COVID-19 challenges to dentistry in the new pandemic epicenter: Brazil.

A nationwide survey of dentists was carried out in Brazil, a new pandemic epicenter, to analyze how dental care coverage has been affected in public versus private networks, changes in routine and burdens, and how local prevalence of COVID-19 affects dental professionals. Dentists were recruited via email and Instagram®. Responses to a pre-tested questionnaire were collected May 15-24, 2020. COVID-19 case/death counts in the state where respondents work was used to test associations between contextual status and decreases in weekly appointments, fear of contracting COVID-19 at work, and current work status (α = 0.05). Over 10 days, 3,122 responses were received (response rate ~2.1%) from all Brazilian states. Work status was affected for 94%, with less developed regions being more impacted. The pandemic impact on clinical routine was high/very high for 84%, leading to varied changes to clinic infrastructure, personal protective equipment use, and patient screening, as well as increased costs. COVID-19 patients had been seen by 5.3% of respondents; 90% reported fearing contracting COVID-19 at work. Multilevel models showed that greater case and death rates (counted as 1000 cases and 100 deaths per million inhabitants) in one's state increased the odds of being fearful of contracting the disease (18% and 25%). For each additional 1000 cases/100 deaths, the odds of currently not working or treating only emergencies increased by 36% and 58%. The reduction in patients seen weekly was significantly greater in public (38.7±18.6) than in private clinics (22.5±17.8). This study provides early evidence of three major impacts of the pandemic on dentistry: increasing inequalities due to coverage differences between public and private networks; the adoption of new clinical routines, which are associated with an economic burden for dentists; and associations of regional COVID-19 incidence/mortality with fear of contracting the disease at work.

Introduction

Brazil has emerged as a new COVID-19 pandemic epicenter with steadily growing caseloads. By July of 2020, Brazil was the country with the second-most cases and deaths [1]. With dentistry being a context of high contraction risk and the international supply of personal protective equipment (PPE) compromised, the pandemic has brought major challenges to the dental sector, including maintaining universal dental care coverage for 211 million people dispersed across an 8.5-million-km2 area. Brazil, which has more than half a million dental professionals, including 348,000+ dentists [2], and accounts for an approximately 2.5% share of the 29+ billion USD global market [3], has the most important dental industry in Latin America.

Studies on pandemic effects to dentistry have been carried out in other countries. A survey with 440 dentists in Italy [4] reported that 68% were afraid of being infected during dental procedures during a lockdown period. A survey with 669 dental practitioners from 30 countries [5] showed that 87% were afraid of getting infected with COVID-19 from patients or co-workers, and 90% felt anxious while treating patients who coughed or were suspected of COVID-19 infection. In contrast, a survey with general population in Spain [6] indicated that above 90% of respondents were not afraid of contracting COVID-19 at dental offices, nor would cancel a dental appointment. These differences in behavior could be related to factors including differences in local COVID-19 contraction and death rates, or even how local healthcare systems are managing the pandemic. There is also evidence of changes in clinical routines in dental offices: a survey with 287 dentists in Saudi Arabia [7] showed that 65% of clinics had a workflow for COVID-19 patient screening and new management routines, including body temperature measurements and social distancing in the waiting room. In Italy, telephone triages in dental offices have been reported by 57% of dentists [4], and 80% reported improved training routines on how to wear, remove, and dispose PPE.

While high-quality technological dentistry is available in the private sector in Brazil, low-income citizens depend on a public healthcare system, which showed signs of struggling to cope with the pandemic [8]. Dentistry personnel seem to be facing new routines, more expensive and less comfortable PPE, fewer appointments, and less revenue. These challenges are superimposed upon already existing economic instability in Latin America that has persisted since mid-2014. In this context, dentists may be challenged with fears of contracting COVID-19 while working in a quickly-changing, turbulent situation. Dental teams need to make preventive care efforts to ensure that they do not contribute to worsening the epidemiology of the pandemic. Moreover, the situation could be worsened due to Brazil being in a region of developing countries with entrenched inequalities [9].

