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Journal of Cranio-Maxillo-Facial Surgery 48 (2020) 942e955

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Review

Prevalence of degenerative disease in temporomandibular disorder


patients with disc displacement: A systematic review and meta-
analysis
Maria Alves Garcia Silva a, *, Letícia Lopes Quirino Pantoja b,
Kamile Leonardi Dutra-Horstmann c, Jose  Valladares-Neto d, Felipe Lucyk Wolff e,
 Luís Porporatti , Eliete Neves Silva Guerra g, Graziela De Luca Canto h
Andre f

a
Department of Stomatological Sciences, Faculty of Dentistry, Federal University of Goia s, Goia^nia, Goia
s, Brazil
b
Laboratory of Oral Histopathology, Health Sciences Faculty, University of Brasília, Brasília, DF, Brazil
c
Brazilian Centre for Evidence-Based Research, Federal University of Santa Catarina, Florianopolis, Santa Catarina, Brazil
d s, Goia
Department of Orthodontics, Faculty of Dentistry, Federal University of Goia ^nia, Goias, Brazil
e polis, Santa Catarina, Brazil
Private Practice, Floriano
f
Brazilian Centre for Evidence-Based Research, Department of Dentistry, Federal University of Santa Catarina, Florianopolis, Santa Catarina, Brazil
g
Laboratory of Oral Histopathology, Health Sciences Faculty, University of Brasília, Brasília, Brazil
h
Department of Dentistry, Federal University of Santa Catarina, Florianopolis, Santa Catarina, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: To assess the available literature on the prevalence of degenerative joint disease (DJD) in patients with
Paper received 4 March 2020 anterior disc displacement (ADD) of the temporomandibular joint (TMJ), using a systematic review with
Accepted 16 August 2020 meta-analysis.
Available online 25 August 2020
Search strategies were performed in the following databases: PubMed/MEDLINE, EMBASE, LILACS,
Web of Science, Scopus, and LIVIVO. A search was also carried out in the gray literature. Two independent
Keywords:
reviewers selected the included articles using a two-phase process based on the eligibility criteria. Three
Temporomandibular joint
reviewers independently collected the required information from the included articles. The methodo-
Disc displacement
Degenerative joint disease
logical quality of the selected studies was assessed individually.
Systematic review In accordance with the inclusion and exclusion criteria, 1349 studies were found and 18 articles were
Evidence-based dentistry included. The total sample size was 3158 TMJs. The sex distribution was predominant for females (1161
females and 345 males). The average age was 46 (range 10e82) years. Among the 1762 TMJs quantita-
tively assessed, the prevalence of DJD involving disc displacement with reduction (DDWR) was 35%,
while for disc displacement without reduction (DDWoR) the prevalence was 66%. The prevalences of
different features of DJD were as follows: sclerosis 24.3%, erosion 23.5%, osteophyte 17.9%, and subcortical
cyst 7.6%.
The prevalence of DJD in temporomandibular disorder patients with disc displacement is around 50%
and is higher in DDWoR (66%) than in DDWR (35%). Sclerosis and erosion would be the most expected
radiological signs in a developing DJD. Clinicians should adequately address the frequent DJD features
associated with disc displacement in terms of diagnostics and therapeutic management.
© 2020 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights
reserved.

1. Introduction

Degenerative joint disease (DJD) of the temporomandibular


joint (TMJ) is characterized by ‘deteriorations of articular tissue
* Corresponding author. Department of Oral Sciences and Oral Radiology, School with concomitant osseous changes in the condyle and/or articular
s, Av. Universita
of Dentistry, Federal University of Goia ria Esquina com 1a Avenida s/ eminence’ (Schiffman et al., 2014). The terms osteoarthritis and
n, Setor Universitario, CEP 74605-220, Goi^ ania, Goi
as, Brazil. Fax: þ55 62 3209 osteoarthrosis are subclasses of DJD, implying the presence and
6067. absence of pain, respectively. Although crepitus detected with
E-mail addresses: mariaagsilva@gmail.com, mags@ufg.br (M.A.G. Silva).

https://doi.org/10.1016/j.jcms.2020.08.004
1010-5182/© 2020 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
M.A.G. Silva et al. / Journal of Cranio-Maxillo-Facial Surgery 48 (2020) 942e955 943

