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Original Paper

Caries Res 2018;52:406–419 Received: August 6, 2017


Accepted after revision: December 20, 2017
DOI: 10.1159/000486429 Published online: March 8, 2018

The International Caries Detection


and Assessment System – ICDAS:
A Systematic Review
Kim Rud Ekstrand a Thais Gimenez b Fernanda R. Ferreira b Fausto M. Mendes b
       

Mariana M. Braga b  

a Department of Odontology, University of Copenhagen, Copenhagen, Denmark; b Department of Pediatric


 

Dentistry, School of Dentistry, University of São Paulo, São Paulo, Brazil

Keywords ment associated with the ICDAS. The meta-analyses pooled


Dental caries · Caries detection · Activity assessment · results based on the same methodology and parameters as
Visual inspection · ICDAS · Performance · Accuracy above. Longitudinal findings regarding caries progression
were described to estimate the validity of these systems. On
average, the systems for activity assessment of caries lesions
Abstract showed moderate values concerning reproducibility and
The aims of this study were: (1) to evaluate the overall repro- overall performance. Active caries lesions were more prone
ducibility and accuracy of the International Caries Detection to progress than inactive ones after 2 years. In conclusion,
and Assessment System (ICDAS) for assessing coronal caries the ICDAS presented a substantial level of reproducibility
lesions, and (2) to investigate the use of systems associated and accuracy for assessing primary coronal caries lesions.
with the ICDAS for activity assessment of coronal caries le- Additional systems associated with the ICDAS that classify
sions. Specific search strategies were adopted to identify caries lesion activity can be useful as they are moderately
studies published up to 2016. For the first objective, we se- reproducible and accurate. © 2018 S. Karger AG, Basel
lected studies that assessed primary coronal caries lesions
using the ICDAS as a reference standard. A total of 54 studies
were included. Meta-analyses summarized the results con- The ICDAS was devised between 2002 and 2004, based
cerning reproducibility and accuracy (correlation with his- on the following statements at 2 consensus conferences
tology, summary ROC curves [SROC], and diagnostic odds held around the millennium [Bader et al., 2001; Pitts and
ratio [DOR]). The latter 2 were expressed at D1/D3 levels. The Stamm, 2004]: (a) that the reliability of the available caries
heterogeneity of the studies was also assessed. Reproduc- detection/diagnostic systems (at that time), including vi-
ibility values (pooled) were >0.65. The ICDAS mostly present-
ed a good overall performance as most areas under SROC This paper is based on a presentation given at the ORCA Saturday
were >0.75 at D1 and > 0.90 at D3; DOR ≥6. For the second Afternoon Symposium “Critical Appraisal of Current Clinical Caries
objective, we selected studies investigating activity assess- Diagnostic Systems” in Athens on July 6, 2016.
128.111.121.42 - 3/9/2018 3:15:09 PM
Univ. of California Santa Barbara

© 2018 S. Karger AG, Basel Kim Rud Ekstrand


Section of Cariology and Endodontics, Dental School of Copenhagen
University of Copenhagen, Nörre Alle 20
E-Mail karger@karger.com
DK–2200 Copenhagen (Denmark)
www.karger.com/cre
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E-Mail kek @ sund.ku.dk


sual and visual-tactile criteria, was not strong, and (b) that producibility of the scoring system has been evaluated
there were too many incompatible systems. A group of clinically [Agustsdottir et al., 2010; Ferreira Zandona et
caries “experts” were invited to a meeting in Dundee in al., 2012].
2002. The tasks were to devise a simple, logical, evidence-
based system for the detection and classification of caries
in dental education, clinical practice, dental research, and Aims of the Present Study
dental public health in order to provide appropriate diag-
The organizers of the Saturday afternoon symposiums in 2016
nosis, prognosis, and clinical management of dental car-
gave the authors the following working title: Aims, Advantages,
ies at both the individual and public health levels [Pitts, and Limitations of the International Caries Detection and Assess-
2004, 2009]. ment System – ICDAS.
Three groups were formed to report the literature To cover the advantages and limitations of the ICDAS and de-
within clinical classification systems on coronal caries, termine its overall reliability and accuracy/validity, we carried out
a systematic review including a meta-analysis. Furthermore, we
root caries, and caries adjacent to restorations. The expert
aimed to synthesize published information about the ICDAS
group dealing with coronal caries suggested using the linked to activity assessment systems in terms of reproducibility,
Ekstrand, Kidd, Ricketts system (ERK system) [Ekstrand sensitivity/specificity, and predictive and construct validity.
et al., 1997] because that system used histology as valida- The aims of this paper can be summarized as: (1) to evaluate the
tion [Ekstrand et al., 1998; Cortes et al., 2000; Ricketts et overall reproducibility and accuracy of the ICDAS for assessing cor-
onal caries lesions, and (2) to investigate the use of systems associ-
al., 2002], and activity assessment of caries lesions had
ated with ICDAS for activity assessment of coronal caries lesions.
also been tried with the ERK system [Ekstrand et al.,
1998]. Eventually, the 5 scores in the original ERK-system
were extended to 7 scores in the International Caries De-
tection and Assessment System, abbreviated as ICDAS I Materials and Methods
[Pitts, 2004]. The systematic reviews in this paper follow the PRISMA guide-
The other 2 groups at the Dundee meeting devised lines [Moher et al., 2009]. This review comprised a subset anal-
scoring systems for root caries lesions and caries adjacent ysis from an umbrella review registered in Prospero (2013/
to restorations [ICDAS, 2017]. The latter eventually be- CRD42013003718) and previously published [Gimenez et al., 2015].
came similar to that developed for coronal caries. The ex-
Systematic Review: The Accuracy of the ICDAS in Detecting
pert group also suggested that the ICDAS should be a Coronal Caries
2-digit system where the first digit was the status of the Information Sources, Study Selection, and Eligibility Criteria
surface and the second score was the ICDAS caries status In the first review, the focus of attention was on answering the
of the surface [ICDAS, 2017]. following question: “how reproducible and accurate is the ICDAS
In 2004, there was a consensus conference in Boston, in assessing coronal caries lesions?”
Based on this, a search was performed until July 2016, using an
USA, where it was agreed that the original score 3 (shad- adaptation of a published search strategy [Gimenez et al., 2015]
owed lesion) and 4 (enamel cavitation) should swap plac- (online suppl. Fig. S1; for all online suppl. material, see www.karg-
es in the ICDAS scoring system, as shadowed lesions his- er.com/doi/10.1159/000486429). The PubMed, Embase, and Sco-
tologically were a bit more mature (deeper) than enamel pus databases were searched to retrieve published studies. Also
cavitated lesions [Cortes et al., 2000, 2003]. Thus, the IC- OpenSIGLE and the annals of the IADR/AADR (International and
American Associations for Dental Research) and ORCA (Euro-
DAS II was devised [Ismail et al., 2007], which eventually pean Organization for Caries Research) congresses were accessed
became understood as the ICDAS. to retrieve unpublished literature. The references of included ar-
At a pre-ORCA congress in 2005 in Indianapolis, the ticles were checked manually.
ICDAS Coordinating Committee discussed criteria for Titles and abstracts were initially assessed against the inclusion
activity assessment of the caries lesion [ICDAS, 2017]. criteria, which were: (1) available information regarding detecting
primary coronal caries lesions using visual inspection; (2) mate-
Some of these criteria were afterwards combined and rial of primary and permanent human teeth, including either a
named the ICDAS-LAA system. Both the original activity laboratory or clinical setting and all types of surfaces, and (3) writ-
assessment system as well as the ICDAS-LAA have been ten in the English language, as performed for an umbrella review
evaluated [Ekstrand et al., 2007; Braga et al., 2010; Pio- [Gimenez et al., 2015]. Studies that did not specifically use the
vesan et al., 2013; Guedes et al., 2014; Floriano et al., ICDAS for caries detection or did not present a reference standard
were excluded from this review. Those studies not reporting the
2015]. Finally, at the preORCA congress held in Den- used threshold or any data allowing an estimation of the perfor-
mark in 2007, an ICDAS radiographical system based on mance of the method were excluded. This was also the case for
7 scores was devised [Halfsteein et al. 2007] and the re- conceptual papers and other reviews (not primary studies).
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Univ. of California Santa Barbara

