Abrahamian 2022
Abrahamian 2022
DOI: 10.1111/jcpe.13618
ORIGINAL ARTICLE
1
Department of Periodontology, Universitat
Internacional de Cataluña, Barcelona Abstract
2
ETEP (Etiology and Therapy of Periodontal Aim: To evaluate the inter-examiner reliability in classifying periodontitis using the
and Peri-Implant Diseases) Research Group,
2018 classification of periodontal diseases, when used by postgraduate students, aca-
Complutense University of Madrid, Madrid,
Spain demics, and specialist clinicians trained in European Federation of Periodontology (EFP)
and American Academy of Periodontology (AAP) postgraduate-accredited programmes.
Correspondence
Lucía Barallat, Department of Periodontology, Materials and Methods: An online survey including five patients with periodontitis
Universidad Internacional de Cataluña,
was sent twice to seven specialists in periodontology to provide the staging and grad-
C/Josep Trueta s/n, Sant Cugat del Vallès,
Barcelona 08195, Spain. ing characteristics. After agreeing on a “gold-standard” classification, the same ques-
Email: [email protected]
tionnaire was sent to 16 EFP and 73 AAP postgraduate programmes, to be answered
Funding information by their faculty, graduates, and students. The responses were compared with the gold-
The study was initiated and solely based on
standard classification, and the inter-examiner agreement was calculated.
institutional funding.
Results: One-hundred and seventy-four participants completed the survey. The
inter-examiner agreement resulted in 68.7% in assigning the stage, 82.4% in assigning
the grade, and 75.5% in assigning the extent. The academic position and the experi-
ence of the participants did not have any significant influence on classifying peri-
odontitis as the gold standard.
Conclusions: The use of the 2018 periodontitis classification resulted in high inter-
examiner reliability when used by a specialist group of clinicians, postgraduate stu-
dents, and academicians, irrespective of their current position and experience. Given
the low response rate and potential selection bias, results pertaining to the use of this
system in classifying periodontitis should be interpreted with caution.
KEYWORDS
classification, diagnosis, periodontal diseases, periodontitis, survey
Clinical Relevance
Scientific rationale for study: A new periodontitis classification scheme was adopted during the
2018 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Con-
ditions, in which “periodontitis” is further characterized based on a multi-dimensional staging
and grading system. There is a need to assess the reliability of this classification.
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any
medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
© 2022 The Authors. Journal of Clinical Periodontology published by John Wiley & Sons Ltd.
Principal findings: The 2018 classification of periodontitis has a very high inter-examiner reliabil-
ity in a specialist group of postgraduate students and periodontists.
Practical implications: These results suggest that this new classification can be used accurately to
classify periodontitis. However, given the potential low response rate and selection bias, caution
is needed in interpreting results.
FIGURE 1 Representative example of a case in the survey. FMBS, full-mouth bleeding score; FMPS, full-mouth plaque score
the World Workshop on the Classification of Periodontal and Peri- electronically the survey was sent to the programme directors, who
Implant Diseases and Conditions” (Caton et al., 2018; Papapanou were asked to forward it to their faculty, graduates, and postgraduate
et al., 2018; Tonetti et al., 2018), following the associated algorithm students. Respondents were then categorized according to their aca-
developed by Tonetti and Sanz (2019) and by responding to close- demic position and experience into postgraduate students, specialist
ended questions. The online survey documents including the five cases clinicians, and university faculty. Postgraduate students were consid-
were created in English using the Google Forms platform from April to ered dentists currently enrolled in the periodontology masters of the
May 2020. Once the survey was completed, the answers were saved accredited programmes, while specialist clinicians were considered
and visible to a single examiner (Lory Abrahamian). board-certified periodontists who are dedicated to private practice
and are not involved in academics. University faculty were considered
as periodontists currently teaching in the accredited programmes;
2.2.1 | Experts0 evaluation they could also sometimes be alumni of the respected specialist pro-
gramme but not necessarily.