palpation is suggestive of DJD, the diagnosis should be confirmed Protocols (PRISMA-P) statement was prepared (Shamseer et al.,
by imaging (Schiffman et al., 2014). Cone beam computed tomog- 2015). This protocol was registered with the International Pro-
raphy (CBCT) is becoming the reference standard for the evaluation spective Register of Systematic Reviews (PROSPERO) under number
of osseous components of the TMJ (Larheim et al., 2015; CRD42018105979. This systematic review was also reported ac-
Hilgenberg-Sydney et al., 2018). Osseous changes in the DJD are cording to PRISMA (Moher et al., 2009).
identified by at least one of the following changes: erosion, sub-
chondral cyst, generalized sclerosis, or osteophyte (Ahmad et al.,
2.2. Focus question
2009). The bony changes are most commonly seen in the
condyle; however, they may also involve the mandibular fossa or
This systematic review was performed to address the following
articular eminence. Flattening and cortical sclerosis have been
questions: (1) What is the prevalence of degenerative joint disease
considered an adaptive change rather than a DJD (Schiffman et al.,
in patients with anterior disc displacement? (2) What is the prev-
2014). In contrast, magnetic resonance imaging (MRI) is considered
alence of each osseous change d for instance, erosion, osteophyte,
the reference standard for the evaluation of disc displacement and
sclerosis, and subcortical cyst?
other soft tissues related to the TMJ (Pupo et al., 2016).
We selected studies using the following PICOS acronym as a
The association between DJD and anterior disc displacement
guide. (1) Population: children, adolescents or adults. (2) Inter-
(ADD) has been investigated in several studies (Emshoff et al., 2002a,
vention/exposition: a degenerative disease in TMJ with disc DDWR
s
2002b; Alexiou et al., 2009; Dias et al., 2012; Melo et al., 2015; Corte
or DDWoR. (3) Comparison or control: not applicable. (4) Outcome:
et al., 2016). ADD is a common internal derangement of the TMJ,
primary outcome d prevalence of the DJD; secondary outcome d
which is usually reported in young to middle-aged female adults
prevalence of each osseous change (erosion, osteophyte, sclerosis,
(20e50 years of age), with a tendency for more advanced stages of
and subcortical cyst). (5) Studies included: observational studies.
ADD with increasing age (Alexiou et al., 2009; Melo et al., 2015). ADD
is classified as disc displacement with reduction (DDWR) or disc
displacement without reduction (DDWoR). 2.3. Eligibility criteria
Studies have also investigated the prevalence of, and association
between, DDWR or DDWoR and pain, jaw locking, and limited mouth 2.3.1. Inclusion criteria
opening (Emshoff et al., 2002a; Dias et al., 2012; Hasan and Observational studies that assessed the prevalence of DJD with
Abdelrahman, 2014; Moncada et al., 2014; Corte s et al., 2016). ADD were included. Only studies that diagnosed ADD by MRI were
Changes in dentofacial morphology have also been evaluated, with assessed. No restrictions on the publication period or language
perhaps more serious consequences expected in a younger population were applied.
with DDWoR and DJD, including limited mandibular growth or hori-
zontal mandibular and vertical ramus deficiency (Bertram et al., 2011;
2.3.2. Exclusion criteria
Roh et al., 2012), as well as an important determinant factor of back-
The studies were excluded in two phases.
ward mandibular positioning and/or clockwise rotation (Emshoff
In phase 1 (titles and abstracts), the following exclusion criteria
et al., 2011). Osseous changes related to DJD are important signs that
were applied: (1) studies conducted in animals or in vitro; (2)
need to be considered in diagnosing temporomandibular disorder
studies that did not investigate the prevalence of, or association
(TMD) (Hilgenberg-Sydney et al., 2018), a disease that affects 5e12% of
between, DJD and TMJ disc displacement; (3) studies with different
the population (National Institute of Dental and Craniofacial
image modalities, such as panoramic radiographs, or without any
Research). The hypothesis that DJD is a progression of previous disc
images; (4) studies related to the treatment of TMJ disorders; (5)
displacement has often been proposed (Emshoff et al., 2001; Larheim
studies involving patients with systemic articular disease; (6) re-
et al., 2001), particularly in cases of DDWoR. On the other hand, some
views, letters, conference abstracts, editorials, case reports, case-
authors have not found an association between ADD and DJD (Emshoff
series studies, and guidelines.
et al., 2002a,
In phase 2 (full-text), the following additional exclusion criteria
2002b,bib_Emshoff_et_al_2002a,bib_Emshoff_et_al_2002b; Kurita
were applied: (1) studies published twice; (2) studies in which only
et al., 2006).
CT/CBCT were performed.
A recent systematic review (Pantoja et al., 2018) reported a high
prevalence of DJD either in patients with a systemic rheumatic
disease (ranging from 40.42% to 93.33%) or in patients with TMD 2.4. Information sources
without systemic involvement (ranging from 18.01% to 84.74%). For
this reason, clinicians should not neglect the relationship between Detailed search strategies for each of the following biblio-
ADD and DJD; however, this relationship is not completely graphic databases were developed: PubMed/MEDLINE, EMBASE,
understood. LILACS, Web of Science, Scopus, and LIVIVO. The database search
To the best of our knowledge, there has not been a systematic strategies can be found in Appendix 1. Partial gray literature
review that has addressed the prevalence of DJD in patients with searches through Google Scholar, OpenGrey, and ProQuest were
disc displacement. Therefore, the aim of this systematic review and also performed. The Google Scholar search was limited to the first
meta-analysis was to determine the prevalence of the degenerative 100 most relevant articles published in the last 10 years. Refer-
joint disease in TMD patients with anterior disc displacement, and ences were managed using EndNoteR X7 (Thomson Reuters,
also the prevalence of each type of osseous change, such as erosion, Philadelphia, PA), and duplicates were removed using Rayyan
osteophyte, sclerosis, and subcortical cyst. (Qatar Computing Research Institute, Doha, Qatar) (Ouzzani et al.,
2016). Furthermore, hand searches were performed on the refer-
2. Materials and methods ence lists of included articles.
Both the gray literature searches and electronic database
2.1. Protocol and registration searches were conducted from their coverage starting date to May
11, 2020. Three experts were chosen from the authors who pub-
A systematic review protocol based on the 2015 Preferred lished the most relevant papers, and an email was sent asking for
Reporting Items for Systematic Reviews and Meta-Analyses additional references.
944 M.A.G. Silva et al. / Journal of Cranio-Maxillo-Facial Surgery 48 (2020) 942e955

Fig. 1. Flow diagram of literature search and selection criteria.

2.5. Study selection a final decision. The final selection was always based on the full text
of each publication.
In phase 1, two reviewers (MAGS and FLW) independently
reviewed the titles and abstracts of all the identified electronic 2.6. Data items and collection process
database citations. Articles that did not match the inclusion criteria
were discarded. In phase 2, the same two reviewers (MAGS and Three reviewers (MAGS, JV-N, and KLDH) independently
FLW) applied the inclusion criteria to the full texts of the articles. collected the required information from the included articles using
This blind process was ensured and registered through using a predetermined extraction form. The following data were collected
Rayyan (Ouzzani et al., 2016). The reference lists of the selected from each article: study characteristics (authors, year of publica-
studies were then critically assessed. Any disagreement in the first tion, country, and study design); population characteristics (sample
or second phase was resolved by discussion until a mutual agree- size, age of participants, and sex); intervention (type of imaging
ment between the two authors was attained. When they did not assessment, criteria for ADD and DJD); and outcome characteristics
reach a consensus, a third author (KLDH) became involved to make (main results and conclusions). Again, any disagreement in either
Table 1
Summary of descriptive characteristics of included articles.

