Biosafety Measures in Clinical Practice During the COVID-19 Pandemic

National and international guidelines existed before the COVID-19 outbreak to prepare dental staff for the different biological risks inherent to the profession. ^{Reference Silveira, Fernandez and Tillmann15} In the last decade, cross-sectional studies conducted in non-pandemic periods have reported that Brazilian dental students have sufficient and appropriate knowledge and attitudes to avoid contamination and cross-infection risks in clinical practice, especially in aspects related to the use of personal protective equipment (PPE), performance of the disinfection process, and the use of surface barriers. ^{Reference Pimentel, Batista Filho, Santos and Rosa32–Reference Arantes, de Andrade Hage, do Nascimento and Pontes35} However, some previously published protective measures are not effective in preventing the transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). ^{Reference Silveira, Fernandez and Tillmann15}

Faced with the global context of public health emergency, new guidelines have been established to prevent the spread of SARS-CoV-2 and any other pathogens in a clinical setting. ^{25–Reference Thomé, Bernardes, Guandalini and Guimarães29} In addition to increased personal protection with PPE use, changes in primary patient screening, care delivery, and dental clinic infrastructure were also included in the new care protocols. ^{Reference Silveira, Fernandez and Tillmann15} Recently, a web-based study conducted during the pandemic found that Brazilian dental students were familiar with some preoperative preventive measures. However, specific measures to prevent or decrease aerosol generation have been less recognized as a measure to prevent the spread of SARS-CoV-2. ^{Reference Aragão, Gomes, Pinho Maia Paixão-de-Melo and Corona18}

Other studies also evaluated the knowledge of biosafety aspects in the pandemic of COVID-19 among dental students in Asian/Middle Eastern (Iran ^{Reference Esmaeelinejad, Mirmohammadkhani and Naghipour36} and Turkey ^{Reference Ataş and Talo Yildirim37} ) and African (Nigeria ^{Reference Umeizudike, Isiekwe and Fadeju19} ) countries. Although the findings of these studies showed that students have acceptable response rates regarding the correct biosafety measures to prevent transmission of SARS-CoV-2 in a clinical setting, the results reflect the need for the expansion of knowledge related to the disease, ^{Reference Umeizudike, Isiekwe and Fadeju19} and about the extra biosafety measures that should be performed by students in the dental routine. ^{Reference Aragão, Gomes, Pinho Maia Paixão-de-Melo and Corona18,Reference Esmaeelinejad, Mirmohammadkhani and Naghipour36,Reference Ataş and Talo Yildirim37}

Comparisons between the findings of the present study and recent reports are limited by differences in the presentation and selection of biosafety procedures among the studies. ^{Reference Aragão, Gomes, Pinho Maia Paixão-de-Melo and Corona18,Reference Umeizudike, Isiekwe and Fadeju19,Reference Esmaeelinejad, Mirmohammadkhani and Naghipour36,Reference Ataş and Talo Yildirim37} Despite that, similar information may be retrieved from a study with a Turkish sample, ^{Reference Ataş and Talo Yildirim37} as both studies demonstrated that students understand the importance of primary screening to identify potential SARS-CoV-2 patients. Conversely, the present study considered the remote modality as the main learning method, while the Turkish study encompassed this step as part of face-to-face care. ^{Reference Ataş and Talo Yildirim37} Interestingly, this finding contrasts with the fact that most Iranian dental students did not recognize the role of initial screening (face-to-face) in preventing coronavirus transmission at dental departments and clinics. ^{Reference Esmaeelinejad, Mirmohammadkhani and Naghipour36}

Erroneously, Brazilian dental students in our study agreed that clinical sessions for periodontal maintenance and prosthetic adjustments are elective emergency procedures for dental treatment during the pandemic. Emergency treatments involve the presence of intense painful symptoms and require immediate intervention for pain relief, as in cases of traumatic dental injury, pericoronitis, abscess, or localized bacterial infection. ²⁵ Thus, as recognized by Turkish students, patients with clinical pictures that stimulate the presence of intense pain are eligible for dental treatment in the pandemic, ^{Reference Ataş and Talo Yildirim37} which differ from the elective treatment listed in the questionnaire of the present study.