The first step included the evaluation of the survey by seven interna-
tionally recognized experts in the field from the UIC and from the Uni-
versity Complutense of Madrid (José Nart, Cristina Valles, Andrés 2.3 | Statistical analysis
Pascual, Lucía Barallat, Mariano Sanz, David Herrera, and Elena
Figuero). The survey including the five cases was sent twice, with a The primary outcome variable was the agreement of the staging, grad-
minimum timespan of 7 days from the first classification. Then, in June ing, and extent with the established gold-standard classification. Sec-
2020, an agreement on the periodontal classification on each case was ondary outcomes, considered as potential explanatory outcomes,
set up among these experts by open discussion in videoconference were the years of experience and the academic position.
where the final reference classification was established and considered In the first part of the study, the intra-examiner reliability of the
as the gold-standard classification for the second part of the study. seven experts developing the gold standard was evaluated by calcu-
lating the percentage of concordance and the kappa score. This was
calculated at the first and second classifications of any expert, with-
2.2.2 | General survey out any distinction between experts. Subsequently, the intra-
examiner agreement was attained by comparing any expert's
In the second phase, the same survey was sent to 16 EFP- and response between the first and second “diagnoses.” For the extent,
73 AAP-accredited postgraduate programmes. The link to access unweighted kappa scores were calculated, while for the stage and
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ABRAHAMIAN ET AL. 735
Note: Unweighted kappa for extent and weighted kappa for stage and Case 4 III C Generalized
grade. Case 5 III B Localized
Abbreviation: CI, coefficient interval.
dence interval (CI). Reference categories were determined as “special- Note: Absolute frequency and percentage: n (%).
ist clinician” and “<5 years of experience.”
Sample size calculation resulted in the estimation of 90 partic-
ipants, assuming an expected 70% agreement, which was consid- 3.2 | General survey
ered as substantial (α risk = 5%, β risk = 10%) in a bilateral
contrast, and a response rate of 30%. The level of significance The “Periodontitis Cases Online Survey” was completed by 174 partic-
was set at .05. The version 3.5.2 of the software R was used for ipants, 58.7% being male and 39.4%, between 30 and 39 years of age.
all analyses. The sociodemographic characteristics of the sample are presented in
Table 3.
3 | RESULTS
3.2.1 | Inter-examiner agreement
3.1 | Experts
The comparison of the participants' responses to the gold standard
3.1.1 | Intra-examiner agreement resulted in an overall percentage of agreement of the stage of 68.7%,
the grade of 82.4%, and the extent of 75.5%.
The intra-examiner reliability by the experts' evaluation resulted in Neither the current academic position nor the experience of the
82.30% concordance in the stage (kappa score = 0.71, 95% CI [0.48– participants had a statistically significant influence on the level of
0.93]; p < .001), 91.40% concordance in the grade (kappa score = 0.85, agreement (p > .05). Table 4 shows the absolute frequencies and per-
95% CI [0.71–0.99]; p < .001) and 83% concordance in the extent centages of agreement of the different categories when comparing
(kappa score = 0.52, 95% CI [0.17–0.87]; p = .001) (Table 1). with the gold standard.
The resulting “gold-standard” classification corresponded to four A logistic regression model (Table 5) was used to analyse the interac-
cases defined as stage III and one case as stage IV; four cases were tion of the different variables and showed a statistically significant
generalized while one was localized (Table 2). lower probability of agreement on the grade for university faculty
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736 ABRAHAMIAN ET AL.
TABLE 4 Absolute frequency and percentage of agreement comparing with gold standard
Note: Logistic regression model used. The odds ratio of the probability of agreement of university faculty and postgraduate students was calculated taking
as a reference the clinicians.
Abbreviations: CI, coefficient interval; OR, odds ratio.
*Bold values are Statistically significant (p ≤ .05).