Author, year, Study design Sample (N, Settings Age in years, mean Imaging Data collection Criteria for ADD Criteria for DJD Main results Conclusions
country female/male (range) analysis (CT, (calibration/ diagnosis diagnosis
(nTMJ) CBCT, or MRI) reproducibility)

Alkhader et al., Observational 55 University hospital 41 (13e69) MRI (1.5 T) Two calibrated DDWR and Erosion, deformity, DJD ¼ 14.28% (in ADDWoR or disc
2010, Japan descriptive 31/24 (106 TMD patients CBCT observers DDWoR sclerosis, ankyloses, DDWR) deformity on MRI
TMJ) Disagreements by flattening, DJD ¼ 81.63% (in are at risk of having
consensus osteophyte DDWoR) osseous
Inter-examiner Erosion ¼ 42% abnormalities in
concordance: good Sclerosis ¼ 40% the TMJ, and
(0.60e0.74) Osteophytes ¼ 13%further
examination with
CBCT is
recommended
Badel et al., 2012, Cross-sectional 30 with OA Department of 52.6 (19e82) MRI NI DDWR and Flattening, DJD ¼ 43.33% (in DJD is associated

M.A.G. Silva et al. / Journal of Cranio-Maxillo-Facial Surgery 48 (2020) 942e955


Croatia 25/5 (60 TMJ) prosthodontics Control: CT DDWoR deformity, ADD) with DDWoR,
TMD patients and 23.5 (21e27) sclerosis, although DJD may
control osteophyte, develop in joints
subcortical cyst with physiological
disc position
Bolzan, 2002, Brazil Observational 51 Clinical files and 40 (18e62) MRI NI DDWR and Sclerosis, cyst, DJD ¼ 43% (in ADD) There is a strong
descriptive 46/5 (102 TMJ) MRI DDWoR osteophyte, erosion correlation
TMD patients between DJD and
disc displacement
Butzke et al., 2007, Observational 37 with TMD MRI files from NI MRI One calibrated DDWR and Deformity, DJD ¼ 27.1% (in DJD is significantly
Brazil descriptive (65 TMJ) occlusion discipline examiner DDWoR flattening, sclerosis, DDWR) more frequent in
TMD patients Two times (15 days osteophyte, erosion DJD ¼ 70.6% (in cases with
interval) DDWoR) ADDWoR
Intra-examiner
concordance:
accepted (0.7)
s et al., 2016,
Corte Observational 180 MRI/CT files 33.4 (16e65) MRI Intra-examiner DDWR and Flattening, erosion,DJD ¼ 20.27% (in There is a
Chile descriptive 179/39 (360 TMD patients Groups: CT concordance: 0.86 DDWoR deformity, DDWO) significant
TMJ) 16e25 osteophyte, cyst DJD ¼ 31.11% (in association
26e35 DDWoR) between DDWoR
36e45 Erosion ¼ 25% and DJD in
46e55 Osteophyte ¼ 3% symptomatic
56e65 Subchondral patients with TMD
cyst ¼ 8% (p < 0.001)
Dias et al., 2012, Observational 112 MRI files from (18e70) MRI One trained and DDWR and Condylar bone Disc displacement/ Disc displacement
Brazil descriptive 91/21 (224 radiology TMD calibrated DDWoR changes: flattening, DJD OR ¼ 3422 (in is correlated with
TMJ) patients examiner osteophyte, general); DJD, particularly in
Intra-examiner erosion, sclerosis, OR ¼ 2.737 (DDWR) cases of DDWoR
concordance:  combined OR ¼ 8.250
0.60 degenerative (DDWoR)
changes
Emshoff et al., 2001 Observational 48 Oral surgery and 35.3 (12e79) MRI NI DDWR and Flattening, DJD ¼ 7.4% (in DDWoR is related
Austria descriptive 40/8 (96 TMJ) oral radiology DDWoR sclerosis, surface DDWR) to DJD, however,
departments irregularities, DJD ¼ 72.2% (in while emphasizing
TMD patients erosion, osteophyte DDWoR) that disc
displacement and
DJD may not be
regarded as the
unique and
dominant factor
(continued on next page)

945
Table 1 (continued )

946
Author, year, Study design Sample (N, Settings Age in years, mean Imaging Data collection Criteria for ADD Criteria for DJD Main results Conclusions
country female/male (range) analysis (CT, (calibration/ diagnosis diagnosis
(nTMJ) CBCT, or MRI) reproducibility)

Gil et al., 2012, Observational 74 TMD patients Female: 40.4 (13 MRI Two experienced DDWR and TMJ and temporal DJD ¼ 5.3% (in DJD in the articular
Brazil descriptive 51/23 (148 e69) radiologists (one DDWoR components: DDWR) eminence and the
TMJ) Male: 35.9 (17e58) doctor, one dentist) osteophyte, DJD ¼ 35.2% (in combination of
sclerosis or erosion DDWoR) erosion and
osteophytes in the
condyle are related
to DDWR
Grossmann et al., Observational 100 Diagnostic clinic 49.48 (18e82) MRI One experienced DDWR and Osteophyte, DJD ¼ 9.4% (in Possible
2016, Brazil descriptive 81/19 (200 TMD patients radiologist DDWoR flattening of the DDWR) relationship of
TMJ) condyle, erosion, DJD ¼ 55.7% (in cause and effect
and bone marrow DDWoR) between
edema osteophytes and

