key: cord-0911354-hyj7g87f
authors: Madathil, Sreenath; Siqueira, Walter L.; Marin, Lina M.; Sanaulla, Farisa Banu; Faraj, Nancy; Quiñonez, Carlos R.; McNally, Mary; Glogauer, Michael; Allison, Paul
title: The incidence of COVID-19 among dentists practicing in the community in Canada: A prospective cohort study over a six-month period
date: 2021-10-25
journal: J Am Dent Assoc
DOI: 10.1016/j.adaj.2021.10.006
sha: b99a42c62b66c9f25e09d25c8a925586330947c8
doc_id: 911354
cord_uid: hyj7g87f

Background Dental care settings potentially carry a high risk of cross-infection between dentists and patients and among dental staff due to close contact and use of aerosol-generating procedures. This study aimed to estimate COVID-19 incidence rates among Canadian dentists over a six-month period. Methods We conducted a prospective cohort study of 644 licensed dentists across Canada, from 29th July 2020 to 12th February 2021. An online questionnaire, adopted from WHO Unity Study protocols for assessment of COVID-19 risk among healthcare workers was used to collect self-reported SARS-CoV-2 infection, every four weeks. Bayesian Poisson model was used to estimate the incidence rate and corresponding 95% credible intervals (CI). Results The median age of participants was 47 years, with the majority being female (56.4%) and general practitioners (90.8%). The median follow-up time was 188 days. Six participants reported COVID-19 infection during the study period, giving an incidence rate of 5.10 per 100,000 person-days (95% CI = 1.86 – 9.91 per 100,000 person-days). The incidence proportion was estimated to be 1084 per 100,000 dentists (95% CI = 438 to 2011 per 100,000), while it was 1864 per 100,000 persons (95% CI = 1859 to 1868 per 100,000 persons) in the Canadian population during the same period. Conclusion The low infection rate observed among Canadian dentists over the period July 2020 to February 2021 is reassuring to the dental and general community.

Evidence shows an increased incidence of COVID-19 among health care providers (HCPs) compared to population rates 1-4 . A systematic review of COVID-19 infection rates and deaths among HCPs globally, using data collected until 8 th May 2020, reported 3.9% of cases and 0.5% of COVID-19-related deaths globally were among HCPs 2 . An investigation of a cohort of HCPs in New York City demonstrated a seroprevalence of SARS-CoV-2 antibodies of 13.7% 3 . Using data available up to 23 rd July 2020, the Canadian Institute of Health Information (CIHI) reported that 19 .4% of cases in Canada up to that point were among HCPs 1 , although cases varied significantly across provinces, from 5.4% in Saskatchewan to 24.1% in Quebec 1 . Dentists, a high-risk group of HCPs, are not included, or at least not identified as a group, in these studies. The available data concerning COVID-19 infections in dentists and dental professionals come studies from the USA 5, 6 , UK 7 , and France 8 and a retrospective case series report of 31 infected oral HCPs from China 9 . The US study reported a prevalence of 0.9% for confirmed or probable cases of COVID-19 among 2,195 dentists who responded to the survey sent to 5,479 dentists across all states in June 2020 5 . The six-month cumulative prevalence from this study remains low at 2.6% 6 . The French study covered an earlier period (April 2020) and reported a higher prevalence of 1.9% among dentists and 0.8% among dental hygienists 8 . The study from the UK, on the other hand, reported 16.3% seroprevalence in May 2020 among dental care professionals which included dentists and other support staff 7 . These reports highlight the geographical heterogeneity in the disease burden and the need to estimate the same among Canadian dentists.

Dental care settings potentially carry a high risk of cross-infection between dentists and patients and among dental staff due to their close contact and aerosol-generating procedures (AGP) [10] [11] [12] . Common instruments used for dental care (e.g., high-speed handpiece) can splash patient saliva or blood directly onto dental staff and patients and aerosolize these fluids, potentially suspending them in the air for several hours [10] [11] [12] [13] . Consequentially, in mid-March 2020, as the COVID-19 pandemic emerged in Canada, dental regulatory authorities (DRAs) across Canada obliged dentists to close their offices to routine care and provide emergency care only 14-16 . In early May 2020, the Saskatchewan and Manitoba provincial governments permitted dentists to open their offices for routine dental care following guidelines issued by the relevant DRAs 17, 18 . This was quickly followed by the other Canadian provinces and territories. Since this reopening, there have not been any jurisdictional shutdowns of dental care in Canada. Early on in the re-opening phase in spring 2020, DRAs published detailed infection control and prevention (IPC) protocols for providing dental care and these varied across provinces. However, the level of evidence supporting the use of particular personal protective equipment (PPE) or the use or not for AGPs and the risk of contamination with SARS-CoV-2 and contracting COVID-19 remains very poor 19 . In this context, in July 2020, we initiated a study whose aim was to document the incidence of COVID-19 in community-based dentists in Canada over a 12-month period. Here, we report findings after six months.