(OR = 0.09, 95% CI [0.00–0.49]; p = .023) and postgraduate residents seem to indicate that this new classification framework can be suc-
(OR = 0.12, 95% CI [0.01–0.63]; p = .045) compared to specialists. In cessfully used to diagnose periodontitis cases, which was reflected by
other words, the odds of reaching an agreement with the gold stan- the high concordance (>80%) between repeated diagnoses in the
dard for grade was approximately 11 times lower for university faculty group of experts and by the high percentage of correct diagnoses in
than clinicians and approximately 8 times lower in postgraduate stu- the general survey. However, it was more likely to reach a correct
dents than clinicians. grade classification (85%), followed by the extent (75.5%), and, finally,
the stage, which was the most difficult to assess (68.7%).
One of the objectives of this investigation was to determine
4 | DISCUSSION whether expertise or the academic position could have an impact on
the classification. However, the reported results show that neither the
Every new classification system involves a learning curve, and this current position nor the experience of the periodontist influenced the
process may require some years. Hence, training, implementation, and outcomes, which further decreases the probability of diagnostic bias.
practice are fundamental to avoid misclassification and incorrect We can interpret this finding in three different ways: first, this classifi-
treatment plans (Hefti & Preshaw, 2012). Furthermore, inconsistency cation is simple enough to be accurately implemented outside of the
in defining the different periodontitis categories can lead to incongrui- academic setting; second, training does not require previous experi-
ties in their prevalence, severity, and extent in epidemiological studies ence in the field; and third, transitioning from the previous classifica-
(Borrell & Papapanou, 2005; Page & Eke, 2007; Costa et al., 2009). tion can be done rather smoothly by the older generation of
For this reason, the purpose of this observational study was to assess periodontists. Interestingly, the comparison between categories
the intra- and inter-examiner reliability in diagnosing periodontitis showed an effect of clinical experience on the assessment of the
cases among specialist clinicians, faculty, and postgraduate students grade, as university faculty and postgraduate students demonstrated
following the criteria of the 2018 World Workshop on the Classifica- a slightly lower probability of determining the correct grade, com-
tion of Periodontal and Peri-Implant Diseases and Conditions. The pared to clinicians. Although specialist clinicians had a statistically
results from the present study have demonstrated a high level of significant greater probability of correct assessment of the grade
validity and reliability in a sample of postgraduate students and spe- than postgraduate students and university faculty, the odds were still
cialists from EFP- and AAP-accredited programmes. These findings very low and maybe not clinically relevant.
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ABRAHAMIAN ET AL. 737
These results are in line with the study of Marini et al., (2020) three of which were directly involved in the development of this clas-
where 30 participants of various education levels were recruited to sification system. In addition, this study also assessed the consistency
evaluate 25 periodontitis cases. The sample consisted of undergradu- across time for every expert, which is also important in daily practice
ate students, general dentists, and periodontal experts. Although the to establish a consistent treatment plan (Hefti & Preshaw, 2012).
sample from the present study was larger, it did not include under- The major limitation of this study was the use of an online survey
graduate students or general dentists. The periodontal experts' group sent indirectly by the programme director of each of the accredited
in this study found a substantial agreement when comparing to a programmes, which limited our ability to calculate the response rate,
gold-standard classification for the stage (82%), the grade (72.4%), thus potentially entailing a selection bias. In fact, the survey was sent
and the extent (84%). This result is comparable with the results from to 89 programmes and resulted in 174 participants completing the
the present investigation, mainly for the grade (82.4%) and for the study. Although 174 replies seem low, sample size calculation had
extent (75.5%), while it is slightly lower for staging (68.7%). Although resulted in 90 participants, making the final sample adequate. How-
both studies have shown good reliability for staging and grading, the ever, we were able to estimate a response rate of 27% as
lower percentages in the staging in this investigation can be explained 11 programmes confirmed their participation to the survey via email,
by the presence of only stages III and IV, as the distinction between resulting in 550 possible respondents. If we also consider that 5% of
stage III versus IV seems to be more difficult than the distinction programmes did not confirm their participation but still forwarded the