M.A.G. Silva et al. / Journal of Cranio-Maxillo-Facial Surgery 48 (2020) 942e955


DDWoR
Hasan and Observational 53, Diagnostic 25.9 (19e43) MRI (1.5 T) NI DDWR and More than one of DJD ¼ 43.2% (in There is a direct
Abdelrahman, descriptive 36/17 (106 radiology DDWoR the following DDWR) relationship
2014, Egypt TMJ) department changes were DJD ¼ 60% (in between the degree
TMD patients noted: flattening, DDWoR) of ADD and other
subcortical Risk of TMJ and soft tissue
sclerosis or cyst, degenerative and bone
erosion, changes increased abnormalities
osteophytes, and significantly in
generalized joints with ADD
sclerosis Compared with
normal:
OR ¼ 1.8 (partial
DDWR)
OR ¼ 3.6 (partial
DDWoR)
OR ¼ 4.8 (complete
DDWR)
OR ¼ 6.2 (complete
DDWoR)
Kurita et al., 2000, Observational 130 TMD clinic 30.7 (16e80) MRI One trained DDWR and Erosion, flattening, DJD ¼ 42.35% (in The prevalence of
Japan descriptive 107/23 (170 Probably TMD radiologist and one DDWoR osteophyte, ADD) DJD is significantly
TMJ) patients author eburnation higher in joints
Any disagreements with advanced
were resolved by internal
forced consensus derangement
(p < 0.05)
Melo et al., 2015, Observational 102 Radiology clinic 17 (10e20) MRI (1.5 T) Two experienced According to Adapted from DJD ¼ 45.1% (in Bilateral DJD is
Brazil descriptive 80/22 (204 TMD patients radiologists Ahmad et al. Ahmad et al. ADD) strongly correlated
TMJ) (2009) e as (2009): with ADD
‘normal’ or osteophytes,
‘displaced’ flattening, erosion,
Subclassified sclerosis, edema
into DDwR or
DDwoR
Moncada et al., Observational 88 Orthodontic and 14.7 (10e18) MRI (1.5 T) Blinded and DwD, DDWR, Erosion, concavity, DJD ¼ 39.8% (in Significant
2014, Chile descriptive 65/23 (176 radiology clinic duplicated analysis and DDWoR flattening, ADD) association
TMJ) TMD patients by one of the osteophyte, DJD ¼ 32% (in between DDWoR
authors sclerosis, DDWR) and DJD in children
(Kappa ¼ 0.86) subchondral cyst, DJD ¼ 71% (in and adolescents
and/or deformity DDWoR) with TMD
Erosion ¼ 26%
Osteophytes ¼ 2%
Subchondral
cyst ¼ 6%
ütcen-Toller
Og Observational 63 TMD patients 28.13 (16e55) MRI (0.5 T) One investigator Degree of ADD: Spurring, flat- DJD ¼ 32% (in DJD is more severe
et al., 2002, descriptive 48/15 (126 Normal tening, and erosion DDWR) with an increased
Turkey TMJ) Slight along the condylar DJD ¼ 62.85% (in degree of ADD
Mild surface, glenoid DDWoR)
Moderate fossa, or articular
Severe eminence
Rao et al., 1990, Observational 138 TMD patients (15e75) MRI (1.5 T) NI Any forward Flattening, DJD ¼ 45% (in There is a
USA descriptive 127/11 (276 deviation of subchondral cyst DDWR) correlation
TMJ) posterior band, Regressive DJD ¼ 64% (in between the
relative to the remodeling: DDWoR) severity of internal
condylar apex, hypoplastic, small, derangement and
constituted or pointed condyles regressive bony
anterior disc condylar

M.A.G. Silva et al. / Journal of Cranio-Maxillo-Facial Surgery 48 (2020) 942e955


displacement remodeling
Roh et al., 2012, Observational 254 MRI files Mean Female 26.2 MRI (1.5 T) Two examiners DDWR and Erosion, sclerosis, DJD ¼ 31.7% (in The risk of
Korea descriptive 162/92 (508 TMD patients Male 32.9 Two examiners Inter-examiner DDWoR flattening, DDWR) degenerative
TMJ) (two times) concordance: 0.80 osteophyte DJD ¼ 47.2% (in changes increase
Groups: for disc DDWoR) with ADD
Normal 18 displacement and (although not all
DDR 134 0.66 for disc displacements
DDWR 102 degenerative progress to
disease degenerative
disease, the
possibility of risk of
progression is
increased)
Şener and Akgünlü, Observational 88 (NI) TMD patients NI MRI (1.5 T) Two observers (one DDWR ¼ 130 Erosion, flattening, DJD ¼ 84.6% (in Degenerative
2004, Turkey descriptive (175 TMJ) One clinician clinician, one DDWoR ¼ 45 osteophyte DDWR) changes do not
DDWR ¼ 130 One radiologist radiologist) DJD ¼ 84.4% (in appear to be
DDWoR ¼ 45 DDWoR) markers of either
DDWR or DDWoR
Zhuo and Cai, 2016, Cohort 28 Department of oral 33.1 (20e57) MRI (1.5 T) One examiner DDWoR Erosion, sclerosis, DJD ¼ 51.8% (in Significant increase
China retrospective 22/6 (56 TMJ) surgery 1st MRI e Intra-examiner flattening, ADD e initial) in bone changes in
Patients with disc baseline concordance: 0.75 osteophyte DJD ¼ 75% (in ADD adults with
displacement 2nd MRI e 24 Kappa ¼ 0.75 e follow-up) bilateral DDWoR
e54 months Inconsistency e all (in cases of long
after no authors follow-up of
treatment (Two DDWoR, all discs
times e 1 week remained displaced
interval) and there was a
significant increase
in bone changes,
although some
remained stable)

CBCT e cone beam computed tomography; CT e computed tomography; DD e disc displacement; DDR e disk displacement with reduction; DDWR e disc displacement without reduction; NI e not informed; MRI e magnetic
resonance imaging; NI e not informed; OA e osseous abnormalities; TMJ e temporomandibular joint; TMD e temporomandibular disorder.

