assessment of Case-Control Studies, 2014).

2003; Ren & Isberg, 1995; Rubinstein et al., 1993) or tinnitus but also about CSD. Because no data of CSD
RDC/TMD (Buergers et al., 2014; Camparis et al., were reported in the controls, these data were also not
2005; De Felicio et al., 2008; Fernandes et al., 2013; included in the meta-analysis.
Hilgenberg et al., 2012; Pekkan et al., 2010; Tuz et al.,
2003). In the other studies, participants were asked to Tinnitus and CSD. One study (Khedr et al., 2010) did
report pain provoked during physical examination of not and three studies did find a significant association
that region, such as assessment of myofascial trigger between myofascial pain in the neck region and tinnitus.
points (TrPs; Simons, Travell, & Simons, 1999). In one All studies investigated CSD in patients with and with-
study, a physician was trained to deliver a standardized out tinnitus. The study-size weighted odds ratios ranged
finger pressure for evaluating TrPs (Bernhardt et al., from 1.2 to 10.9, with an overall odds ratio of 2.6 (95%
2004). In another study, an algometer was used for CI [1.1, 6.4]; Figure 2).
assessment of TrPs (Hilgenberg et al., 2012).
Tinnitus and CSD plus TMD. All three studies analyz-
Meta-analysis. The results of Lee et al. (2016) were ing the association between tinnitus and CSD plus TMD
reported as hazard ratios (tinnitus with and without found a significant association between myofascial com-
TMD, Crude HR ¼ 2.73, p < .001) instead of odds plaints in head, jaw, neck, or shoulders. All studies inves-
ratios and were not included in the meta-analysis. tigated CSD plus TMD in patients with and without
Rubinstein et al. (1993) reported not only significant dif- tinnitus. All patients were recruited from specialized hos-
ferences in TMD between patients with and without pitals. Of these patients, 67% to 83% perceived tinnitus.
Bousema et al. 9

Figure 2. Forest plot of the association between tinnitus and CSD or TMD differentiated into five categories.
Adjusted odds ratios: To adjust for potential publication bias, Duval and Tweedie’s (2000) nonparametric trim-and-fill approach to impute
theoretical missing studies was applied.
CSD ¼ cervical spine disorders; TMD ¼ temporomandibular disorders; TMDa ¼ TMD arthrogenous; TMDm ¼ TMD myogenous.

The study-size weighted odds ratios ranged from 4.9 to 2016; Fernandes et al., 2013). Overall, 37% to 88% of
7.0, with an overall odds ratio 5.5 (95% CI [3.4, 9.0]). patients with TMD who were recruited from specialized
TMD clinics perceived tinnitus. The study-size weighted
Tinnitus and TMD (not specified). All studies but one odds ratios ranged from 1.7 to 44.3, with an overall odds
(De Felicio et al., 2008) found an association between ratio of 6.7 (95% CI [2.4, 18.8]).
tinnitus and TMD (not specified). One study investigated
TMD in patients with and without tinnitus (Park & Tinnitus and TMDa. Eight out of 11 studies found a
Moon, 2014). Conversely, five studies investigated tin- significant association between tinnitus and TMDa. Of
nitus in patients with and without TMD (Buergers the patients who were recruited from specialized TMD
et al., 2014; De Felicio, De Oliveira, Nunes, Jeronymo, clinics, 20% to 59% perceived tinnitus; when recruited
& Ferreira-Jeronymo, 1999; De Felicio et al., 2008; Effat, elsewhere, 21% to 48% perceived tinnitus. Eight studies
10 Trends in Hearing