between stages I and II versus III and IV (Marini et al. 2020). Similar survey link to their alumni, this could result in 750 possible respon-
conclusions was made by Kornman and Papapanou (2020), who dents. Moreover, the anonymity of the participants could have
highlighted ground rules, clarifications, and “grey zones” for the clini- resulted in a selection bias across participants and specialist
cal application of this new classification, emphasizing the need for programmes, favouring those more familiar with the classification,
a collective assessment of the potential complexity factors for the thus overestimating the agreement. Furthermore, it could not be eval-
determination of the stage, rather than a mere “checking of a box” uated whether there was a clustering of responses by programme, as
approach of isolated features. They also added that a correct the survey was completely anonymous. Of the 11 programmes that
implementation of the staging system requires a nuanced, thorough confirmed their participation to the survey by email, there were
interpretation of a broad array of findings by a knowledgeable clini- six EFP and five AAP programmes. Furthermore, during the response
cian. In this investigation, the participants were asked to use the acceptance phase of the survey (1 month), some important clarifica-
algorithm developed by Tonetti and Sanz (2019) as an aid to reach tions and updates were published, possibly changing the decision-
the classification and to develop a treatment planning following the making process between the first responders and the last responders
recently published treatment guidelines for the different stages of the (Sanz, Herrera, et al., 2020; Sanz, Papapanou, et al., 2020). In light of
disease (Sanz, Herrera, et al., 2020; Sanz, Papapanou, et al., 2020). this new publication, one important clarification was that the assess-
These “grey zones” were further highlighted in a similar online ment of extent should be made after stage determination and should
case-based study by Ravidà et al., in which 103 clinicians with prior describe the percentage of teeth at the stage-defining severity level
training in the new periodontitis classification classified 10 severe (Sanz, Herrera, et al., 2020; Sanz, Papapanou, et al., 2020). This might
periodontitis cases (Ravidà et al., 2021). The raters in this study explain the difference in the group of experts in assessing the stage
achieved an inter-examiner agreement of 76% for stage, 82% for and the grade between the first and the second time. Stage assess-
grade, and 84.8% for extent. This data are in line with the results from ment may be particularly tricky, mostly for distinguishing between
the present investigation as raters in both studies achieved very simi- stages III and IV. The reason might be in calculating the number of
lar agreements for stage, grade, and extent. Moreover, the authors teeth lost due to periodontitis, which constitutes the main severity
identified five common grey zone factors that reduced rater consis- factor differentiating stage III from stage IV. This assessment should
tency by inviting the raters to submit queries concerning the selected also include hopeless teeth, which can be difficult to appropriately
cases. The said factors were the main determinants for identifying the define (Sanz, Herrera, et al., 2020; Sanz, Papapanou, et al., 2020).
stage, the definition of hopeless teeth, the differentiation between Moreover, complexity factors such as masticatory dysfunction might
stage III and IV, the shift between the stages, and the assignment be hard to diagnose. These factors can be considered rather
of the extent. In agreement to the authors' suggestions and in order judgemental in nature and could explain the difficulty in assessing the
to improve the classification agreement, identification of diagnostic stage. Moreover, the periodontal chart used in this study reveals the
challenges and complexities is required to promote the training of probing pocket depth and the recession and indirectly permits the cal-
clinicians. culation of the CAL, which can lead to mathematical errors. Finally,
One of the main strengths of the present study is the sample, the objective of this preliminary study was to assess the validity of
consisting of 174 participants from accredited periodontal training the 2018 periodontitis classification in a specialist population. Another
programme from both Europe and North America with different pro- study including general dentists could be eventually contemplated in
fessional backgrounds, academic positions, and experiences. This the future.
study evaluated the inter-examiner agreement not only between par- In conclusion, notwithstanding the low response rate, the poten-
ticipants but also in comparison to a gold-standard classification, tial selection bias, and clustering of the responses by programme, the
determined by a group of seven internationally recognized experts, data suggest that the use of the 2018 World Workshop on the
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Sanz, M., Papapanou, P. N., Tonetti, M. S., Greenwell, H., & Kornman, K.
Barallat, L., Valles, C., Herrera, D., Sanz, M., Nart, J., & Figuero,
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