The International Caries Detection and Caries Res 2018;52:406–419 407


Assessment System – ICDAS DOI: 10.1159/000486429
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408
Intra-examiner reproducibility

Primary teeth Permanent teeth


I2 (%) 65.1; 95% CI 10.8–90.8 I2 (%) 68.0; 95% CI 27.1–85.7

Chawla et al. [2012] 0.55 (0.35, 0.75) Neuhaus et al. [2015a] 0.41 (0.20, 0.62)
Freitas et al. [2016] 0.75 (0.67, 0.83) Achilleos et al. [(2013] 0.74 (0.23, 1.25)
Braga et al. [2009b] 0.95 (0.80, 1.10) Ozturk and Sinanoglu [2015] 0.71 (0.51, 0.91)
Bussaneli et al. [2015] 0.75 (0.40, 1.10) Neuhaus et al. [2015b]* 0.57 (0.33, 0.81)
Noaves et al. [2012] 0.76 (0.55, 0.96) Neuhaus et al. [2015b]*** 0.50 (0.26, 0.74)
Neuhaus et al. [2011] 0.73 (0.21, 1.25) Jallad et al. [2015] 0.88 (0.80, 0.96)
Ekstrand et al. [2011] 0.96 (0.83, 1.09) Diniz et al. [2011] 0.89 (0.86, 0.92)
Souza et al. [2013] 0.92 (0.72, 1.12) Gomez et al. [2013] 0.85 (0.56, 1.14)
Cotta et al. [2015] 0.84 (0.57, 1.11)

DOI: 10.1159/000486429
RE model 0.81 (0.71, 0.92) Rodrigues et al. [2008] 0.61 (0.29, 0.93)

Caries Res 2018;52:406–419


Jablonski-Momeni et al. [2008] 0.78 (0.49, 1.07)
–0.2 0 0.2 0.4 0.6 0.8 1.0 1.2 Diniz et al. [2009] 0.59 (0.31, 0.87)
IRR
Zandona et al. [2009]* 0.79 (0.70, 0.88)
Zandona et al. [2009]** 0.84 (0.75, 0.93)
Zandona et al. [2009]*** 0.81 (0.70, 0.92)
Ekstrand et al. [2011] 0.91 (0.78, 1.04)
Castilho et al. [2016] 0.60 (0.24, 0.96)
Ozkan et al. [2015] 0.76 (0.38, 1.14)
Ko et al. [2015] 0.96 (0.94, 0.96)
Ekstrand et al. [2007] 0.85 (0.65, 1.05)

RE model 0.78 (0.71, 0.85)

–0.2 0 0.2 0.4 0.6 0.8 1.0 1.2


IRR

Braga
Ekstrand/Gimenez/Ferreira/Mendes/
(For legend see next page.)
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Interexaminer reproducibility

Primary teeth Permanent teeth


I2 (%) 87.6; 95% CI 71.8–95.0 I2 (%) 8.5; 95% CI 3.21–20.6

Chawla et al. [2012] 0.41 (0.35, 0.47) Neuhaus et al. [2015a] 0.64 (0.42, 0.86)
Teo et al. [2014] 0.84 (0.61, 1.07) Mitropoulos et al. [2010] 0.51 (0.36, 0.66)
Braga et al. [2010] 0.91 (0.69, 1.13) Parviainen et al. [2013] 0.47 (0.02, 0.92)

Assessment System – ICDAS


Braga et al. [2009b] 0.82 (0.62, 1.02) Achilleos et al. [2013] 0.73 (0.28, 1.18)
Braga et al. [2009a] 0.47 (0.31, 0.63) Ozturk et al. [2015] 0.37 (0.17, 0.57)
Bussaneli et al. [2015] 0.58 (0.17, 0.99) Jallad et al. [2015] 0.72 (0.63, 0.81)
Piovesan et al. [2013]# 0.84 (0.69, 1.00) Diniz et al. [2011] 0.81 (0.75, 0.87)

