Knowledge about syphilis and its oral manifestations among dental students: a cross-sectional study from Brazil, 2019

Background: Clinical manifestations of the syphilis can occur in the mouth and in the perioral region. This study aimed to investigate the knowledge about syphilis and its oral manifestations among dental students and to discuss the role of the dentist in prevention and control of this disease. Methods: This is a cross-sectional study carried out with 171 dentistry students enrolled in the second, third, fourth and fth years in the rst semester of 2019 from the Federal University of Espírito Santo, Brazil. Data collection was performed by a questionnaire containing 16 questions answered by students in classroom. Analyses of absolute and relative frequency were performed. To perform association among variables, the Chi-square test (or Fisher's exact test with Yates correction) was performed with 5% signicance level. Results: Overall, 169 students participated in the study. Only 40 (46.4%) students correctly answered the question about disease stages. Almost all participants answered that syphilis has oral manifestations; however, only 44 (25.7%) answered the question correctly. Regarding differential diagnoses of other oral lesions, only 63 (37.3%) reported knowledge on this subject. There was a statistically signicant association between student’s educational level and knowledge about the etiological agent (p<0.0001), clinical manifestations (p<0.0001), disease stages (p<0.0001), oral manifestations (p<0.0001) and drugs (p = 0.005) related to the disease. Conclusions: Participants showed important gaps in their knowledge about syphilis and its oral manifestations. Our ndings, together with the increased number of new cases of the disease in the world, reinforce the need for training dental professionals with knowledge about early diagnosis, effective treatment and follow-up of syphilis cases.


Background
Syphilis is a sexually transmitted infection (STI), considered a public health problem and is among one of the most common communicable diseases, affecting the health and life of people around the world. In 2016, the global incidence and prevalence rate for this infection was 6.3 million and 19.9 million cases, respectively [1]. It is estimated that 60% or more of cases occurring in men who have sex with men, being strongly associated with HIV co-infection and high-risk sexual behavior [2].
The situation of syphilis in Brazil is not different; the number of cases of the infection is worrying.
Acquired syphilis, a condition of compulsory noti cation since 2010, had its detection rate increased from 59.1 cases per 100,000 inhabitants in 2017 to 75.8 cases per 100,000 inhabitants in 2018 [3].
The disease presents four distinct stages that are characterized by particular symptoms, clinical manifestations, and infectivity levels: primary, secondary, tertiary, and latent syphilis. Clinical manifestations can occur in the mouth and in the perioral region and primary and secondary lesions are highly contagious [4].
The main oral manifestations are hard chancre, mucous plaques and gumma. Oral chancre in primary syphilis is characterized as a painless ulcer, measuring 1 to 2 centimeters, with rm and rolled border [5].
It manifests as a single ulcer, usually on the lip or, more rarely, on the tongue [6]. Secondary syphilis presents multiple and generally symptomatic ulceration [7]. In these cases, lesions are maculopapular, affecting the hard palate and, sometimes, the soft palate. Gumma, associated with tertiary syphilis, initially manifests as one or more painless swelling, especially on the hard palate [8].
For this reason, in many cases, the dentist is the professional who makes the diagnosis of this pathology, and therefore plays an extremely important role in contributing to the effectiveness of diagnosis, control and treatment, through the identi cation of its signs and symptoms, guiding the patient in relation to procedures, treatment support and follow-up [4].