investigated TMDa in patients with and without tinnitus tinnitus more frequently experienced TMD than sub-
(Bernhardt et al., 2004; Camparis et al., 2005; Hilgenberg jects without tinnitus, and, vice versa, patients with
et al., 2012; Khedr et al., 2010; Kuttila et al., 2005; Peroz, TMD experienced tinnitus more frequently compared
2003; Pezzoli et al., 2015; Rubinstein, 1993). Conversely, with subjects without TMD. For CSD, the results
three studies examined tinnitus in patients with and with- only revealed a unidirectional relationship. Thus,
out TMDa (Akhter et al., 2013; Parker & Chole, 1995; patients with tinnitus more frequently reported CSD.
Tuz et al., 2003). Temporomandibular disc displace- None of the included studies reported on the reverse
ments was investigated in four studies (Akhter et al., relation, that is, whether patients with CSD have an
2013; Camparis et al., 2005; Hilgenberg et al., 2012; increased probability to experience tinnitus. Meta-ana-
Pezzoli et al., 2015), while pain or noises in the TMJ lysis showed that patients with tinnitus have an average
were studied in the other studies. The study-size weighted of 2.6 and 6.7 times greater risk of reporting CSD or
odds ratios ranged from 1.2 to 9.9, with an overall odds TMD, respectively.
ratio 2.3 (95% CI [1.5, 3.6]).
Bias and Quality Assessment
Tinnitus and TMDm. All seven studies found a signifi-
cant association between tinnitus and TMDm. These Almost all studies reported a significant association
studies examined myofascial pain in the jaw region. between tinnitus and CSD or TMD, which may suggest
Five studies investigated TMDm in patients with and a risk of publication bias. This bias seems to be con-
without tinnitus (Bernhardt et al., 2004; Camparis firmed by the absence of data points on the left side of
et al., 2005; Hilgenberg et al., 2012; Leher, Dietrich, & the funnel plots in Figure 3(b), (c), and (e). When theor-
Peroz, 2003; Pezzoli et al., 2015). One study investigated etical missing studies were imputed, the adjusted odds
tinnitus in patients with and without TMDm (Tuz et al., ratios for these items reduced, but an association per-
2003). Patients were recruited from specialized TMD sisted. In Figure 3(d), one theoretical missing study is
clinics. The study-size weighted odds ratios ranged imputed in the right side of the funnel plot causing a
from 1.3 to 10.0, with an overall odds ratio of 4.1 minimum increment of the adjusted odds ratio. This
(95% CI [2.1, 8.1]). might be caused by a systematic difference between the
Finally, three studies investigated laterality between studies of higher precision and the only study of lower
unilateral tinnitus and unilateral TMD (Buergers et al., precision. In the analysis, one outlier was found with an
2014; Ren & Isberg, 1995; Rocha & Sanchez, 2007). In odds ratio of 44.3 (Pekkan et al., 2010). Quality assess-
two studies, all the participants had both conditions on ment could not sufficiently explain this outlier, except
the same side (Buergers et al., 2014; Ren & Isberg, 1995), that the sample size was small.
while the contralateral TMJ region was asymptomatic in The methodological quality assessment showed that
94% (Ren & Isberg, 1995). The third study found an only in a few studies were the assessors blinded (2/22)
association of laterality in 56.5% (p > .001) of the and the patients and controls randomly selected (3/22) or
patients between the tinnitus side (or the side with the matched for gender and age (5/22; Table 2). Despite this
worst tinnitus) and the side of the body with most TrPs shortcoming, no studies found a significant difference
(Rocha & Sanchez, 2007). regarding distribution of gender or mean age between
comparison groups. Further, in some studies, patients
Publication bias. Based on the funnel plots (Figure 3(a) and controls were not recruited from the same popula-
to (e)), publication bias was suggested regarding the tion. For instance, patients visiting a specialized TMD
association between tinnitus and CSD/TMD, TMD clinic were compared with controls visiting a dentist for
(not specified), and TMDm. The overall odds ratio minimal dental care. Consequently, recruitment from
reduced after trim and fill from 5.5 to 4.9 for the associ- different populations may result in differences between
ation with CSD/TMD, from 6.7 to 4.5 for the associ- groups that influence outcomes. To analyze effects of
ation with TMD (not specified), and from 4.1 to 3.3 quality, we initially intended to perform a meta-regres-
for the association with TMDm (Duval & Tweedie, sion to explore associations between quality criteria of
2000). studies and their outcomes. After reviewing the results,
however, we decided to refrain from meta-regression
because quality criteria were either met in the vast major-
Discussion ity of studies or not met, resulting in a skewed distribu-
tion between studies.
Summary of Main Results Instead of a validated questionnaire such as the
In the majority of the studies, a significant association Tinnitus Handicap Inventory (Newman, Jacobson, &
between tinnitus and TMD was identified. This rela- Spitzer, 1996), tinnitus was often assessed by means of
tionship is bidirectional meaning that, patients with a single question as part of the RDC/TMD or other
Bousema et al. 11