The International Caries Detection and


Piovesan et al. [2013]## 0.57 (0.36, 0.77) Cotta et al. [2015] 0.60 (0.26, 0.94)
Piovesan et al. [2013]### 0.78 (0.39, 1.17) Rodrigues et al. [2013] 0.61 (0.43, 0.79)
Novaes et al. [2009] 0.62 (0.52, 0.72) Rodrigues et al. [2008] 0.51 (0.17, 0.85)
Novaes et al. [2012] 0.63 (0.38, 0.88) Jablonski-Momeni et al. [2008] 0.82 (0.64, 1.00)
Neuhaus et al. [2011] 0.35 (–0.26, 0.96) Diniz et al. [2009] 0.51 (0.22, 0.80)
Ekstrand et al. [2011] 0.87 (0.70, 1.04) Ekstrand et al. [2011] 0.86 (0.72, 1.00)
Souza et al. [2013] 0.55 (0.44, 0.66) Ozkan et al. [2015] 0.63 (0.18, 1.09)
Shoaib et al. [2009]### 0.68 (0.65, 0.71) Ekstrand et al. [2007] 0.82 (0.60, 1.04)
Shoaib et al. [2009]## 0.70 (0.64, 0.76)
Soviero et al. [2012] 0.93 (0.70, 1.16) RE model 0.67 (0.58, 0.75)
–0.2 0 0.2 0.4 0.6 0.8 1.0 1.2
IRR
RE model 0.68 (0.60, 0.76)
–0.2 0 0.2 0.4 0.6 0.8 1.0 1.2
IRR

Fig. 1. Forest plots for meta-analysis and heterogeneity analysis of intra- and inter-examiner reproducibility when ICDAS was used for assessing caries lesion severity.

DOI: 10.1159/000486429
Caries Res 2018;52:406–419
IRR, intra- or inter-rater reproducibility. Examiners: * experienced; ** intermediate (+training); *** novice. Surfaces: # approximal; ## smooth; ### occlusal.

409
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Study selection was performed independently by 2 reviewers [CRD, 2009]. The trim and fill method was used to adjust the
(T.G. and M.M.B.). Disagreements were resolved by discussion pooled estimates, when necessary (R package meta, version 4.8-2)
with a third researcher (K.R.E.). For studies with the same data set, [Schwarzer, 2007].
only the study considered the most complete was included in this
review. If the same study evaluated the accuracy of different sub- Systematic Review: Activity Assessment Associated with the
groups, the data were recorded as different studies. ICDAS
Information Sources, Study Selection, and Eligibility Criteria
Data Collection Process For the second review, the focus of attention was to collect in-
We searched papers for intra- and inter-examiner reproduc- formation about the systems associated with the ICDAS for activ-
ibility data of the ICDAS including quantitative intra- or inter- ity assessment of coronal caries lesions and, when possible, to ex-
rater reliability coefficients (intra-RR or inter-RR). When more press their performance in terms of reproducibility and accuracy.
than 1 examiner was involved, the mean values of the coefficients Following the question: “How has the activity assessment been
were used. If the study presented any estimation of variance, they performed when the ICDAS is used?” another search was per-
were also registered. If not, the standard error was estimated using formed in PubMed until January 2017 to summarize the evidence
a graphical model [Hanley, 1987]. about activity assessment using the ICDAS (online suppl. Fig. S1).
We also collected the absolute numbers of true positives, false We screened studies that combined any type of activity assess-
positive, true negatives, and false negatives or data to calculate ment and the visual examination performed by the ICDAS, how-
these figures. If the study had evaluated the performance of the ever exclusively on coronal caries. Articles that did not report data
method with more than 1 examiner, we used the values of the first about performance of the activity assessment or only reported in
examiner. If examiners with different levels of training participat- vitro experiments were excluded. The same strategy described in the
ed, data from the first examiner per category of training were col- previous section was used for duplicates. The selection of studies
lected and each category was considered as an independent set of was also performed by 2 independent reviewers (F.R.F. and M.M.B.)
data. Data about the correlation between the ICDAS scores and the and the same strategies were used for solving disagreements.
histological validation were also collected.
Data Collection Process and Synthesis of Results
Summary Measures and Synthesis of Results We summarized the studies that used the activity assessment
Subgroups concerning the type of teeth and study setting were associated with the ICDAS and their purposes. When aiming to
considered for all analyses. For the meta-analyses of intra-RR and validate the method, we also registered how it was performed. For
inter-RR, random-effects models were fitted using the R package longitudinal studies, findings regarding caries progression related
metafor (GNU General Public License version 2) [Viechtbauer, to the activity status of caries lesions were collected. When report-
2010]. Separate analyses were conducted for intra-RR and inter-RR ing data about performance, we carried out data collection and
data. When more than 1 IRR value was collected from the article as analyses similarly to in the first section.
reproducibility measurements, we preferred the following order of For the accuracy of activity assessment systems, sound surfaces
IRR coefficients to be used in these analyses: weighted Kappa, un- were not included in these analyses. Pooled results were presented
weighted Kappa, and intraclass correlation coefficient. Coefficients for all merged systems since they evaluated similar characteristics.
were pooled according to the methodology of a previously pub-
lished study [Bornmann et al., 2010]. Concerning the correlation Risk of Bias of Individual Studies
coefficients between the ICDAS and histology, pooled coefficients Two reviewers (M.M.B. and T.G.) were responsible for risk of
and their 95% confidence intervals are summarized in forest plots. bias assessment in the reviews reported above. The QUADAS-2
For accuracy, statistical analyses were performed for the sub- was used to assess the potential risk of bias of included test accu-
groups above and also the thresholds (D1 or D3). At D1 threshold, racy studies in both reviews. According to 4 domains (sample se-
all lesions were considered as carious. At D3, only more advanced lection, index test, reference standard, or timing and flow), the
caries lesions were included. Thus, surfaces considered as carious for studies were classified as low, high, or unclear risk of bias.
these analyses were those lesions into dentine when lesion depth was For longitudinal studies, the Newcastle-Ottawa quality assess-
assessed, or cavitated lesions when surface integrity was considered. ment scale was used to classify the risk of bias in 3 different do-
Statistical pooling of sensitivity, specificity, positive likelihood mains: selection, comparability, and outcome. This system identi-
(sensitivity/1 – specificity) and negative likelihood (1 – sensitivity/ fies the risk of bias using stars. If most of the stars were awarded
specificity), and diagnostic odds ratio [DOR = (TP/FP)/(FN/TN)] for the domain, the study was classified as having a low risk of bias
was carried out using the DERSimonian Laid method (random ef- considering this aspect.
fects meta-analyses model). We summarized these analyses in re-
ceiver operating characteristics curves (SROC) and tested the het-
erogeneity among the included studies using the Cochran Q and I2
tests. Sensitivity analyses were performed to check the influence of Results
studies with approximal caries lesions on the pooled estimates. All
these analyses were performed in MetaDisc 1.4 software (Unidad de Systematic Review: The Accuracy of the ICDAS in
Bioestadistica Clinica del Hospital Ramón y Caja, Madrid, Spain). Detecting Coronal Caries
Publication bias was assessed by checking the asymmetry of
funnel plots visually and using regression analysis performed in R Synthesis of Results
package metafor. Alternatively, for accuracy, we used funnel plots A total of 54 studies from 46 papers fulfilled the re-
of natural logarithm (ln) DOR versus 1/√effective sample size quirements for enrolment (online suppl. Fig. S2). Most of
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410 Caries Res 2018;52:406–419 Ekstrand/Gimenez/Ferreira/Mendes/


