Problem-based learning in dentistry : Diagnostic capability of dentists in the detection of calcified carotid artery atheroma on digital panoramic radiographs

Objective: The aim of this study was to evaluate the diagnostic capability of dentists in the identification of suggestive images of calcified carotid artery atheroma (CCAA) on panoramic radiographs (PRs) before and after using a problem-based learning method (PBL). Methodology: Five dentists (no specialists in oral and maxillofacial radiology) analyzed 102 digital PRs divided into: PRs with suggestive images of CCAA (n=51) and without suggestive images of CCAA (n=51). After the first analysis, the examiners attended an activity on soft tissue calcifications using the PBL method. Afterwards, they analyzed the 102 PRs again. The results of the analysis were calculated using the Cohen's Kappa Test and the Receptor Operational Characteristic Curves (ROC). Results and Discussion: Regarding examiners’ performance before and after the activity, the intra-examiner test showed reasonable Kappa coefficients (0-0.40). For inter-examiner agreement after the activity, the Kappa coefficient was almost perfect (> 0.80). When comparing examiners’ performance after the activity with a template performed by an experienced radiologist, the Kappa Coefficient was > 0.80 with significant agreement (p<0.05). Conclusion: The precision and the probability of correctly detecting suggestive images of CCAA on PRs increased when the examiners participated in the active pedagogical method. The continuing education of the dentist and how it can make a difference in the systemic health of patients should be considered.


Introduction
Heart disease and stroke are the two most common causes of death worldwide. In 2017, 17.7 million people died of heart disease, of which 6.7 million died from stroke (World Health Organization, 2017). Ischemic stroke is caused by atherosclerosis, which is a chronic inflammatory disease characterized by the narrowing and loss of elasticity of blood vessels, in which fat deposits, called atheromas, adhere to the inner layers of the arteries, reducing blood flow (Wakabayashi, 2010). Calcified atheromas start to form after the deposition of small crystals of cholesterol that grow (in size and volume), leading to increased calcium deposition and production of fibrous tissue by fibroblasts. This causes hardening of the arteries and results in the formation of the calcified carotid artery atheromas (CCAAs) (Bayram et al., 2006). These calcifications can be incidentally identified in dental imaging exams, such as panoramic radiographs (PRs). It is called an incidental finding since this radiograph is not indicated for this purpose. However, it can be an important tool for early diagnosis atherosclerotic disease. For dentists and patients, there is no additional effort as this type of radiography is part of daily clinical practice (American Dental Association, 2004;American Dental Association Council on Scientific Affairs, 2006). In PRs, suggestive images of CCAAs are described as nodular and heterogeneous masses, independent of the hyoid bone and epiglottis, located below, above or between the spaces of the intervertebral discs C3 and C4 or at an angle of 45 with the angle of the mandible (MacDonald et al., 2012;Roldán-Chicano et al., 2006). However, some radiopacities such as calcified triticeal cartilage and the superior Research, Society and Development, v. 9, n. 11, e70991110451, 2020 (CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v9i11.10451 5 horn of a calcified thyroid cartilage can be confused with CCAAs (Carter, 2000;Kamikawa, 2009).
The thyroid cartilage is a hyaline cartilage that shows a physiological process of calcification with advancing age. In PRs, it can be seen as a vertical calcification approximately 4 mm wide and 15 mm long, medial to the image of the C4 vertebra (Carter, 2000;Kamikawa, 2009). On the other hand, the triticeal cartilage is the smallest cartilage in the laryngeal skeleton, usually appearing in PRs as a round calcification within the pharyngeal air space and adjacent to C3 or C4, approximately 3 mm wide and 7 mm long (Carter, 2000). It is also hyaline and shows the same physiological process of calcification with advancing age (Carter, 2000). No treatment is needed for these calcifications. However, patients with CCAAs need further medical attention to avoid ischemic strokes (Ertas & Sisman, 2011).
As shown, calcifications in the soft tissues of the neck can be seen in the PRs favoring the early diagnosis of heart and vascular diseases. However, many dentists are unaware of the appearance of these alterations in imaging exams and this screening is not part of the routine of most of them. This work discusses the importance of continuing education for dentists and how it can make a difference in patients' systemic health. The study was conducted using a problembased learning method (PBL) on soft tissue calcification in PRs and evaluated the diagnostic capability of dentists in the identification of CCAA suggestive images on PRs before and after using this method.

Methodology
This retrospective and observational study was approved by the local Committee on General dentists, with no master's/doctorate, specialization or postgraduate studies in Oral and Maxillofacial Radiology were considered. For this, the graduates (last five years) of the undergraduate course in Dentistry at the university (UEM) were contacted through their records and an invitation to participate in the research was sent by email. Some did not return our contact, others refused to participate, and some had a graduate degree in Radiology and therefore were excluded from the sample. Finally, five dentists voluntarily agreed to participate in the research and signed the consent form.
The 102 images and instructions were shared with the participants through a cloud storage service. Examiners were instructed to analyze images in a semi-dark and quiet room and to take breaks between analysis to avoid eye fatigue. They were instructed not to seek help on the internet, in textbooks or with other colleagues. They had access to all images for a period of one month, when the results of this first analysis were recorded. The one-month deadline was given as there were a large number of PRs and the examiners had no experience with radiology. In addition, each volunteer did not have access to the data or knew the identity of the other participants in order to avoid communication. Also, the radiographs were randomly numbered for each examiner. Finally, the deadline was extended to respect the routine of each volunteer.
Fifteen days later, a resident of oral and maxillofacial radiology gave a lecture and training on soft tissue calcifications detected in PRs to all examiners. Special attention was paid to the CCAAs. The pedagogical method used was the PBL, which is a technique that situates learning in a problem-solving context, where students learn by solving problems and reflecting on them (Tamblyn & Se, 1981). This was done in approximately 4 hours, in person.
Finally, all examiners analyzed the 102 PRs again following the same guidelines as the first assessment. The same deadline for the evaluation was established, counting from the PBL activity. The performance of the examiners was then compared to a template developed by the experienced radiologist who performed the first evaluations. Research, Society and Development, v. 9, n. 11, e70991110451, 2020 (CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v9i11.10451