Because of their ability to reduce the number of microorganisms in the oral cavity, ^{Reference Marui, Souto and Rovai38} antiseptics have been used as a standard measure before dental treatment, especially in the pre-operative stage. ^{Reference Dominiak, Shuleva, Silvestros and Alcoforado39} When used in adequate concentrations and time, different solutions, such as Povidone-Iodine (PVP-I), Hydrogen Peroxide (H₂O₂), and Cetylpyridinium Chloride (CPC) are also capable of reducing the viral load of certain strains, such as the human coronavirus. ^{Reference Vergara-Buenaventura and Castro-Ruiz40} In this study, less than a third of the sample recognized mouth rinsing with PVP-I (0.02%, 0.04%, 0.05%—9mL; 30 seconds) as a pre-procedure measure in the pandemic. Nevertheless, a low frequency of perception about the need for mouthwash was also seen in previous studies conducted with Brazilian and Iranian students in the pandemic. ^{Reference Aragão, Gomes, Pinho Maia Paixão-de-Melo and Corona18,Reference Esmaeelinejad, Mirmohammadkhani and Naghipour36} This finding reinforces the need for wide dissemination about the importance of mouth rinsing and the use of appropriate pharmacological substances among dental students. ^{Reference Vergara-Buenaventura and Castro-Ruiz40} Evidence shows that the use of commercial mouthwashes with H₂O₂, CPC and PVP-I can be useful as a pre-procedure conduct, ^{Reference Seneviratne, Balan and Ko41} influencing in the reduction of cross-contamination in clinical practice. ^{Reference Vergara-Buenaventura and Castro-Ruiz40,Reference Langa, Muniz and Costa42}

Contaminated aerosols and droplets can be produced from saliva and blood during different dental procedures, from drying the dental element for anamnesis, during intraoral X-rays, even in more complex procedures, such as the removal of decayed dental enamel using a high-speed handpiece and air syringe, and in the ultrasonic irrigation of the root canal. ^{Reference Yang, Chaghtai and Melendez43,Reference Azim, Shabbir and Khurshid44} Effective measures to prevent or minimize the production of COVID-19 contaminated droplets or aerosols in the dental office are well documented in the literature. ^{25,28,Reference Thomé, Bernardes, Guandalini and Guimarães29} Among these, the 4-hand technique, for example, is considered beneficial for infection control. In addition, the use of manual instruments (where applicable), rubber dams, and high-powered salivary suckers can significantly reduce the production and dissemination of airborne particles in clinical practice. ^{25,Reference Yang, Chaghtai and Melendez43} It is important to highlight that taking radiographs with intraoral techniques may stimulate microbial expulsion in aerosols ^{Reference Vandenberghe, Jacobs and Bosmans45} and, therefore, extraoral techniques, such as dental panoramic radiographs (DPR), and cone beam computed tomography (CBCT), may be suitable alternatives to be used in the outbreak of COVID-19. ^{Reference Meng, Hua and Bian8,Reference Thomé, Bernardes, Guandalini and Guimarães29}

Our findings showed that the assistance of another operator in infection control during dental procedures (4-hand technique) in the pandemic was not a conduct recognized by a representative portion of dental students. In addition, more than one third of the participants were not aware of the need to use manual instruments, protective rubber barriers, and powerful sucker during these procedures, which is in accordance with previous national ^{Reference Aragão, Gomes, Pinho Maia Paixão-de-Melo and Corona18} and international ^{Reference Esmaeelinejad, Mirmohammadkhani and Naghipour36} findings, which identified a low adherence of these accessories as a strategy to prevent the dissemination of COVID-19 by dental students in procedures that generate aerosol. Still, it is noteworthy that almost half of the students in this study disagree on the use of extraoral techniques to replace intraoral modalities during the pandemic, which could avoid the dissemination of contaminated droplets. It is essential to consider that, although DPR may replace intraoral radiographs in specific diagnoses during these difficult times, CBCT is associated with higher radiation doses and cost, and its use as an alternative to intraoral technique should be employed with extreme caution. ^{Reference Dave, Coulthard and Patel46}

The need to wear a PPE set during dental care, such as gloves, disposable cap, surgical mask overlapped by masks N95/PFF2 or equivalent, face shield, and capote or apron with long sleeves and waterproof, was reported by most students in this study. This finding corroborates pre-pandemic records that demonstrate a satisfactory rate of PPE use among Brazilian dental students, ^{Reference Zocratto, Silveira, Arantes and Borges47,Reference Abreu, Lopes-Terra and Braz48} and matches the global perspective of previous reports with similar samples that also showed satisfactory levels of perception about the use of different PPE in clinical dental practice during the pandemic. ^{Reference Aragão, Gomes, Pinho Maia Paixão-de-Melo and Corona18,Reference Esmaeelinejad, Mirmohammadkhani and Naghipour36}

The readjustment of the infrastructure of university clinics, especially regarding the spacing and isolation of dental units and the control of air circulation, is one of the great challenges of dental schools during the pandemic. ^{Reference Machado, Bonan, Perez and Martelli6,Reference dos Santos Fernandez, da Silva, dos Santos Viana and da Cunha Oliveira7,Reference Vieira, Pedrotti Moreira and Mondin31} In Brazil, most universities have dental care units distributed in the open-plan clinics format (ie, multiple chairs in 1 clinical area with only modest dividing walls that do not reach the ceiling). ^{Reference Machado, Bonan, Perez and Martelli6,Reference dos Santos Fernandez, da Silva, dos Santos Viana and da Cunha Oliveira7} In these environments, there is a higher risk of cross-infection, due to the dissemination of pathogens through the concentration of aerosols from the various dental procedures performed simultaneously, as well as due to the high turnover of students, employees, and patients in these facilities. ^{Reference Meng, Hua and Bian8,Reference Peng, Xu and Li9,Reference Holliday, Allison and Currie49}