DOI: 10.1159/000486429 Braga
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Laboratory studies
SROC curve SROC curve
1.0
n studies = 16 n studies = 24
0.9
AUC(SE) = 0.8695 (0.0170) AUC(SE) = 0.8892
0.8 Pooled Sen = 0.785 (0.0297)
(0.759–0.810) Pooled Sen = 0,870
Pooled Spe = 0.786 (0.854–0.884)
0.7
(0.751–0.817) Pooled Spe = 0.725
(REM) pooled LR+ = 3.579 (0.682–0.766)
0.6 (2.128–6.020) (REM) pooled LR+ = 3.187
Sensitivity

(REM) pooled LR– = 0.244 (2.271–4.472)


0.5 (0.157–0.380) (REM) poole
(REM) pooled DOR = LR– = 0.147 (0.092–0.296)
0.4 16.115 (10.707–24.256) (REM) pooled DOR =
Heterogeneity Q (SE) = 26.467 (13.686–51.182)
24.06 (d.f. = 15), p = 0.064 Heterogeneity Q (SE) =
0.3 Inconsistency I2 = 37.6% 90.09 (d.f. = 23) p < 0.001
Estimate of between-study Inconsistency I2 = 74.5%
0.2 variance τ = 0.2447 Estimate of between-
study variance τ = 1.7641
0.1

0
0 0.2 0.4 0.6 0.8 1 0 0.2 0.4 0.6 0.8 1
1 – specificity 1 – specificity
Primary teeth

Permanent teeth
Clinical studies
SROC curve SROC curve
1.0

n studies = 6 n studies = 4
0.9
AUC(SE) = 0.7908 AUC(SE) = 0.7820
0.8 (0.0297) (0.0420)
Pooled Sen = 0.553 Pooled Sen = 0.563
0.7 (0.521–0.585) (0.523–0.602)
Pooled Spe = 0.861 Pooled Spe = 0.966
(0.831–0.888) (0.958–0.973)
0.6
(REM) pooled LR+ = 2.647 (REM) pooled LR+ = 2.889
Sensitivity

(2.103–3.332) (0.594–14.060)
0.5
(REM) pooled LR– = 0.407 (REM) pooled LR– = 0.438
(0.261–0.635) (0.242–0.792)
0.4 (REM) pooled DOR = (REM) pooled DOR =
6.118 (3.988–9.384) 7.522 (1.519–37.255)
0.3 Heterogeneity Q (SE) = Heterogeneity Q (SE) =
8.33 (d.f. = 5) p = 0.139 20.55 (d.f. = 3) p < 0.001
Inconsistency I2 = 40.0% Inconsistency I2 = 85.4%
0.2
Estimate of between- Estimate of between-
study variance τ = 0.1045 study variance τ = 2.1578
0.1

0
0 0.2 0.4 0.6 0.8 1 0 0.2 0.4 0.6 0.8 1
1 – specificity 1 – specificity

Fig. 2. Summary ROC diagrams for meta-analysis and heterogeneity analysis of ICDAS accuracy on assessing
any caries lesions at the D1 threshold – number of studies, area under the ROC curves, pooled sensitivity (Sen),
specificity (Spe), DOR, positive and negative likelihood ratios (LR), results for the Cochran Q test for heteroge-
neity, I2 and τ coefficient variances between studies.

the studies were laboratory studies (77%) conducted on Summary Measurements


permanent teeth (60%). A wide variety of examiner train- Thirty-two studies assessed the inter-RR and 28 stud-
ing/qualification was observed among the studies. Half of ies the intra-RR. Only a few of the studies were performed
the studies were performed with experienced examiners in a clinical setting and we therefore opted for a graphic
and approximately 40% were intermediately experienced summary, independently of setting (Fig.  1). The mean
but trained for the purposes of the study. The vast major- IRR values were all ≥0.67. The intra-RR tended to be
ity of studies (approx. 75%) concerned occlusal surfaces slightly higher than the inter-RR. The levels of heteroge-
(online suppl. Table S1). neity (I2) significantly varied among the subgroups
(Fig. 1).
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The International Caries Detection and Caries Res 2018;52:406–419 411