We used data from an ongoing, prospective cohort study of Canadian dentists. Eligibility criteria included (i) being licensed to practice general or specialty dentistry in Canada during the study period; (ii) being SARS-CoV-2 negative at recruitment; and (iii) no history of COVID-19. Potential participants identified through rosters of nine provincial dental licensing bodies or dental associations (NL, NS, PE, QC, ON, MB, SK, AB and BC) were invited to participate through their emailing lists. Regular reminder emails were sent until we reached the required sample size. The study was approved by the ethics review board of the leading institutions.

The sample size for the cohort study was calculated based on estimates of infection rates in May 2020 in Canada. We calculated a sample size of 380 participants, to be followed-up for 1 year, to estimate an incidence proportion of 1% with a margin of error of 1%. Of which, at least 200 participants were required in a sub-cohort to estimate an incidence proportion of 0.5% for nonsymptomatic COVID-19 with a margin of error of 0.9%. [20] [21] [22] 

Invitations to participate were sent to dentists registered across nine participating dental licensing bodies or associations in late July 2020. Out of 702 participants who consented to participate in the study, 651 completed the baseline survey. Excluding participants who stopped working before November 2019 (n=2) and prevalent COVID-19 cases, 644 participants were invited to the longitudinal phase. We randomly invited 226 participants from this group to provide saliva samples every four weeks to test for asymptomatic cases of infection. Of these, two participants were later excluded due to logistical challenges in shipping samples from their location, resulting in a final sample size of 224 for the sub-cohort.

After providing informed consent, participants completed an online baseline survey. Three domains of information were collected at this stage: i) demographics and comorbidities; ii) details of dental care provided to patients in the previous two weeks (e.g., number of AGPs performed, N95 use, ventilation in clinics) (Clinical activity form); and iii) symptoms and infection status (e.g., Fever≥38 o C, respiratory and other symptoms related to COVID-19, whether the participant has tested positive for SARS-CoV-2, date and type of test) (Outcome form). Questionnaires were adapted from WHO Unity Study protocols for assessment of COVID-19 risk among health care workers 23 and were available in both official languages. SAR-CoV-2 negative participants at baseline were invited for the longitudinal phase of the study and to provide their contact information (e.g., telephone, email, postal address). Every four weeks post-baseline, participants completed an online questionnaire through the 'LimeSurvey' platform 24 . These follow-up questionnaires included the Clinical activity and Outcome forms. In addition to questionnaire data, the participants included in the sub-cohort self-collected saliva samples every four weeks post-baseline (saliva sample collection described below) and mailed them to the relevant laboratory for analyses.

The end of participant follow-up was defined as the earliest event among the following: i) selfreported diagnosis of COVID19; ii) detection of SARS-CoV-2 RNA in saliva; iii) death; iv) leave of absence from practice (retirement, parental leave > 3 months); or v) administrative end for interim analysis (12 th February 2021).

Saliva samples were self-collected using a saliva collection kit (Super•SAL™ oral fluid collection system, Oasis Diagnostics® Corporation, USA) containing RNA stabilizer (RNAlater, SIGMA) and proteinase inhibitors following the instructions for saliva collection prepared by our research team. The Super•SAL™ oral fluid collection system is a swab device designed for saliva collection that allows the collection of protein, DNA and RNA from human and microorganism sources. A total of 1.5 mL of saliva were collected at each follow-up.

Immediately after collection, saliva samples were shipped to the Salivary Proteomics Research Laboratory (SPRL), College of Dentistry, University of Saskatchewan. At the SPRL, samples were centrifuged at 14,000×g for 30 min at 4 ºC to separate pellets containing microorganism, host cells and other debris, from saliva supernatant containing the host and viral proteins/peptides 25 . Saliva supernatant was concentrated to half its volume using a centrifugal concentrator. Then, total RNA was extracted from 220 µL of saliva supernatant using QIAmp Viral RNA Mini Kit (Qiagen) according to the manufacturer's instructions. Extracted RNA was used for the qualitative detection of SARS-CoV-2 specific RNA in saliva samples with the RealStar® SARS-CoV-2 RT-PCR Kit 1.0 (Altona Diagnostics GmbH) real-time RT-PCR (rRT-PCR) technology using a CFX96™ Real-Time PCR Detection System (Bio-Rad). Thus, our primary method for determining COVID-19 cases using saliva samples was rRT-PCR, considered the gold-standard method for the detection of SARS-CoV-2 RNA in different biofluids 26 .