In addition, treponema pallidum can be transmitted by blood if the individual is exposed to infected blood and body uid [9,10]. This possibility of non-sexual transmission makes the dentist to be among health professionals most at risk of contamination, as accidental contact with saliva and blood may occur during clinical practice. In addition, the risk is greater when considering that 9 out of 10 patients with syphilis do not present any clinical manifestations, although they remain infectious or unaware about the infection (CDC) [11,12] In May 2016, the World Health Assembly adopted the 2016-2021 strategy of the global health sector for STIs. This strategy includes expanding evidence-based interventions and services to control syphilis and reduce its impact as a public health problem by 2030 [13]. Our goal is to provide data that generates insights that help create interventions to combat and prevent syphilis in the Brazilian and international scenario.
Given the above and considering the importance of academic formation that allows the insertion of dentists in multiprofessional teams for diagnosis and treatment of STIs [14] and that the knowledge may in uence attitudes and behaviors [15], the aim of this study was to investigate the knowledge about syphilis and oral manifestations among dental students and to discuss the role of the dentist in prevention and control of this disease. Methods This is a cross-sectional study conducted with dental students from a Federal University of Espírito Santo (UFES), Brazil. UFES is located in the capital of the state of Espírito Santo in southeastern Brazil and is the only public university in the state. In 2018, the detection rate of acquired syphilis in Espírito Santo was 114.1 cases per 100,000, higher than the rate for Brazil for the same year [3].
The sample universe was composed of all students enrolled in the second semester of the second (27), third (65), fourth (55) and fth (44) years of the rst semester of 2019, including 171 students. Students in the rst year and rst semester of the second year (third period) were excluded for not having taken the Stomatology discipline, which o cially addresses the content discussed in this study. Data were collected through a self-administered questionnaire with closed questions, specially designed for the research. Research subjects were included in the study based on two criteria: accepting to participate in the study and being present in classroom on the day the study was carried out. Students did not know that they would be asked about syphilis and its oral manifestations on the day they were approached. The questionnaire was applied in collective mode in classroom at time considered appropriate and convenient to students, with guarantee of privacy and con dentiality of information collected from March to May 2019.
The questionnaire was developed in Portuguese and translated into English for the presentation of this research. The scienti c literature [16][17][18][19] and guides from the Brazilian Ministry of Health [20] and the Centers for Disease Control and Prevention [21] were consulted to build the questionnaire. The nal version containing 16 questions about identi cation (sex, age), school year and aspects related to knowledge about syphilis (what is it, agent etiology, forms of transmission, clinical manifestations, disease stages, oral manifestations, differential diagnoses and drugs used for treatment).
A pilot study was conducted with rst-year dentistry students to ensure suitability, validity, and interpretation of answers. On the basis of comments and suggestions obtained, the questionnaire was revised. During the pilot study, researchers aimed to assess the understanding of students regarding the text, sensitivity of responses and vocabulary used. At the end, two experts were consulted to express their opinion on the nal version of the instrument.
Questionnaire data were entered into the IBM SPSS Statistics for Windows 19.0 software package by two researchers, respecting the con dentiality of information. An independent researcher reviewed 10% of database entries, validating them for the analysis phase. Data were statistically analyzed through absolute and relative frequency. To perform the association among variables, the Chi-square test (or Fisher's exact test with Yates correction) was performed with 5% signi cance level. This project was approved by the Ethical Committee of the Department of Science, Federal University of Espírito Santo, Brazil. All participants who agreed to participate in the research signed the Free and Informed Consent Form.