Assessment System – ICDAS DOI: 10.1159/000486429
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Laboratory studies
SROC curve SROC curve
1.0
n studies = 16
0.9 n studies = 22
AUC(SE) = 0.9171
0.8 (0.0278) AUC(SE) = 0.9219 (0.0220)
Pooled Sen = 0.704 Pooled Sen = 0.730
(0.661–0.744) (0.696–0.762)
0.7
Pooled Spe = 0.876 Pooled Spe = 0.872
(0.856–0.894) (0.853–0.890)
0.6 (REM) pooled LR+ = 7.582 (REM) pooled LR+ = 5.957
Sensitivity

(4.423–12.999) (3.862–9.188)
0.5 (REM) pooled LR– =0.339 (REM) pooled LR– = 0.253
(0.235–0.488) (0.138–0.464)
0.4 (REM) pooled DOR = (REM) pooled DOR =
33.866 (13.165–87.115) 26.937 (13.701–52.959)
0.3 Heterogeneity Q (SE) = Heterogeneity Q (SE) =
92.31 (d.f. = 15) p < 0.001 98.27 (d.f. = 21), p < 0.001
Inconsistency I2 = 83.7% Inconsistency I2 = 78.6%
0.2 Estimate of between- Estimate of between-study
study variance τ2 = 2.9472 variance τ2 = 1.8415
0.1

0
0 0.2 0.4 0.6 0.8 1 0 0.2 0.4 0.6 0.8 1

Permanent teeth
1 – specificity 1 – specificity
Primary teeth

Clinical studies
SROC curve SROC curve
1.0
n studies = 6
0.9 n studies = 5*
AUC(SE) = 0.9246
0.8 (0.0384) AUC(SE) = 0.6763 (0.0792)
Pooled Sen = 0.598 Pooled Sen = 0.545 (0.475–
(0.504–0.688) 0.614)
0.7 Pooled Spe = 0.971 Pooled Spe = 0.972
(0.962–0.978) (0.965–0.977)
0.6 (REM) pooled (REM) pooled LR+ = 6.419
LR+ = 11.478 (3,763– (1.744–23.619)
Sensitivity

0.5 35.009) (REM) pooled LR– = 0.513


(REM) pooled LR– = 0.401 (0.443–0.594)
(0.217–0.738) (REM) pooled DOR =
0.4
(REM) pooled DOR = 16.286 ( 3.275–80.990)
59.627 (14.361–247.58)
0.3 Heterogeneity Q (SE) = Heterogeneity Q (SE) =
17.13 (d.f. = 5), p = 0.004 30.68 (d.f. = 4) p < 0.001
0.2 Inconsistency I2 = 70.8% Inconsistency I2 = 87.0%
Estimate of between- Estimate of between-study
study variance τ2 = 2.1709 variance τ2 = 2.4894
0.1

0
0 0.2 0.4 0.6 0.8 1 0 0.2 0.4 0.6 0.8 1
1 – specificity 1 – specificity

Fig. 3. Summary ROC diagrams for meta-analysis and heterogeneity analysis of ICDAS accuracy on assessing
more advanced caries lesions (cavitated caries lesions or those lesions histologically into dentine/at the D3 thresh-
old – number of studies, area under the ROC curves, pooled sensitivity (Sen), specificity (Spe), DOR, positive and
negative likelihood ratios (LR), results for the Cochran Q test for heterogeneity, I2 and τ coefficient variances
between studies. * One study was omitted in the pooled analysis because of a false-positive value = 0, Spe = 1.

The pooled Spearman correlation between the ICDAS trast, the pooled sensitivities values were lower in the clin-
scores and histology was 0.78 for primary teeth (95% CI ical studies (0.55–0.60), but higher in the laboratory stud-
0.73–0.84; n = 5) and 0.68 for the permanent teeth (95% ies (>0.70). Pooled likelihood ratios (LR+) were above the
CI 0.58–0.78; n = 12). As very few studies were performed value 1 (2.65–11.48) and LR data ranged from 0.15 to
in vivo, we presented the global pooled results. 0.51. The DOR values were very high (6.1–59.6; Fig. 2, 3).
The areas under the ROC curves were all substantial Values of SROC, sensitivity and specificity were simi-
(≥0.75), apart from permanent teeth in clinical studies, lar between D1 and D3 levels for laboratorial studies
where the area under the ROC curve was 0.67 (Fig. 2, 3). (Fig. 2, 3). At the D1 threshold, slightly higher SROC val-
The pooled specificities were also all high (>0.70). In con- ues were found for laboratorial conditions. We also no-
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Sensitivity (95% CI)
SROC curve Freitas et al. [2016] 0.53 (0.41–0.64)
1.0 Cotta et al. [2015] 0.79 (0.49–0.95)
Braga et al. [2010] 0.79 (0.49–0.95)
0.9 Ekstrand et al. [2007] 0.84 (0.74–0.90)

0.8
Pooled sensitivity = 0.70 (0.63–0.77)
0.7 χ2 = 20.66: d.f. = 3 (p = 0.0001)
Inconsistency I2 = 85.5%
0 0.2 0.4 0.6 0.8 1.0
0.6
Sensitivity
Sensitivity

0.5

0.4

0.3
Specificity (95% CI)
0.2 Freitas et al. [2016] 0.64 (0.45–0.80)
Cotta et al. [2015] 0.40 (0.24–0.58)
Braga et al. [2010] 0.17 (0.02–0.48)
0.1
Ekstrand et al. [2007] 0.81 (0.64–0.93)

0 0.2 0.4 0.6 0.8 1.0


Pooled specificity = 0.56 (0.47–0.66)
1 – specificity
χ2 = 21.44: d.f. = 3 (p = 0.0001)
Inconsistency I2 = 86.0%
n studies = 4 0 0.2 0.4 0.6 0.8 1.0
Specificity
AUC(SE) = 0.7519 (0.1217)
(REM) pooled LR+= 1.596 (0.844–3.018)
(REM) pooled LR– = 0.508 (0.213–1.216)
(REM) pooled DOR = 3.274 (0.776–13.807)
Heterogeneity Q (SE) = 16.32 (d.f. = 2) p = 0.001
Inconsistency I2 = 81.6%
Estimate of between-study variance τ2 <0.001