947
948 M.A.G. Silva et al. / Journal of Cranio-Maxillo-Facial Surgery 48 (2020) 942e955

phase was resolved by discussion and agreement between the the feature of DJD (erosion, osteophyte, sclerosis, and subcortical
three reviewers. A third author (LQP) was involved, when required, cyst).
to enable the formulation of the final decision. In cases where the
required data were not available, three attempts were made to
contact each author by email in order to retrieve any pertinent 2.9. Analysis of the subgroups
unpublished information.
Subgroup analysis for prevalence was performed by grouping
studies according to the type of disc displacement (DDWR or
2.7. Risk of bias for individual studies
DDWoR) and according to the type of degenerative change of the
TMJ (erosion, osteophyte, sclerosis, or subcortical cyst), following
The risk of bias for the selected studies was assessed using the
the classification of DC/TMD (Schiffman et al., 2014). Although
Joanna Briggs Institute Critical Appraisal Checklist for Studies
cortical sclerosis has been considered an adaptive rather than direct
Reporting Prevalence Data (2014) (Munn et al., 2014). This
DJD, ‘sclerosis’ was included in this study since it was not possible
checklist addresses the critical issues of internal and external
to differentiate cortical from generalized sclerosis within the
validity that must be considered when assessing observational
studies.
studies. Two reviewers (MAGS and LQP) independently scored the
risk of bias as ‘low risk’, ‘moderate risk’, or ‘high risk’. Disagree-
ments were resolved by a consensus involving a third author
3. Results
(ENSG). The risk of bias was categorized by the authors as high
when up to 49% of the items scored ‘yes’, moderate when 50e69%
3.1. Study selection
of the studies scored ‘yes’, and low when more than 70% of the
studies scored ‘yes’.
The search strategy resulted in 738 articles after removing the
duplicates. A comprehensive evaluation of the titles and abstracts
2.8. Synthesis of the summary measures was performed, and 695 articles were excluded, resulting in 43
potentially useful articles. There were 102 additional studies from
Review Manager 5.3 (Rev-Man 5.3, The Nordic Cochrane Centre, the gray literature search, but only two were included. Conse-
Copenhagen, Denmark) and MedCalc Statistical Software version quently, 45 full-text articles from databases were screened ac-
14.8.1 (Ostend, Belgium) were used to analyze the data. Heteroge- cording to the inclusion and exclusion criteria. The reference lists of
neity was calculated using the inconsistency index (I2), with values these studies were screened, but no additional studies were
higher than 50% being considered indicative of substantial het- included. No experts suggested the addition of any articles. Finally,
erogeneity between the studies, implying a random effect. The after full-text reading, 27 studies were excluded (Appendix 2) and
prevalence of DJD among cases of ADD of the TMJ was assessed 18 studies were finally included in this review. A flowchart of the
with 95% confidence intervals (CI). The studies were clustered ac- process of identification, inclusion, and exclusion of studies is
cording to the type of disc displacement (DDWR or DDWoR) and shown in Fig. 1.

Table 2
Results from Joanna Briggs Institute Critical Appraisal Checklist for studies reporting prevalence data (Munn et al. Int J Health Policy Manag 3(3), 123e128, 2014).

Author, year Q1 Q2 Q3 Q4 Q5 Q6 Q7 Q8 Q9 Total Risk of bias

Alkhader et al., 2010 Y U Y Y U Y Y Y Y 70.7% Low


Badel et al., 2012 Y U Y Y U Y Y Y Y 70.7% Low
Bolzan, 2002 Y U Y Y U Y U Y Y 60.6% Mod
Butzke et al., 2007 Y N Y Y U Y N Y Y 60.6% Mod
Cortes et al., 2016 Y U Y Y Y Y Y Y Y 80.8% Low
Dias et al., 2016 Y N Y Y U Y Y Y Y 70.7% Low
Emshoff et al., 2001 Y N Y Y U Y U Y Y 60.6% Mod
Gil et al., 2012 Y N Y Y U Y Y Y Y 70.7% Low
Grossmann et al., 2016 Y U Y Y U Y N Y U 50.5% Mod
Hasan and Abdelrahman, 2014 Y U Y Y U Y Y Y Y 70.7% Low
Kurita et al., 2000 Y U Y Y Y Y Y Y Y 80.8% Low
Melo et al., 2015 Y U Y Y U Y Y Y Y 70.7% Low
Moncada et al., 2014 Y N Y Y U Y Y Y Y 70.7% Low
Ogütcen-Toller et al., 2002 Y N Y Y U Y N Y Y 60.6% Mod
Rao et al., 1990 U U Y Y U Y U U Y 40.4% High
Roh et al., 2012 Y U Y Y U Y Y Y Y 70.7% Low
Şener and Akgünlü, 2004 Y U Y Y Y Y U Y Y 70.7% Low
Zhuo and Cai, 2015 Y U Y Y U Y Y Y Y 70.7% Low

Y yes, N no, U unclear, NA not applicable.


Q1 e Was the sample representative of the target population?
Q2 e Were study participants recruited in an appropriate way?
Q3 e Was the sample size adequate?
Q4 e Were the study subjects and the setting described in detail?
Q5 e Was the data analysis conducted with sufficient coverage of the identified sample?
Q6 e Were objective, standard criteria used for the measurement of the condition?
Q7 e Was the condition measured reliably?
Q8 e Was there appropriate statistical analysis?
Q9 e Are all important confounding factors/subgroups/differences identified and accounted for?
Total ¼ SY/applicable items (the not applicable (NA) items were excluded from the sum).
Risk of bias was categorized as high when the study reached a score of up to 49% ‘yes’, moderate when the study reached a score of 50e69% ‘yes’, and low when the study
reached a score of more than 70% ‘yes’.
M.A.G. Silva et al. / Journal of Cranio-Maxillo-Facial Surgery 48 (2020) 942e955 949

Fig. 2. Risk of bias and applicability concerns graph: review of authors' judgments about each risk of bias item for each included study: (A) risk of bias graph; (B) risk of bias
summary.

Fig. 3. Forest plot of prevalence of DJD among ADD (DDWR þ DDWoR).


950 M.A.G. Silva et al. / Journal of Cranio-Maxillo-Facial Surgery 48 (2020) 942e955

Fig. 4. Forest plot of prevalence of DJD among DDWR.

Fig. 5. Forest plot of prevalence of DJD among DDWoR.