Longitudinal patterns of in-person dental care provided by participants and types of personal protective equipment used were summarized using descriptive statistics. We used a Bayesian Poisson model to estimate the incidence rate. Analyses were conducted using data collected during the period 29 th July 2020 to 12 th Feb 2021. To account for the uncertainty in the date of infection due to time lapse between infection and test dates, we implemented the recently proposed single random point imputation technique shown to be superior to other standard techniques [27] [28] [29] . The technique imputes a value for the follow-up duration from the interval between the date of the last reported negative result and the date of the sample, which led to a positive result. This approach is based on the assumption that the infection could have happened at any point between these two visits. A non-informative prior [Gamma (0.0001, 0.0001)] was used for the rate parameter. The model was fit in JAGS 30 using four parallel MCMC chains with 25,000 burn-in and 25,000 samples each (see supplementary materials for details of the model). The convergence of MCMC chains was assessed using trace plots and Gelman and Rubins Rhat value 31, 32 . Incidence rates and corresponding 95% credible intervals (95%CI) are reported.

COVID-19 prevalence at baseline and incidence proportion were estimated using a Bayesian binomial model with non-informative Beta(1,1) prior distribution. We also compared the incidence proportion estimate to the national estimate during the study period as obtained from J o u r n a l P r e -p r o o f the Government of Canada Coronavirus disease (COVID-19): Outbreak update (https://www.canada.ca/en/public-health/services/diseases/2019-novel-coronavirusinfection.html).

The average age of participants was 47.3 years with a range of 24 to 79 years; the majority was female (56.4%) and general practitioners (90.8%). As expected given the general population distribution in Canada, the majority of our sample had their primary practice in the provinces of Quebec or Ontario (62.9%), serving a metropolitan or urban community (57%) and practiced only in one office per week (83.4%) ( Table 1 ). The data collection period was 29 th July 2020 to 12 th Feb 2021. The median follow-up was 188 days with an IQR of 183 to 191 days. Eighteen participants (2.7%) were lost-to-follow-up during the study period.

The majority of participants (>80%) continued to provide in-person dental care across the baseline and follow-up visits. Among this subgroup of participants, most performed AGPs for at least one patient across the study period. However, a very low proportion of participants provided care for patients who were known to be COVID-19 positive or suspected of having COVID-19 (Table 2) .

During the follow-up period, the usage of N95 or higher specification masks increased from approximately 40% to 60% (Table 3 & Figure 1 ). Further, the proportion of participants using both N95 or higher specification masks and visors for all in-person dental care procedures doubled during the follow-up period (9.3% to 19.6%). The majority of participants (>90%) used goggles or eyeglasses during all types of dental procedures throughout the follow-up period.

During the follow-up period, six participants reported COVID-19 resulting in an incidence rate of 5.10 per 100,000 person-days (95% CI = 1.86 -9.91 per 100,000 person-days). The cumulative incidence curve is presented in Figure 2 . The incidence proportion was estimated to be 1084 per 100,000 dentists (95% CI = 438 to 2011 per 100,000). In other words, we estimate that 1.08% (95% CI = 0.44 % to 2.01%) of Canadian dentists were COVID-19 positive during the study period from July 2020 to Feb 2021. The incidence proportion among the general population during the same period was 1864 per 100,000 persons (95% CI = 1859 -1868 per 100,000 persons).

None of the participants who were in the sub-cohort who provided saliva reported to have ever tested positive of COVID-19 during the period of this study. As expected, no SARS-CoV-2 were detected in any of the saliva samples from 224 participants over the study period.

Several publications have highlighted oral health care professionals as a high-risk group for SARS-CoV-2 infections [33] [34] [35] [36] . Previous reports on COVID-19 risk among health care professionals in general also pointed towards this direction [37] [38] [39] . Studies from the U.S. and France conducted during the early phase of the pandemic showed low prevalence compared to the general population. However, no studies have reported the incidence rates of SARS-CoV-2 infections among Canadian dentists. We present the results from an ongoing, prospective cohort study of COVID-19 incidence rates in Canadian dentists working in the community.