Fig. 4. Meta-analysis of ICDAS+LAA accuracy on assessing caries lesion activity (left: summary ROC diagram;
right: forest plots for meta-analysis using sensitivity and specificity of the method).

ticed a trend of lower pooled sensitivities for clinical stud- ing primary teeth. At the D3 threshold, for the same set-
ies; however, these were associated with higher specificity ting, only sensitivity was increased (0.86; 95% CI 0.76–
values (Fig. 2). For clinical studies, a slightly lower pooled 0.94).
sensitivity was observed at the D3 level. For more ad- Apart from clinical studies conducted with primary
vanced caries lesions, a very high pooled specificity teeth, moderate to high levels of heterogeneity (I2) were
(>0.90) was observed for primary teeth, while a very low observed among the studies (Fig. 4, 5).
pooled specificity was found for permanent teeth (Fig. 3).
A wide variety of results was observed, especially among Systematic Review: Activity Assessment Associated
studies using permanent teeth (Fig. 3). with the ICDAS
Looking to the SROC, we observed some very discrep- Synthesis of Results
ant points, which represent some of the studies per- Thirty-six studies were retrieved in this search (online
formed with approximal lesions (Fig. 2, 3). When exclud- suppl. Fig. S3). Out of 11 included studies, 9 were cross-
ing the studies with approximal surfaces from the sample sectional and 2 were longitudinal studies (online suppl.
(sensitivity analysis), the DOR was increased by 20% for Table S2). Five studies validated a system to be used in
laboratory studies concerning permanent teeth at the D1 caries activity assessment in conjunction with the ICDAS.
threshold. For clinical studies, the exclusion of this type One additional study showed data compatible with a pre-
of surface resulted in a significantly higher sensitivity dictive validation of activity assessment of caries lesions
(0.88; 95% CI 0.81–0.93), AUC (0.90; 95% CI 0.83–0.97), [Ferreira Zandona et al., 2012]. Four studies were inter-
and DOR (14.860; 95% CI 6.756–32.670) at D1 concern- ested in the relationship between the ICDAS and activity
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known to change its color around a pH of 5.5 [Mac-
Clinical studies Gregor, 1962; Ekstrand et al., 1998].
A moderate overall performance was observed (see
Flow/timing
area under SROC, Fig. 4). The pooled DOR was greater
Reference standard than 1, and the pooled LRs were slightly closer to 1 (Fig. 4).
Index test The pooled specificity tended to be lower than the pooled
Patient selection sensitivity (Fig. 4). A high level of heterogeneity among
the studies was observed (Fig. 4).
a 0 10 20 30 40 50 60 70 80 90 100 % Assessment of Lesion Progression over a Period of Time.
■ High ■ Uncertain ■ Low Two studies performed verified caries progression after 2
Laboratory studies years [Ferreira Zandona et al., 2012; Guedes et al., 2014]
Flow/timing (online suppl. Table S4).
Significantly more active noncavitated caries lesions
Reference standard
progressed to frank cavitation in 2 years compared to the
Index test inactive ones in primary teeth (online suppl. Table S4).
Patient selection Differences in caries progression rates between active and
inactive cavitated caries lesions were still stronger in both
b 0 10 20 30 40 50 60 70 80 90 100 %
studies (online suppl. Table S4).
Risk of Bias of Individual Studies (Both Reviews). The
main source of risk of bias within the included studies for
Fig. 5. Risk of bias within included studies when investigating the
accuracy of ICDAS: laboratory studies (a) and clinical studies (b).
testing accuracy of the ICDAS was related to sample se-
lection (Fig. 5; online suppl. Table S5). This observation
was true both for accuracy in assessing caries lesion sever-
ity and activity. Most clinical studies testing the ICDAS
assessment and other indices or other clinical patterns for assessing lesion severity in permanent teeth (5 from 6
(online suppl. Table S2). studies) presented the potential of bias when the sample
Eight studies used the ICDAS and LAA for activity as- was selected, including specifically teeth indicated to be
sessment of caries lesions (online suppl. Table S2). Other extracted or restored. The same was observed in studies
studies considered similar characteristics as LAA (color, with primary teeth, but less often (3 from 6 studies). Near-
luster, and texture), but did not use the point system pro- ly 50% of studies also presented a high or unclear risk of
posed by Ekstrand et al. [2007]. Seven studies were per- bias regarding the reference standard (Fig. 5; online sup-
formed with permanent teeth (63%). Six studies included pl. Table S5). The longitudinal studies presented a low
all tooth surfaces (55%), while 4 focused specifically on risk of bias considering all 3 domains evaluated (see on-
specific surfaces (online suppl. Table S2). line suppl. Table S5).

Summary Measurements Publication Bias (Both Reviews)