Planning medium- and long-term actions to respond to the challenges facing the dental sector related to the COVID-19 pandemic will require establishing a knowledge of baseline parameters, including estimates of key resources, of the sector. In addition, understanding the initial signs of how the pandemic affected the Brazilian dental sector could help other countries in the region to prepare for possible impacts to dentistry. In this study, we conducted a survey with dentists in Brazil, the aims of which were to assess COVID-19 pandemic effects on (i) dental care coverage, (ii) dental office routines and economic burdens, and (iii) the behavior of dentists. The nationwide survey was conducted in May 2020, when the contagion curve was escalating in Brazil.

Methods

Study design

The study protocol was approved by the research ethics board from the Medical School, Federal University of Pelotas, Brazil, in May 8, 2020 (#4.015.536). A questionnaire was developed, pre-tested, and used in a cross-sectional open survey with a large sample of dentists in Brazil. The objective of the survey was to address key questions that could impact the dental sector in Brazil as the country was a new pandemic epicenter. The questions were designed to provide data on possible changes in dental coverage between public and private assistance networks and new dental office routines that could be associated with economic burdens for dentists. In addition, the instrument was designed to assess how dentists were behaving during the pandemic, including their confidence of seeing COVID-19 patients and their fear of contracting the disease at work. The strategy for recruiting participants combined emails sent to dentists and a social media campaign, as further detailed. In order to maximize participation, the questionnaire was designed to be short and having only close-ended questions. In accordance with open science practices, the research protocol, questionnaire in its original language, databank of responses, and other information related to this study are published in an open platform (doi:10.17605/OSF.IO/DNBGS). An English translation of the questionnaire is presented in S1 Table. SURGE guidance [10] and CHERRIES reporting guideline [11] were consulted for this article, which does not cover the full survey content.

Questionnaire development and pre-testing

A self-administered questionnaire was developed through consultation with eight experienced dental researchers in three discrete review rounds. The questionnaire was hosted online in Google Forms (Google; Mountain View, CA, USA). To obtain information about the reliability and validity of the tool and items, we conducted a pre-test in a sample of 22 dentists who were asked to evaluate its clarity, writing style, question sequence, and internal consistency. The population of pre-testers included differences in sex, age, working sector, region of country, experience, and education levels in an endeavor to resemble the population of dentists in Brazil [2, 12]. The pre-testers were asked to respond the questionnaire and record the time to complete; the mean time to complete ± standard deviation (SD) was 7 ± 2 min.

Pre-testers scored the clarity of each question on a scale of 1 (not clear) to 5 (very clear). A text box was available after every question for pre-testers to explain their scores and place comments, critiques, suggestions, and other response options. All items with a score ≤3 (n = 9) were discussed by at least three researchers to obtain a consensus regarding how to improve them based on pre-tester feedback and then edited accordingly. The mean clarity scores ± SD were high in all cases, varying from 4.79 ± 0.10 for the 9 items that needed revision to 4.91 ± 0.11 for all 30 items considered together. The individual mean score of each question was ≥ 4.86 in 25 questions, and between 4.59 and 4.82 in 5 questions (#5, #9, #12, #14, and #23). The pre-test was important to include other response options in questions #5, #9 and #23, which aided in reducing response bias. Different regulatory authorities were aggregated in question #12, and online training was grouped with general instructions in #14. These groupings were important to avoid overlapping between questions that did not collect multiple answers. Since the changes were minor, the decision was that a second pre-test round was not necessary. The questionnaire was reviewed and revised iteratively by the executive group for approval. Pre-testers were precluded from participating in the main study to avoid response bias.

Questionnaire content

The first page of the questionnaire contained the study title and objective, an invitation for only dentists to participate and complete the questionnaire only once. They were noticed that their participation was voluntary and not paid, given potential risk and benefit information, and assured that all responses would be treated confidentially and anonymously. In addition, the respondents were asked not to participate if they were not dentists and not to respond the survey again if they have already done it before, reducing the risk for duplicate answers. Participants were directed to print or save the first page of the questionnaire as a PDF file to retain a copy of the informed consent form. Contact information of the researchers and institution responsible for the survey were provided. The participant had to click ‘Yes’ after the question “Do you agree to participate in the study voluntarily?” to access the questionnaire. The definitive questionnaire contained 30 mandatory close-ended items (three screens), divided into three sections: demographic and professional profile (n = 8); professional practices during the pandemic (n = 11); and structure and routine of the respondent’s main workplace (n = 11). No randomization of items or adaptive questioning were used. The main outcomes were related to the professionals’ behavior regarding their clinical routines. The options ‘I'd rather not say’, ‘I don't know how to answer’, and ‘Does not apply’ were available to avoid response errors (see the S1 Table for details about questionnaire content).