Fig. 6. (A) Forest plot of prevalence of DJD among ADD cases (DDWR þ DDWoR) e young patients only. (B) Funnel plot of the overall effect of DJD among ADD cases for young
population only.
M.A.G. Silva et al. / Journal of Cranio-Maxillo-Facial Surgery 48 (2020) 942e955 951

3.2. Study characteristics osseous change in DJD, 737 TMJs were analyzed for erosion, 921 for
osteophyte, 250 for sclerosis, and 487 for subcortical cyst.
The total sample size was 3158 TMJs in 1631 patients (1161 All included studies used MRI for the evaluation of DJD and
females and 345 males d a ratio of 3.37:1), with sex not reported ADD; however, four studies also used CT or CBCT imaging (Rao
in 125 cases from two studies (Şener and Akgünlü, 2004; Butzke et al., 1990; Alkhader et al., 2010; Badel et al., 2012; Corte s et al.,
et al., 2007). The average age was 46 (range 10e82) years. The 2016). Therefore, in order to reduce the heterogeneity between
18 selected studies were all published between 1990 and 2016 the included data, only MRI data were used. Evaluation of ADD was
from the following 10 countries: Austria (Emshoff et al., 2001), carried out in most of the studies (Emshoff et al., 2001; Bolzan,
Brazil (Bolzan, 2002; Butzke et al., 2007; Gil et al., 2012; Melo 2002; Og ütcen-Toller et al., 2002; Roh et al., 2012; Dias et al.,
et al., 2015; Dias et al., 2016; Grossmann et al., 2016), Chile 2012; Alkhader et al., 2010; Melo et al., 2015) following the usu-
(Moncada et al., 2014; Corte s et al., 2016), China (Zhuo and Cai, ally accepted criteria for disc displacement: DDWR when the pos-
2016), Croatia (Badel et al., 2012), Egypt (Hasan and terior band of the disc was displaced from its normal position
Abdelrahman, 2014), Japan (Kurita et al., 2000; Alkhader et al., (11:30e12:30 clock position relative to the top of the condyle in the
2010), Korea (Roh et al., 2012), Turkey (Og ütcen-Toller et al., closed-mouth position), but assumed a normal position upon jaw
2002; Şener and Akgünlü, 2004), and the USA (Rao et al., 1990). opening; DDWoR when the disc was displaced anteriorly in all
The sample sizes in these studies ranged from 56 to 508 TMJs. Two mouth positions (Ahmad et al., 2009).
studies (Butzke et al., 2007; Şener and Akgünlü, 2004) did not Variability was observed for the DJD criteria. Some authors
elucidate the sex ratio in the total sample. From the sample of 16 included condylar, articular eminence, and fossa bone changes
studies (n ¼ 2818), 84.5% were female. The patients recruited were (Ogütcen-Toller et al., 2002; Gil et al., 2012), while others considered
mostly from TMD clinics. only condylar changes for the diagnosis of DJD (Dias et al., 2016;
From the total sample, it was possible to include data for 1762 Grossmann et al., 2016). Most of the studies considered flattening as
TMJs in the quantitative analysis for the prevalence of DJD in both DJD. Only two out of the 18 included articles did not consider flat-
ADD groups. It was possible to analyze the prevalence of DJD in 800 tening (Bolzan, 2002; Gil et al., 2012). A summary of the descriptive
TMJs with DDWR, and of DJD in 654 TMJs with DDWoR. For each characteristics of the included articles is provided in Table 1.

Fig. 7. Forest plot of prevalence of each DJD among DD cases (DDWR and DDWoR): (A) erosion (23.5%); (B) osteophyte (17.9%); (C) sclerosis (24.3); (D) subcortical cyst (7.636).
952 M.A.G. Silva et al. / Journal of Cranio-Maxillo-Facial Surgery 48 (2020) 942e955

3.3. Risk of bias within the studies (Rao et al., 1990; Kurita et al., 2000; Emshoff et al., 2001; Bolzan,
2002; Og ütcen-Toller et al., 2002; Şener and Akgünlü, 2004;
The complete analysis of the quality assessment items list is pre- Butzke et al., 2007; Gil et al., 2012; Roh et al., 2012; Hasan and
sented in Table 2. All studies were methodologically acceptable; Abdelrahman, 2014; Moncada et al., 2014; Melo et al., 2015;
however, none of them fulfilled all the risk of bias criteria according to Grossmann et al., 2016). As shown in Fig. 3, which represents the
the Joanna Briggs Institute Critical Appraisal Checklist (Ouzzani et al., sum of DDWR and DDWoR, we found a prevalence of DJD of around
2016). The main methodological limitations of the studies were 50% (95% CI 29 189e84 571; n ¼ 1762; p < 0.0001; and high het-
related to poor recruitment (Question 2), since the samples were erogeneity, I2 ¼ 92.59%).
mostly recruited by convenience, and to Question 5 (Was the data ütcen-Toller
Ten studies (Rao et al., 1990; Emshoff et al., 2001; Og
analysis conducted with sufficient coverage of the identified sam- et al., 2002; Şener and Akgünlü, 2004; Butzke et al., 2007; Gil et al.,
ple?). Of the 18 studies, 12 presented a low risk of bias (Kurita et al., 2012; Roh et al., 2012; Hasan and Abdelrahman, 2014; Moncada
2000; Şener and Akgünlü, 2004; Alkhader et al., 2010; Dias et al., et al., 2014; Grossmann et al., 2016) had enough data to calculate
2012; Roh et al., 2012; Gil et al., 2012; Badel et al., 2012; Hasan and the prevalence of DJD in DDWR. We found a prevalence of DJD in
Abdelrahman, 2014; Moncada et al., 2014; Melo et al., 2015; Zhuo DDWR of around 35% (95% CI 5263e84 615; n ¼ 800; p < 0.0001;
and Cai, 2016; Cortes et al., 2016). A moderate risk was observed in and high heterogeneity, I2 ¼ 95.64%), as presented in Fig. 4.
five studies (Emshoff et al., 2001; Og ütcen-Toller et al., 2002; Bolzan, Eleven studies (Rao et al., 1990; Emshoff et al., 2001; Og ütcen-
2002; Butzke et al., 2007; Grossmann et al., 2016), and a high risk of Toller et al., 2002; Şener and Akgünlü, 2004; Butzke et al., 2007;
bias was observed in one study (Rao et al., 1990) (Fig. 2). Gil et al., 2012; Roh et al., 2012; Hasan and Abdelrahman, 2014;
Moncada et al., 2014; Grossmann et al., 2016; Zhuo and Cai, 2016)
3.4. Data synthesis and meta-analysis results included enough data to calculate the prevalence of DJD in DDWoR.
We found a prevalence of DJD in DDWoR of 66% (95% CI
Among all 18 studies, Badel et al. (2012) were the only authors to 47 826e84 444; n ¼ 654; p ¼ 0.0228 and medium heterogeneity,
present data comparing both TMD and control groups. They found I2 ¼ 51.84%), as shown in Fig. 5.
no DJD in the control group. However, there was a statistically It was not possible to separate older and younger ages in order
significant difference for degenerative changes between symp- to show if the DDWR or DDWoR was more related to a specific age
tomatic and asymptomatic TMD patients (p ¼ 0.009). group, since the original studies did not separate them. However,
The test for heterogeneity showed mostly high heterogeneity; when excluding the studies that mixed younger and older pop-
therefore, the meta-analyses were applied using a random-effects ulations, leaving six studies with only adult populations (Bolzan,
model. 2002; Şener and Akgünlü, 2004; Butzke et al., 2007; Roh et al.,
The meta-analysis for the prevalence of DJD was performed in 2012; Hasan and Abdelrahman, 2014; Grossmann et al., 2016), the
order to evaluate DJD in DDWR and DDWoR, combining 13 studies meta-analysis showed a slightly higher prevalence of 53% (95% CI