Reproducibility and Accuracy. Systems showed mod- Through funnel plots analyses (online suppl. Fig. S3),
erate to substantial values of pooled intra-RR (0.7; 95% CI we identified the occurrence of publication bias when test-
0.60–0.79) and inter-RR (0.65; 95% CI: 0.41–0.80). Lower ing the accuracy (DOR) in clinical studies involving pri-
reproducibilities seemed to be more frequent in those mary teeth (p < 0.001) and the correlation with histology
cases in which all surfaces were considered for analyses (p < 0.001). After the adjustment of pooled estimates, slight
instead of specific surfaces and/or more examiners were differences could be observed (see online suppl. Fig. S3).
involved. High levels of heterogeneity were observed
(I2 > 80%).
Four studies tested the accuracy of systems for caries Discussion
lesion activity assessment (online suppl. Table S3; Fig. 4).
The studies used a kind of criterion validity (concurrent An enormous interest in the ICDAS has been regis-
validity) inferring the pH in the plaque covering the le- tered since it was released in 2003–2004. A simple search
sion by using an appropriate impression material for ICDAS in PubMed conducted in January 2017 result-
[Ekstrand et al., 2007] or using methyl red, a solution ed in 264 hits.
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The collected data about reproducibility came from manent teeth, mostly teeth presenting special conditions
those studies that also examined the accuracy of the were extracted for histological validation, being consid-
ICDAS and indicated that both the intra- and inter-repro- ered a high risk of bias in clinical studies. On the other
ducibility of the ICDAS were substantial (Fig. 1). A few hand, when other validation methods (such as expert
additional studies only focusing on the reproducibility of consensus) were used in these studies, we could also in-
the ICDAS could have been included using other selection troduce a partial verification, and consequently a confir-
criteria. If these studies had been included, probably mation bias.
slightly different figures would have been observed. How- Another factor that may influence the accuracy is the
ever, we do not believe this option could have changed the choice of the reference system and the use of thresholds.
actual trend observed. Additionally, as only English stud- Different validation methods have been used (online
ies were included, we could point out another limitation suppl. Table S1). It may be very difficult to decide visu-
of this review. On the other hand, systematic reviews seem ally if a noncavitated lesion is deep in the enamel or just
not to have been impacted when non-English studies were into the dentine, which suggests it may be best to use
included [Juni et al., 2002; Moher et al., 2003]. enamel lesion or dentine lesion limited to the outer third
Although some studies do not optimally follow the versus deeper dentine lesion as the threshold [Ekstrand et
fundamental conditions for using the ICDAS (e.g., the al., 2007, 2011]. This threshold may boost the accuracy of
training of the examiner, cleaning and drying conditions) the system, but is relevant for managing the lesion, as sur-
[Topping et al., 2009], a substantial positive correlation gical intervention should mainly be restricted to lesions
between the ICDAS and histology was observed (rs ≥ deeper than the outer third of the dentine [Ismail et al.,
0.68). Many studies are performed on occlusal surfaces, 2015]. The variety of reference systems could be one ad-
but examinations on extracted teeth where the approxi- ditional explanation for the high level of heterogeneity
mal lesions can be classified also show a significant rela- observed among the studies.
tionship between the ICDAS scores and the lesion depth Different examiners’ expertise and types of training
[Ekstrand et al., 2011; Piovesan et al., 2013]. On the other can be another source of heterogeneity. Less experienced
hand, when excluding approximal lesions from analyses examiners tended to be less accurate in detecting caries
because they by nature are difficult to see, considerable when using visual inspection [Gimenez et al., 2015].
changes were observed in a clinical setting. However, we However, including all kinds of examiners in our analyses
would probably have an error type 2 if meta-regression provides the verification that the system can be used suc-
was used to show this because of the small number of cessfully in caries lesion severity assessment even for non-
studies. This is why we only presented the data by sensi- researchers.
tivity analysis. Studies which could approximate the results to the
The SROC curves pooled in the meta-analysis use clinic situation are limited when testing the accuracy of
thresholds to present the results, permitting an overall ap- the caries detection method because of issues regarding
preciation of method performance by means of DOR, the reference methods used for validation. Moreover,
combining sensitivity and specificity [Glas et al., 2003]. they are not free of bias [Gimenez et al., 2015]. Clinical
Pooled DOR values were very high in all subgroups. LRs studies showed a slight reduction in the examiners’ over-
indicated a slight to large increase on posttest probability all performance using the ICDAS (Fig.  2, 3), probably
of the disease [McGee, 2002], depending on the threshold caused by difficulties when examining under natural con-
and subgroup analyzed. These findings emphasize the ro- ditions. On the other hand, this finding is associated with
bustness of the ICDAS system for assessing caries lesion a high specificity, which could be beneficial and avoid un-
severity. necessary surgical treatment in practice.
One factor that could have an influence on the correla- One can debate the clinical significance of these stud-
tion with histology and performance is that the spectrum ies on accuracy. It is important to highlight that the
of sample disease does not always reflect the disease in the ICDAS has a high correlation with histology. It is also
population. This variation in disease prevalence may af- strongly associated with caries progression [Ferreira Zan-
fect estimates of diagnostic performance [Whiting, 2004]. dona et al., 2012; Guedes et al., 2014, 2016] and conse-
In fact, samples are usually chosen based on suspicious quently could be strongly related to clinical decision mak-
sites (probably more difficult to detect) and certainly a ing. The level of bias in the individual studies included in
larger proportion of such lesions are included than are this review certainly varies, and consequently their poten-
found in the real world. Additionally, especially for per- tial for clinical extrapolation. These aspects reflect the
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Assessment System – ICDAS DOI: 10.1159/000486429
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methodological heterogeneity present among data used ones. However, it takes more time and effort. Few longi-
in this paper. The authors would like to encourage the tudinal studies focused on how active lesions detected us-
inclusion of a consecutive sample, minimizing the selec- ing the ICDAS at baseline behaved after a couple of years
tion and spectrum bias, approximating the real condition [Ferreira Zandona et al., 2012; Guedes et al., 2014].
we tend to find in clinical practice with the sample. Com- In general, despite low progression rates, active caries
plete validation of the sample, noninfluenced by “test ex- lesions classified using the ICDAS had a higher risk of
aminations” is also recommended when accuracy is the progression than inactive ones [Ferreira Zandoná et al.,
issue. In the case of activity assessment, predictive valida- 2012; Guedes et al., 2014], indicating the predictive valid-
tion is desirable for guidance in designing further labora- ity of the activity assessment system. Therefore, the low
tory and clinical studies presenting low risk of bias (as positive predictive value found so far may not necessarily
shown in online suppl. Table S5). be related to the scoring system alone, but also related to
For the activity assessment of caries lesions, the avail- caries progression in the studied sample. In addition, the
able evidence is still limited. In general, 2 systems have findings related to activity assessment using the ICDAS
been added to the original ICDAS. Both take into consid- could not be generalized for all types of surfaces [Guedes
eration similar clinical features. One uses a combination et al., 2014], nor all the ICDAS scores [Ferreira Zandona
of predictors where the final assessment basically is sub- et al., 2012]. On the other hand, we should state that sub-
jectively based as suggested by other indices which con- group analyses were considered for that.
templates the activity assessment of caries lesions [Nyvad Lesion severity assessed with the ICDAS has been
et al., 1999; Kuhnisch et al., 2009]. The other system uses shown to be a strong predictor of lesion progression to
points predefined to the individual predictors (ICDAS- cavitation [Ferreira Zandoná et al., 2012; Guedes et al.,
LAA) and the final assessment is based on adding up the 2014]. However, the activity can be an important param-
points against a threshold. Thus, using the ICDAS-LAA eter to be evaluated in conjunction to the severity in cer-
would reduce the subjectivity in the assessment, which tain circumstances, for example occlusal noncavitated le-
could be a promising advantage. sions (especially the ICDAS score 2) or cavitated lesions
The studies for validating the methods for activity as- clinically into enamel (ICDAS score 3). Additionally, ac-
sessment of caries lesions are still mainly based on pH in/ tive caries lesions were found more frequently in children
at the lesion. In such a design, only concurrent validity of with high caries experience, evidencing also the construct
the system can be expressed. Moderate values of sensitiv- validity of this system [Guedes et al., 2014]. Further pro-
ity and specificity have been shown, pointing out some spective studies are desirable to guarantee stronger levels
shortcomings to be improved. As pooled DOR is signifi- of evidence for caries activity assessment.
cantly higher than 1, the test can give additional informa- Since diagnostic accuracy studies might not demand
tion about the disease [McGee, 2002]. However, LRs sug- previous registration, systematic reviews of these studies
gested a slight impact on posttest probability [Henderson could inflate the test accuracy if only positive results were
et al., 2012]. published [Song et al., 2002]. However, publication bias
These findings could also be affected by the method was only identified in a few analyses in our systematic re-
used in validation. Previous results suggested that the view. Using the trim and fill analysis, we tried to overview
methyl red dye underestimates the activity status of caries possible unbiased results by simulating possible unpub-
lesions [Braga et al., 2010]. In addition, when comparing lished results [Duval and Tweedie, 2000]. Actually, we
LAA with other systems (whether using the ICDAS in as- cannot affirm whether the funnel plot asymmetry is only
sociation or not), different studies suggested it can over- caused by publication bias, or also by the inherent vari-
estimate the activity status and/or need for management ability among the studies [Duval and Tweedie, 2000].
[Braga et al., 2010; Tikhonova et al., 2014; Floriano et al., However, we used this approach to investigate how our
2015; Oliveira et al., 2015]. However, none of these stud- findings could be influenced by this bias, trying to adjust
ies prospectively confirmed these findings. Additionally, for it. Mainly the larger studies tended to show a higher
we observed a high variability in design of the few includ- correlation to histology. On the other hand, using these
ed studies (see online suppl. Table S3). adjustments, results seem not in general to be affected as
Certainly, predictive validation would be the ideal the confidence intervals of adjusted and unadjusted esti-
strategy for checking the ability to correctly assess the car- mates are overlapping.
ies status of the lesions [Baelum, 2006], since we can To answer the question about advantages of the
check if future events are in accordance with the expected ICDAS, based on the available evidence we feel that it is
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416 Caries Res 2018;52:406–419 Ekstrand/Gimenez/Ferreira/Mendes/