Statistical analysis
In order to identify possible differences in the prevalence of CCAA suggestive images between sex and age groups, the Chi-Square test was used. Cohen's Kappa Test was applied to test intra and inter-examiner calibration. Receptor Operational Characteristic Curves (ROC) evaluated the examiners performance in diagnosing suggestive CCAA on PRs after the activity.
The performance of the examiners after the activity was compared with the radiologist's template using Cohen's Kappa Coefficient. All statistical tests were performed with the R 3.6.2 software (R., Auckland, NZL) at a 5% level of significance (p < 0.05).

Results and Discussion
The prevalence of CCAA suggestive images according to sex is showed in table 1.
Although no statistically significant differences were found between unilateral (right/left sides) and bilateral cases in reference to sexes, women were more affected. Individuals with > 60 years were also more affected, despite no statistically significant differences being found (Table 2).  Regarding examiners' performance before and after the activity, the intra-examiner test (Table 3) presented reasonable Kappa coefficients (0 -0.40) (Landis & Koch, 1977;Stojanović et al., 2014), showing that the intra-examiner agreement was purely random (p> 0.05), which means that the examiners' diagnosis after the activity was dissimilar. Regarding the interexaminer agreement after the activity, the Kappa coefficient was almost perfect (> 0.80) (Landis & Koch, 1977;Stojanović et al., 2014); the null hypothesis that the agreement is purely random has been rejected (p <0.05). When analyzing whether the examiners' performance after the activity suffered positive or negative effects, the results were compared with the radiologist template and tested by Cohen's Kappa Coefficient, which was almost perfect (> 0.80) (Landis & Koch, 1977;Stojanović et al., 2014), with significant agreement (p <0.05) (Table 4), demonstrating significant effects of the PBL for the diagnosis of CCAA suggestive images on PRs.    Atherosclerosis can be an asymptomatic disease and early diagnosis is essential to decrease the risk of ischemic strokes (Gaba & Bulbulia, 2019). The gold standard exam for the diagnosis of CCAAs is the carotid doppler ultrasonography (Madden et al., 2007). Although PR is not the exam indicated for the detection of CCAAs, these calcifications can be identified when this exam is requested for other reasons. In addition, PR is one of the most used exams in dentistry (Ertas & Sisman, 2011). For this reason, dentists have an important role in the early diagnosis.
PR is an exam that covers the jaws, facial bones, teeth, and some neck structures with low radiation exposure (Bayer et al., 2011). It shows the critical region of the carotid artery (Bayer et al., 2011) and can be a valuable tool to identify calcifications that indicate cardiovascular disease (Henriques et al., 2011). However, it can be confused with other calcifications, such as that of triticeal cartilage (Wakabayashi, 2010). Carter (2000) described differences between CCAA and calcified triticeal cartilage in PRs. CCAAs appear as irregular and heterogeneous radiopacities, more laterally, while calcified triticeal cartilage appears as a homogeneous oval-shaped radiopacity (Carter, 2000). In case of doubt, an anteroposterior radiography such as the modified Towne technique can be requested (Ahmad et al., 2005). It allows CCAA suggestive images to be seen laterally to the vertebrae, while the calcified triticeal cartilage overlaps these structures (Ahmad et al., 2005).  (Madden et al., 2007). In another study comparing PR and CT scans, the accuracy, sensitivity and specificity of PRs in the detection of CCAAs were 62.3%, 22.2% and 90.0%, respectively (Yoon et al., 2008). In a recent meta-analysis (Schroder et al., 2019), the accuracy of PRs in detecting CCAAs was good to excellent in half of the studies with doppler ultrasonography as the reference standard. However, the accuracy was poor when angiography was used as the reference standard (Schroder et al., 2019).
Unlike these studies, where PRs were compared with other imaging exams, we assessed the dentists' abilities to identify CCAA suggestive images before and after the implementation Therefore, it contributes to improve the educational process (Al-Madi et al., 2018;Oderinu et al., 2019;Moreira et al., 2020). In our study, the PBL method improved the examiners' ability to detect images suggestive of CCAAs in PRs. Therefore, we emphasize the importance of continuing education for health professionals. When dentists have the opportunity to learn more about soft tissue calcifications, the systemic health of patients can be positively affected.
It is worth mentioning that our sample is very standardized, since all PRs were cautiously conducted by a single radiologist with a standardized protocol. However, one limitation of our study was that most studies compare PRs with other imaging methods in the diagnosis of calcifications, making it difficult to compare results. To our knowledge, there are no studies that evaluated the diagnostic capability of dentists in identifying soft tissue calcifications, mainly CCAA suggestive images.

Conclusion
According to our results, the precision and the probability of correct detection of CCAA suggestive images on PRs increased when examiners were submitted to an active pedagogical method.