Fig. 7. (continued).
M.A.G. Silva et al. / Journal of Cranio-Maxillo-Facial Surgery 48 (2020) 942e955 953

29 189e57 738; n ¼ 889) of DJD in DDWR and DDWoR combined in degenerative changes in most of the cases. Although the
(p < 0.0001; high heterogeneity, I2 ¼ 96.40%), as shown in Fig. 6 degenerative changes were evaluated by conventional images, this
(supplementary file). On the other hand, a separate meta-analysis paper documented a probable correlation between DDWoR and
grouping the only two studies (Moncada et al., 2014; Melo et al., degenerative changes. Other longitudinal studies may endorse this
2015) with a young population (10e20 years of age) showed a etiological relationship, and may also ascertain which disorder is
prevalence of 49% (95% CI 47 794e48 649; n ¼ 284) of DJD in DDWR the starting point. Our study could not confirm the association
and DDWoR combined (p ¼ 0.8861; low heterogeneity, I2 ¼ 0.00%), between DDWoR and degenerative changes because all samples
as shown in Fig. 6A. The funnel plot in Fig. 6B shows that the dis- from primary studies were related to TMD clinics. However, the
tribution was symmetric, confirming that there was no publication higher prevalence of osseous changes in DDWoR points in this di-
bias. rection. We also demonstrated a similar prevalence (49%) of ADD
The prevalence of DJD was also investigated for each osseous among patients with DJD. This may contribute to discussions on the
change in DJD, considering both DDWR and DDWoR, as illustrated association of the conditions in two ways: the case of DDWR
in Fig. 7: (A) Erosion 23.5%; 95% CI 2206e28 909; n ¼ 737 (Alkhader changing to DDWoR and resulting in bone changes, as well as the
et al., 2010; Moncada et al., 2014; Melo et al., 2015; Corte s et al., bone changes resulting in disc displacement.
2016; Zhuo and Cai, 2016). (B) Osteophyte 17.9%; 95% CI Some studies have postulated that subclinical DJD may lead to
1351e36 923; n ¼ 921 (Alkhader et al., 2010; Badel et al., 2012; pathological tissue responses in the form of internal derangement;
Moncada et al., 2014; Melo et al., 2015; Corte s et al., 2016; therefore, disc displacement would represent the outbreak of DJD
Grossmann et al., 2016; Zhuo and Cai, 2016). (C) Sclerosis 24.3%; and not the other way round (Alkhader et al., 2010). However,
95% CI 4412e53 061; n ¼ 250 (Alkhader et al., 2010; Melo et al., clinical and radiological diagnoses of advanced TMJ internal
2015; Zhuo and Cai, 2016). (D) Subcortical cyst 7.6%; 95% CI derangement correlate with histological findings of degeneration
4730e10 029; n ¼ 487 (Moncada et al., 2014; Corte s et al., 2016). and inflammation of the articular disc and articular surface
A reverse way was also analyzed (the prevalence of ADD among degeneration of the condyle, suggesting that subclinical DJD may
cases of DJD), grouping two studies (Alkhader et al., 2010; Badel not be the cause of pathological tissue responses such as disc
et al., 2012). Fig. 9 (supplementary file) shows a prevalence of displacement (Dimitroulis, 2005).
49% for ADD (DDWR and DDWoR) in patients with DJD (95% CI 34 It is important to note that the prevalence of DJD may vary ac-
286e61 538; n ¼ 100; p ¼ 0.0092; high heterogeneity, I2 ¼ 85.28%). cording to the criteria used for diagnosis. The pathological process
of DJD can be divided into three slowly progressing stages ac-
4. Discussion cording to the natural course of the disease in the TMJ. The initial
phase is the slowest, and although microscopic tissue damage is
This systematic review with meta-analyses was the first to already present, it is often undetectable on images (Kalladka et al.,
evaluate the prevalence of DJD in patients with ADD. The findings 2014). In the intermediate and late phases, significant osseous
showed a relatively high prevalence of DJD among DDWoR. changes occur and the symptoms worsen.
We considered the following to be osseous changes related to The use of imaging to confirm the clinical diagnosis is a
TMJ degenerative disease, as recommended by the Consortium requirement of the current reference criteria (Schiffman et al.,
Network and Orofacial Pain Special Interest Group (Schiffman et al., 2014). However, this implies that the diagnosis is always made in
2014): subchondral cyst, erosion, generalized sclerosis, or osteo- a late phase of the degenerative disease, in which the probability of
phyte. Sclerosis was considered ‘general sclerosis’ since it was not functional loss is higher (Cevidanes et al., 2014). Although the
possible to identify which kind of sclerosis had been described in prevalence of any disease usually increases with imaging and the
most of the studies. Additional research is needed to separate observer's ability to detect disease-associated abnormalities (Black
flattening and specify general sclerosis in the findings, in order to and Welch, 1990), in the case of DJD this prevalence would be
correlate the main features of DJD. It is important to highlight that higher if the diagnostic criteria allowed the diagnosis at an early
flattening was considered a sign of DJD of the TMJ in almost all the stage when structural changes are not yet detectable by imaging
studies. Only two studies (Bolzan, 2002; Gil et al., 2012) did not (Michelotti et al., 2016).
include flattening in the imaging criteria for DJD. Since 2014, flat- The similar prevalence among children and adolescents (49%)
tening and/or cortical sclerosis have been considered indeter- observed in the studies by Melo et al. (2015) and Moncada et al.
minant findings for DJD (Schiffman et al., 2014); however, most of (2014) does not corroborate the hypothesis of progressive disease,
the studies reported so far have not been designed without flat- and leads us to believe that DJD may not be a time-related disorder.
tening. In order to exclude the influence of flattening from the re- An association between the onset of DDWoR and degenerative TMJ
sults, we carried out meta-analyses considering each osseous changes, as well as the severity of clinical manifestations, has been
change in DJD when it was possible to collect these data in the demonstrated in adolescents and young adults as early as 1 month
included papers. after the onset of DDWoR (Lei et al., 2017; Hasan and Abdelrahman,
The prevalence of DJD was higher in DDWoR than in DDWR. The 2014), reinforcing the recommendation for early diagnosis and
presence of DJD related to ADD, especially DDWoR, is a common intervention of DDWoR, especially in a young population. This
finding in the literature (Rao et al., 1990; Emshoff et al., 2001; suggests that aging may not be a crucial factor in the pathogenesis
Bolzan, 2002; Og ütcen-Toller et al., 2002; Butzke et al., 2007; of DJD (Zhao et al., 2011). It is assumed that in DDWoR, degenerative
Alkhader et al., 2010; Dias et al., 2012, 2016; Roh et al., 2012; Badel changes may progress even after the symptoms and signs of TMJ
et al., 2012; Hasan and Abdelrahman, 2014; Moncada et al., 2014; disorders are resolved or reduced (Kurita et al., 2006).
s et al., 2016; Grossmann et al., 2016; Zhuo
Melo et al., 2015; Corte One study (Lei et al., 2017) only used CBCT to evaluate DJD.
and Cai, 2016), and seems to be a natural progressive change in TMJ Therefore, to not compromise the homogeneity of the data, we
bones. Only one study (Şener and Akgünlü, 2004) included in this decided to exclude the report, since it was intended to also corre-
systematic review found no significant difference between DDWR late ADD, which is better evaluated by MRI.
and DDWoR associated with DJD; however, degenerative changes The criteria for disc displacement were heterogeneous among
were found to be more severe in DDWoR. In a longitudinal study, the studies, but most authors followed the DC/TMD classification
Leeuw et al. (1996) found that degenerative changes were not seen (Schiffman et al., 2014). A displaced articular disc has been
in joints with DDWR in a 30-year follow-up, while DDWoR resulted considered as having an important role in the pathology of internal
954 M.A.G. Silva et al. / Journal of Cranio-Maxillo-Facial Surgery 48 (2020) 942e955