DOI: 10.1159/000486429 Braga
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fair to state that the ICDAS is a robust caries scoring sys- Implications for Research
tem to assess the severity of coronal caries lesions. Even Clinical studies presenting a low risk of bias should be
though there are some limitations concerning activity as- encouraged, especially paying attention to sample acqui-
sessment of the lesions, the ICDAS showed both predic- sition to minimize sample spectrum bias, and offers a
tive and construct validity. The main limitation is that greater approximation to the real clinical situation. In ad-
there are no or very few studies concerning the ICDAS dition, the web page of ICDAS (http://www.icdas.org)
and caries adjacent to restorations, as well as the ICDAS and the monography [Pitts, 2009] are mandatory for de-
and root caries. tailed knowledge.
The training in the ICDAS is burdensome; on the oth-
er hand, it requires dentists and dental hygienists to add
Acknowledgements
several predictors together before the final activity assess-
ment can be performed. In this sense, the visual appear- This study was partially funded by a grant from Brazil (FAPESP
ances of the lesion (ICDAS scores), the location of the 2012/17888-1 and 2014/00271-7), CNPq (400736/2014-4), Capes.
lesion (in plaque stagnation areas or not in plaque stagna- The authors acknowledge feedback from Prof. Nigel Pitts,
Kings College, London, during the development of this paper.
tion areas), as well as the tactile feeling of the lesions are
the best predictors [Ekstrand et al., 2007]. Due to its sub-
stantial association between the external signs of caries Disclosure Statement
and the internal changes in the underlying tissue [Ekstrand
et al., 2007], the ICDAS can be used as an educational tool K.R.E. has participated in the development of ICDAS. The au-
for undergraduates. thors declare no financial conflict of interests.

Implications for Clinical Practice


Author Contributions
The ICDAS presented a substantial level of reproduc-
ibility and accuracy for assessing primary coronal caries K.R.E. contributed to conception and design, acquisition of the
lesions. Thus, the ICDAS is a robust caries detection sys- study, analysis and interpretation of data and drafted the manu-
tem in most of the conditions tested, encouraging its use script. T.G., F.R.F., and F.M.M. contributed to the data acquistion
and analysis of the data. M.M.B. contributed to acquisition, analy-
in clinical practice. Additional systems associated with sis, interpretation of data and drafted the manuscript. All authors
the ICDAS, which classify caries lesion activity, can be critically revised the manuscript, had final responsibility for the
useful as they are moderately reproducible and accurate. decision to submit, and approved the submitted version.

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