After the initial phase of the pandemic, and the re-opening of dental offices to routine dental care across the country in the spring of 2020, the majority of participating dentists provided some form of in-person dental care for patients during the study period. Interestingly, we found the infection rates in our study were lower than those documented for the general population using provincial and federal surveillance data during the study period (29th July 2020 to 12th Feb 2021). However, due to the relatively short follow-up period, dynamic nature of the infection rates among the general population and the fact that dentists are included in the data available from the public domain, this comparison must be interpreted with caution.

Notwithstanding the need to be cautious in interpreting the apparently lower infection rates in our sample compared to the general population, a lower rate may have been a reflection of an array of interacting factors including but not limited to: i) pre-procedure screening of patients, ii) adherence to rigorous infection prevention and control (IPC) protocols used during these procedures, iii) public health measures (e.g., physical distancing, masking), iv) increased awareness and precautionary behavior of dentists in general, outside their work place. For example, the follow-up period of the study primarily spanned the second wave of COVID-19 in Canada, where although more cases were reported compared to the first wave, more stringent social distancing measures were also imposed (e.g., curfews and restriction on inter-regional travel). Also, only a minority of participants provided dental care for patients who were confirmed cases or suspicious of having COVID-19, so this may be an initial signal that the event rates are mainly driven by community contacts rather than any in-clinic transmission. In addition, most participants in the study used multiple face-coverings during most procedures. Although the use of N95 or higher specification respirators was low during the initial follow-ups, it has increased over time, which may reflect increase in the availability of this PPE.

Uptake of vaccination could be a possible explanation for low infection rates. However, our study accumulated more than four months of follow-up by the time the COVID-19 vaccination campaign began in Canada. At the time of this interim analysis (12 th of Feb 2021), the proportion of participants who received at least one dose of the COVID-19 vaccine was low (~5%) and thus cannot explain the low infection rates.

The cumulative incidence curve (Figure 2) indicates the speed at which infections are reported in the study population. A rapid increase of slope of this curve during study period may reflect a cluster of infections and possibly due to an outbreak. Figure 2 illustrates that the infection rate is fairly stable, although with wide confidence intervals.

Saliva samples were analyzed using RT-PCR with the aim of detecting asymptomatic COVID-19 cases among the participants. Herein, we did not detect any SARS-CoV-2 RNA in any of the monthly samples analyzed from the 224 participants who provided saliva samples over the study period. So, we cautiously conclude that there were no symptom-free cases of COVID-19 infection in our sample during the study period. However, we acknowledge the limitations of our technique. Nasopharyngeal swabs are standard for population-wide screening for SARS-CoV-2, however, saliva samples are logistically more feasible and have been reported to have similar sensitivity to the former 40 . The time gap between consecutive saliva samples may have played a role in null detection. For example, if a participant was infected immediately after providing a saliva sample and never develops any symptoms, the viral RNA may reduce to a non-detectable level at the time of the next saliva sample one month later. More frequent sample collection schedules might have caught such infections, but they would have been logistically challenging and may have overburdened participants.

Accuracy of RT-PCR based detection of SARS-CoV-2 RNA in saliva sample may have also played role in our results. However, several systematic reviews have shown that saliva sample based tests have comparable sensitivity and specificity as the nasopharyngeal swab (NPS) samples tests, and offer a cost-effective alternative for screening. [40] [41] [42] Furthermore, a recent study comparing NPS and saliva samples among asymptomatic individuals showed >99% specificity for saliva samples and high concordance with results from NPS samples. 43 Saliva samples were only collected from a sub-cohort of the participants who consented to provide samples every month. This sub-sampling may have resulted in a selection bias if the participants who consented to provide saliva systematically have lower risk than the rest of the study population. However, given that majority (>80%) of participants at baseline consented to provide saliva and we randomly selected participants from this consenting group, the possibility of selection bias in our results is reduced.

Due to low event rates, to date, we were not able to investigate factors such as demographics and PPE use that could be associated with COVID-19 infections in the analyses reported in this paper. Future follow-up data and further analysis from the project will explore these factors. Furthermore, comparing infection rates among different oral health care professionals (dental hygienists, dental assistants) and with other HCPs is also warranted.

Finally, it is important to recognize the nature of the sample which, while including participants from multiple provinces, is a convenience sample of dentists who voluntarily responded to the invitation to participate. Invitations were sent to the large majority of dentists in the country but only a small proportion responded. However, the distribution of demographic characteristics among study population was comparable to national data on Canadian dentists obtained from Canadian Dental Association as of July 2020 (Please see supplementary materials Table S1 ).