derangement of the TMJ; however, this is also a common finding in Ethical approval
the asymptomatic population. Ribeiro et al. (1997) observed 25% of
joints as having disc displacement in asymptomatic volunteers; Not required.
however, the same paper showed an odds ratio of 12.2, suggesting a
strong association between disc displacement and TMD. Patient consent
To the best of our knowledge, this is the first systematic review
to show this correlation, while representing the compilation of Not required.
primary studies. Even after considering some heterogeneity among
the studies, this finding may corroborate the need for longitudinal
Funding
studies in order to determine if prevention or early treatment is
None.
necessary as soon as a DDWoR is diagnosed, and to prevent
anomalies in the facial form or symmetry. Although ADD does not
always evolve into painful situations or DJD due to adaptive ca- CRediT author statement
pacity, the possibility of an increased risk of DJD should be evalu-
ated individually with regards to the presence of contributing MAG Silva: conceptualization, investigation, writing d original
factors, including genetics. draft preparation. LLQ Pantoja: investigation. KL Dutra-Horst-
The limitations of this study include potential heterogeneity mann: investigation. J Valladares-Neto: conceptualization, inves-
among observational descriptive studies, including two with a tigation, supervision. FL Wolff: investigation. AL Porporatti:
young population (Moncada et al., 2014; Melo et al., 2015). Het- formal analysis. ENS Guerra: investigation, writing d reviewing
erogeneity was especially noted in the recruitment of participants and editing. G De Luca Canto: methodology, writing d reviewing
in the studies reviewed, mostly from the TMD population, and the and editing.
lack of sufficient coverage of the identified sample, both of which
are inherent in observational studies. The presence of a young Declaration of competing interest
population, although representing heterogeneity, also serves as a
warning of the importance of prevention and early treatment in The authors declare that they have no conflicts of interest to
order to prevent changes in dentofacial morphology or limited declare.
mandibular growth, leading to facial deformity (Bertram et al.,
2011; Roh et al., 2012). Another limitation is related to the Acknowledgments
methods of imaging. Although CT/CBCT is the reference standard
for investigating DJD (Hilgenberg-Sydney et al., 2018), we could not The authors would like to thank Ms Maria Gorete Monteguti
analyze ADD using CT/CBCT. On the other hand, although not the Savi, a health sciences librarian, for assistance in the bibliographic
preferred approach, it is possible to visualize DJD by MRI, as we search.
could find in many studies. The use of MRI to detect osseous
changes probably influenced the prevalence presented in our re-
Appendix A. Supplementary data
sults, while underestimating initial erosions, which are better
visualized by CT/CBCT. However, the study by Peck et al. on a
Supplementary data to this article can be found online at
consensus-based classification system and associated diagnostic
https://doi.org/10.1016/j.jcms.2020.08.004.
criteria recommended TMJ CT/CBCT or MRI to evaluate osseous
changes (Peck et al., 2014). The perfect study should use both
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