Figure 3. Funnel plots of studies regarding association between tinnitus and CSD or TMD. (a) Association between tinnitus and CSD;
(b) association between tinnitus and CSD and TMD; (c) association between tinnitus and TMD (not specified); (d) association between
tinnitus and TMD (arthrogenous); (e) association between tinnitus and TMD (myogenous).
[o] ¼ Studies included.
[] ¼ Imputed studies to adjust a summary odds ratio in light of these ‘‘missing’’ studies, compensating for the risk of publication bias (Duval
& Tweedie, 2000).
Open and closed rhombuses represent the mean log odds ratios before and after study imputation, respectively (Duval & Tweedie, 2000).
CSD ¼ cervical spine disorders; TMD ¼ temporomandibular disorders.

questionnaire. Thus, only information on the presence, value, but with an acceptable absolute agreement. After
and not about the severity, of tinnitus was provided. It is discussion, however, consensus was reached on all topics.
therefore unclear whether severity of tinnitus affected the Classifying studies according to their risk of bias was con-
associations. sidered, but it was impossible to state at which level and in
As only one author screened abstracts, titles, and which direction the individual quality items contributed to
selected full texts, studies may have been missed. To a study’s risk of bias. Therefore, the results of methodo-
reduce the chance of missing studies, references of the logical quality assessment are described.
included studies were checked. In exploring the association between tinnitus and
We used a modified version of Quality Assessment of TMD, we combined studies recruiting patients with tin-
Case-Control Studies for methodological quality assess- nitus in a TMD clinic and studies recruiting patients with
ment of case-control, cross-sectional, and cohort studies. TMD in a tinnitus clinic. This might have induced selec-
A negative feature of this tool was that the quality criteria tion bias, but as the association was bidirectional, this
were widely interpretable, which resulted in a low kappa analysis did not appear to influence results.
12 Trends in Hearing

The majority of the studies exploring the association and CSD and TMD (Dehmel, Cui, & Shore, 2008). In
between TMD and tinnitus are of acceptable quality, and addition, in case of cochlear damage, this connection is
almost all found an association between TMD and tin- upregulated, as over a time interval of days after reduced
nitus. However, we found no high-quality studies, as auditory nerve input, responses to somatosensory stimu-
each study had at least one critical unfilled individual lation are heightened (Shore, Roberts, & Langguth,
quality criterion, such as lack of blinding or compar- 2016). The interaction between both systems might
ability of the groups, which could have contributed explain why tinnitus sufferers can modulate the loudness
to a study’s risk of bias. Based on the Grading of and pitch of their tinnitus (Ralli et al., 2016; Shore et al.,
Recommendations Assessment, Development and 2016). It is also conceivable that based on stochastic res-
Evaluation level of evidence scale, we qualified the over- onance, the somatosensory input may lead to the devel-
all level of evidence for this association as low (Grading opment of subjective tinnitus, as it may lift subthreshold
of Recommendations Assessment, Development and auditory nerve input to the CN above detection thresh-
Evaluation, 2017). old (Krauss et al., 2016).
In addition, we found no high-quality studies explor- The association between tinnitus and CSD or TMD is
ing the association between CDS and tinnitus. In con- mostly ipsilateral (Buergers et al., 2014; Ren & Isberg,
trast to the good clinometric properties of the instrument 1995; Rocha & Sanchez, 2007). This suggests that neural
assessing TMD, CSD was assessed only by means of interactions between CSD or TMD and tinnitus are
author-designed questionnaires or by examination for based on neural circuits that are sensitive to (mostly)
tenderness or TrPs. The latter was almost always per- ipsilateral stimuli. This is consistent with the functional
formed by means of palpation and only once by means connections between the spinal trigeminal nucleus and
of pressure algometry. Therefore, we also qualified the the CN, which are both located peripheral to major
overall level of evidence for this association as low. neural decussations in the brainstem (Gelfand, 2009;
Somayaji & Rao, 2014). Thus, the possible ipsilateral
association between tinnitus and CSD or TMD is con-
Explanatory Models sistent with a cross-modal mechanism between the tri-
A frequently described explanation for subjective som- geminal systems and the CN.
atosensory tinnitus is that a TMJ disorder (e.g., disc dis- To better understand a possible underlying mechan-
placement) or hypertonia of the masticatory muscles ism, further exploration of the association between tin-
might influence middle ear muscle tension or ventilation nitus and CSD or TMD is needed. This could include not
through an anatomical connection (e.g., the tensor only the relationship of CSD or TMD to unilateral tin-
veli palatini, the eustachian tube, or several ligaments). nitus but also the different symptoms of TMD, such as
These influences would generate afferent signals that disc derangement and pain, in relation to tinnitus.
would—via the cochlear nerve—influence the auditory
pathways (for review, see Ramirez et al., 2008).
However, as tinnitus and its somatosensory modulation
Clinical Implications
can persist after cutting the system off at the auditory This review implies that physical examination of the
nerve (D. M. Baguley, Axon, Winter, & Moffat, 2002; TMJ and the neck region may help explain some phe-
House & Brackmann, 1981), these peripheral explan- nomena described by patients with tinnitus. However,
ations cannot provide the sole explanation. Recently, our study does not provide information on possible
studies have shown anatomical and functional connec- effects of treatment of CSD or TMD on tinnitus.
tions between the trigeminal and dorsal column systems Nevertheless, explaining the existence of a possible asso-
of the somatosensory system and the cochlear nucleus ciation to the patient might support the patient’s ability
(CN) of the auditory system in the medulla oblongata to understand and cope with tinnitus.
(Shore & Zhou, 2006). The spinal trigeminal nucleus
receives nociceptive and proprioceptive input from the
Recommendations
head, face, oral structures, TMJ, and cervical spine
(C1–C3) and projects to the CN (Shore, 2011). A pos- Future studies investigating the association of tinnitus
sible functional role of the auditory-somatosensory inter- with CSD or TMD should focus on improving methodo-
actions involves the differentiation between external logical quality, such as blinding and ensuring compar-
auditory signals and those generated by the body itself ability of groups, and using validated instruments for
(Shore, 2005). This functional connection in the brain- diagnosing tinnitus and symptoms of CSD. CSD and
stem between the auditory and somatosensory system TMD should also be evaluated on the side corresponding
might mediate an association between subjective tinnitus to the lateralization of the perceived tinnitus.
Bousema et al. 13