This is the first report of COVID-19 risk among Canadian dentists. The low infection rate observed during the six-month follow-up period is reassuring to the dental and general community. By providing the disease surveillance data, the results of this study may help decision-makers adapt and optimize clinical guidelines for infection prevention and control during this pandemic and potentially future waves. tabulated in table 1  Table 2 . Details of dental-care provided by participants with at least one in-person care provision in past 2-weeks* Description: Average number of in-patient cares provided and the type of patients according to COVID-19 status is tabulated in table 2. The data in the table is limited to those participants who had at least one in-person care provision during 2 weeks prior to the follow-up visit. Table 3 . Pattern of use of facial coverings during in-person dental care provision over past 2 weeks* Description: Details of type of facial covering used during in-person care including the type of cares are tabulate in table 3. The data in the table is limited to those participants who had at least one in-person care provision during 2 weeks prior to the follow-up visit. 

CIHI COVID-19 cases and deaths among health care workers in Canada | CIHI. Canadian Institute for Health Information 2020

Infection and mortality of healthcare workers worldwide from COVID-19: a systematic review

Prevalence of SARS-CoV-2 Antibodies in Health Care Personnel in the New York City Area

Public Health Agency of Canada 2021

Estimating COVID-19 prevalence and infection control practices among US dentists

COVID-2019 among dentists in the United States: A 6-month longitudinal report of accumulative prevalence and incidence

COVID 19 : Seroprevalence and vaccine responses in UK dental care professionals

Prevalence and risk indicators of first-wave COVID-19 among oral health-care workers: A French epidemiological survey

Epidemiological Investigation of OHCWs with COVID-19

COVID-19 Transmission in Dental Practice: Brief Review of Preventive Measures in Italy

Coronavirus Disease 2019 (COVID-19): Emerging and Future Challenges for Dental and Oral Medicine

Transmission routes of 2019-nCoV and controls in dental practice

Coronavirus COVID-19 impacts to dentistry and potential salivary diagnosis

College of Dental Surgeons of British Columbia 2020

Royal College of Dental Surgeons of Ontario 2020

Ordre des dentistes du Québec 2020

Manitoba Dental Association 2020

College of Dental Surgeons of Saskatchewan 2020

Canadian Agency for Drugs and Technologies in Health 2020

Sample size determination in health studies: a practical manual: World Health Organization

Methods in observational epidemiology: Monographs in Epidemiology and Biostatistics

WHO Unity Studies: Early Investigation Protocols. World Health Organization 2020

LimeSurvey: An Open Source survey tool

Kinetics of histatin proteolysis in whole saliva and the effect on bioactive domains with metal-binding, antifungal, and wound-healing properties

Detection of 2019 novel coronavirus (2019-nCoV) by realtime RT-PCR

Censoring issues in survival analysis

Incidence rate estimation, periodic testing and the limitations of the mid-point imputation approach

Estimating trends in the incidence rate with interval censored data and time-dependent covariates

JAGS: A program for analysis of Bayesian graphical models using Gibbs sampling. Paper presented at: International Workshop on Distributed Statistical Computing

Inference from Iterative Simulation Using Multiple Sequences

General Methods for Monitoring Convergence of Iterative Simulations

COVID-19 transmission risk and protective protocols in dentistry: a systematic review

COVID-19 Outbreak: An Overview on Dentistry

Rational perspectives on risk and certainty for dentistry during the COVID-19 pandemic

COVID-19 Dentistry-Related Aspects: A Literature Overview

COVID-19-Associated Hospitalizations Among Health Care Personnel -COVID-NET, 13 States

COVID-19 and the Risk to Health Care Workers: A Case Report

Risk of COVID-19 among front-line health-care workers and the general community: a prospective cohort study

The Sensitivity and Costs of Testing for SARS-CoV-2 Infection With Saliva Versus Nasopharyngeal Swabs : A Systematic Review and Meta-analysis

Comparison of Saliva and Nasopharyngeal Swab Nucleic Acid Amplification Testing for Detection of SARS-CoV-2: A Systematic Review and Metaanalysis

Comparing saliva and nasopharyngeal swab specimens in the detection of COVID-19: A systematic review and meta-analysis

Mass Screening of Asymptomatic Persons for Severe Acute Respiratory Syndrome Coronavirus 2 Using Saliva