Current protocols reinforce that the old community clinic model should ideally be replaced by individualized care boxes. ^{Reference Meng, Hua and Bian8,Reference Costa, Branco and Vieira30} If this is not possible, the collective care spaces should be reorganized with adequate distancing and use of mechanical barriers between dental chairs, as well as equipment to perform air filtration and flow. ^{Reference Costa, Branco and Vieira30} In the present study, most students recognized the need to adapt the infrastructure of university clinics to the new biosafety reality of the post-pandemic period.

Associated Factors Related to Knowledge in Biosafety Measures in Clinical Setting

Several studies have explored the influence of gender differences on the academic performance of dental students. ^{Reference Stewart, Bates, Smith and Young50,Reference Silva51} Currently, there is a trend toward the feminization of dentistry ^{Reference Kfouri, Moysés and Gabardo52} that may be accompanied by the better performance of women in academic assessments, ^{Reference Silva51} which is related to traditional notions (in the context of culture and biopolitics) of a natural feminine inclination to care and be sociable with other people. ^{Reference Silva51,Reference Kfouri, Moyses and Moyses53} This knowledge may explain why female dental students had a significantly higher mean score of knowledge about biosafety measures than male students in the present study. In the pre-pandemic period, better practices of infection control and academic performance among female dental students have been demonstrated. ^{Reference Silva51}

Students enrolled in the final stages (fourth and fifth years) of the dental degree course had higher average knowledge about biosafety measures in the present study. This finding may be related to the fact that these students have a greater load of theoretical knowledge and clinical experience than those in the initial stages. ^{Reference Stewart, Bates, Smith and Young50,Reference Silva51} Moreover, this difference may be related to the students’ increased expectation to return to clinical practice and a deeper concern to finish their reports and qualifying exams, reflecting their need of learning more about COVID-19 and biosafety measures. ^{Reference Umeizudike, Isiekwe and Fadeju19,Reference Loch, Kuan and Elsalem54}

In the present study, dental students who received instruction on aerosol control measures during their course prior to the pandemic onset, as well as those who participated in theoretical-practical refresher training on biosafety guides during the COVID-19 pandemic, had higher mean knowledge scores than those who had not received such guidance. This finding was not unexpected, as greater access to adequate biosafety information directly justifies this relationship. In any case, it is interesting to note that a representative portion of students did not receive guidance on aerosols, and more than two thirds of the participants were not trained on biosafety measures in the pandemic.

In this context, the analysis of this panorama reflects the need for Brazilian dental schools to use available resources to train their students on the biosafety protocols in force, ensuring safe academic return. ^{Reference Aragão, Gomes, Pinho Maia Paixão-de-Melo and Corona18} Although, at this time, the extensive practical training of students is limited by the pandemic containment measures, it is feasible to use virtual learning environments for the dissemination of reliable guidelines that can decrease or stop the cross-transmission of diseases in the clinical practice. Indeed, the use of the e-learning modality proved to be a successful adjunct and impacted the environment in which dental students learn, promoting a more efficient productive routine with higher levels of engagement during the COVID-19 pandemic. ^{Reference Hattar, AlHadidi and Sawair55}

Strengths and Limitations of the Study

The adoption of an innovative method of online data collection and dissemination through social media, which is an especially useful research tool and a promising method in times of social isolation, is one of the main strengths of this study and deserves to be highlighted. ^{Reference Moraes, Correa and Daneris23} Furthermore, up to date, this is the first Brazilian study that provides evidence on the knowledge of dental students about the current biosafety measures that should be adopted in clinical practice during the pandemic of COVID-19. Considering the important contribution that Brazil offers to dental research and education, our findings are essential to support teaching activities aimed at training students to return to clinical practice, especially by directing educators and managers on which student groups should intervene.

The results of this study should be interpreted with caution, considering some limitations. The first involves the cross-sectional design of the study, as this does not allow cause-effect relationships to be established. Second, the regional differences in the distribution of students showed that most of the sample were not from the region of the country where the largest number of dentistry courses are located (Southeast). Finally, the use of a non-validated research instrument can be listed as a limitation of this study, although it is able to provide important knowledge about the population at this time of pandemic crisis. However, the questionnaire was previously tested by a group of dental students to increase its applicability. Moreover, all associations between the variables of the present study are considered valid and robust.