Conclusion Buergers, R., Kleinjung, T., Behr, M., & Vielsmeier, V. (2014).
There is weak evidence for an association between sub- Is there a link between tinnitus and temporomandibular
jective tinnitus and CSD and a bidirectional association disorders? Journal of Prosthetic Dentistry, 111(3), 222–227.
between subjective tinnitus and TMD. However, the doi:10.1016/j.prosdent.2013.10.001
Camparis, C. M., Formigoni, G., Teixeira, M. J., & De
association between subjective tinnitus and CSD/TMD,
Siqueira, J. T. T. (2005). Clinical evaluation of tinnitus in
TMD (not specified), and TMDm may be overestimated patients with sleep bruxism: Prevalence and characteristics.
due to publication bias in the available studies. Journal of Oral Rehabilitation, 32(11), 808–814. DOI:
10.1111/j.1365-2842.2005.01519.x.
Declaration of Conflicting Interests Chole, R. A., & Parker, W. S. (1992). Tinnitus and ver-
The authors declared no potential conflicts of interest with tigo in patients with temporomandibular disorder.
respect to the research, authorship, and/or publication of this Archives of Otolaryngology - Head and Neck Surgery,
article. 118(8), 817–821.
Davis, A., & El Rafaie, A. (2000). Epidemiology of tinnitus. In
Funding R. S. Tyler (Ed.), Tinnitus handbook (pp. 1–23). San Diego,
The authors received no financial support for the research, CA: Singular, Thomson Learning.
authorship, and/or publication of this article. De Felicio, C. M., De Oliveira, J. A. A., Nunes, L. D. J.,
Jeronymo, L. F. G., & Ferreira-Jeronymo, R. R. (1999).
Ear symptoms related to tinnitus in otological and temporo-
ORCID iD
mandibular joint disorders. Revista Brasileira de
E. J. Bousema http://orcid.org/0000-0002-6819-3078 Otorrinolaringologia, 65(2), 141–146.
De Felicio, C. M., Melchior, M. D. O., Ferreira, C. L. P., &
Supplemental Material Rodrigues Da Silva, M. A. M. (2008). Otologic symptoms
Supplemental material for this article is available online. of temporomandibular disorder and effect of orofacial
myofunctional therapy. Cranio: The Journal of
Craniomandibular Practice, 26(2), 118–125. DOI: 10.1179/
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