Results
Of the total of 171 students, questionnaires were completed by 169, for a response rate of 98.8%. Of the respondents, 129 (75.1%) of whom were female and 139 (81.9%) aged under 25 years (Table 1). they reported that the appearance of chancre is common in the primary disease stages (Graph1).
Regarding the different diagnoses with other oral lesions, only 63 (37.3%) claimed to know them and of these, only 12 (19.3%) correctly responded the question (Hairy Leukoplakia). One hundred and ten students (63.3%) knew that the main form of treatment is penicillin (Graph 1).
There was a statistically signi cant association between student's educational level in the Dentistry course and knowledge about etiologic agent (p<0.000), clinical manifestations (p<0.000), disease stages (p<0.000), oral manifestations (p<0.000) and drugs (p = 0.005) related to syphilis. Students enrolled in the early years had better knowledge about the disease than students in the nal years (Table 2).  [14] reported that although many Brazilian universities present their curricula aimed at general knowledge, they often have not adequately prepared students to recognize and diagnose complex clinical conditions, such as those presented by syphilis.
In this perspective, few students know the oral manifestations of syphilis. In agreement with our research, when investigating knowledge about occupational blood-borne pathogen among Chinese dentistry students, Wu et al. [15], 2016 found that less than half of participants were able to recognize the main oral manifestations of syphilis Recognizing the oral manifestations of syphilis is a crucial role of the dentist, because as oral lesions are highly contagious, the reliability of the correct diagnosis helps in the adequate management, reduces the infection chain and reduces the risk of transmission to health professional [22]. It is worth mentioning that the least registered form of transmission by students was through clinical dental practice in view of exposure to contaminated blood or saliva. This occurs when correct professional practice is not established [4,12].
In addition, a small percentage of students reported knowledge about the differential diagnoses of oral manifestations of the disease. Indeed, studies have shown that the diagnosis of oral manifestations of syphilis represents a challenge for professionals because they have a variety of clinical appearances [23,24]. The fact that some characteristics may be similar to other conditions is of concern, and if diagnosis is not performed in the primary and secondary stages, the patient is exposed to the risk of complications related to the tertiary stage [23].
Our study also showed that students enrolled in the early years of the Dentistry course had better knowledge about etiologic agents, clinical manifestations, disease stages, oral manifestations and drugs than students enrolled in the last two years. The only association that was not statistically signi cant was in relation to differential diagnosis, where knowledge was low for both groups.
Unlike this research, studies that investigated the knowledge of dental students about HIV / AIDS [25][26][27] and occupational of blood-borne pathogens [28,29] showed that knowledge about some aspects was greater among students with higher educational level. Keser et al. [25] justi ed this nding by the fact that the older group may have gained more experience over the years and was exposed to larger number of patients compared to the younger group. Brailo et al. [29] reported that this nding can be explained by the fact that in the clinical phase, at the beginning of the clinical practice in each department, students are introduced to this content again.
Usually, in the st years of the Dentistry course, students have the Stomatology discipline, which addresses the content about syphilis and it' s oral manifestations. However, it is essential that this content is addressed in other moments and disciplines throughout the undergraduate course, so that students are aware of all aspects that involve the disease, regardless of the educational level they are attending.
A fact that attracted attention was that studies on knowledge about the transmission of blood-borne pathogens among dental students conducted by Myers et al. [28] and Brailo et al. [29], published in 2012 and 2011, respectively, did not address syphilis. The study by Wu et al. [15], published in 2016, included the disease, probably due to its increasing prevalence worldwide. Syphilis started to become evident again a few years ago, so many clinicians do not consider syphilis in their differential diagnosis of oral lesions [30]. In Brazil, the disease has shown signi cant increase in incidence since 2010. The detection rate of acquired syphilis increased from 2.1 cases per 100,000 inhabitants in 2010 to 75.8 cases per 100,000 inhabitants in 2018 [3].
The number of participants who recognized penicillin as the drug of choice for treatment was less than expected. Penicillin became universal as an effective way of treating syphilis and was responsible for the signi cant decrease in the epidemiological numbers of the disease. The effective cure of syphilis with penicillin and the decrease in cases over time, that is, the positive result in coping with the disease gradually left a signi cant gap in medical and dental education. [14].
The study has limitations due to its cross-sectional design, which prevented establishing cause and effect relationships. In addition, the study was conducted in only one teaching institution. However, to the best of our knowledge, this is the rst study to analyze the knowledge of dentistry students about syphilis and its oral manifestations. Our ndings, together with the increased number of new cases of the disease in the world, reinforce the need for training dental professional with knowledge about early diagnosis, effective treatment and follow-up of syphilis cases. As the main form of infection transmission is sexual, its diagnosis and treatment must consider socio-cultural and ethical scope. The disease has repercussions on the affected people's way of life, and this issue should also be addressed during the undergraduate courses [31].
It is necessary to raise the student's interest not only in the clinical aspect of the disease, but also in care issues. Improving students' knowledge can be an effective way to increase the willingness to treat patients [15]. However, it is necessary to seek educational methods that can improve student's experience and learning skills.

Conclusions
Participants showed important gaps in their knowledge about syphilis and its oral manifestations.
Knowledge was associated with student's educational level during the undergraduate course. Our results support the request to improve/include syphilis and its oral manifestations in the curricula of Dentistry Education Institutions. We believe that this is an important intervention that can help control and prevent this disease in scenarios where it is prevalent.

Declarations
Ethics approval and consent to participate This project was approved by the Ethical Committee of the Department of Science, Federal University of Espírito Santo, Brazil (number: 2.801.172). All participants who agreed to participate in the research signed the Free and Informed Consent Form.

Consent for publication
Not applicable.

Availability of data and materials
All data generated or analysed during this study are included in this published article Further data may be requested by contacting the corresponding author. Any data regarding the study will be willingly provided.
Competing interests