Participant recruitment and survey administration

A source population of 24,126 registered dentists were sent email invitations to participate. The source list was provided in April 2020 by the Brazilian Ministry of Health. The email contained a brief statement that included the study objective, the average response time, notification of the university conducting the study, and a website link to the questionnaire. The initial emails were sent on May 15, 2020; reminder emails were sent 5 days later. Additionally, we created an Instagram social networking campaign targeting dentists in Brazil (Facebook, Menlo Park, CA). To our best knowledge, this is the first study to use Instagram to recruit healthcare professionals. This social network is highly used by dentists in Brazil; as of, July 8, 2020, there were 5.1 million and 6.8 million posts with #dentistry and #odontologia (Portuguese for dentistry). The campaign, which started on May 20, invited dentists to participate in an online survey regarding the impact of the pandemic on their practices. A significant challenge was the fact that Instagram does not allow placing linking in comments or pots. Thus, an Instagram professional account was created (@odcovid) with a website link to the questionnaire in its bio page. Invitations were posted calling for the participation of dentists; they included the same information provided in the email invites and directed the dentists to use the hyperlink available on the @odcovid bio page. We used hashtags related to dentistry and COVID-19 to increase reach to the target population. Participating researchers shared the invitations on their personal Instagram profiles (feed and stories) and asked other dentists to aid in disseminating the campaign. Brazilian dentists with professional Instagram profiles were asked to also share the invitation post. We reached professionals categorized as micro (<10,000 followers) and meso (10,000–1 million) on the followers scale [13]. A second Instagram campaign with similar content but a slightly different visual presentation was created two days later.

Sample selection, sample size estimation, and collection of responses

All dentists practicing in Brazil were eligible. Given a target population of ~348,000 professionals, we estimated that 2,385 responses would be necessary to ensure a 95% confidence interval and 2% margin of error. Responses were collected between May 15 and May 24, 2020.

Data analysis

Partial questionnaire completion was not possible. In some cases, responses were restricted to a specific population. The response options ‘I'd rather not say’, ‘I don't know how to answer’, and ‘Does not apply’ were treated as missing data. Descriptive statistics were used to identify frequencies and distributions of variables. Responses to questions on numbers of patients assisted weekly, before and after the pandemic, were subjected to t-test. Proportions were compared using chi-square tests. COVID-19 case and death counts in each Brazilian state were obtained from official Ministry of Health reports [14] on May 20, 2020, the date when the greatest number of survey responses was received. For analysis purposes, data were converted into thousands of cases and hundreds of deaths per one million inhabitants in each state. The units of analysis of both variables were the states. Multilevel mixed effect models were used to test the association between the contextual status of the pandemic in each state and dentistry-related outcomes. Outcomes included decrease in number of patients assisted weekly (numerical), fear of contracting COVID-19 at work (no/a little vs. yes/a lot), and current work status (normal/reduced vs. not working/emergencies only). Linear and logistic models were used for numeric and binary outcomes. The models considered two levels of organization: dentist (level 1) and state (level 2). β-coefficients and Odds Ratios (OR) were reported. Contextual level variance was assessed using intraclass correlation coefficient (ICC) for linear models and Median Odds Ratios (MOR) for logistic models (α = 0.05). All analyses were performed in Stata 14.2 (StataCorp, College Station, TX).

Results

A total of 3,122 valid responses were received over 10 days from all 26 Brazilian states and the federal district. No questionnaires were submitted with an atypical timestamp. Gathering of responses over time is shown in Fig 1A. The first 5 days included only email invitation responses. The response rate in this period was 2.1%, but the numbers of actual rejections/losses cannot be calculated because we cannot estimate how many dentists actually received the questionnaire and decided not to respond, for instance. We received 1,572 responses in the first 24 h after the Instagram campaign started. As shown in Table 1, respondents were most female (75%) and in practice for ≤20 years (74%). Meanwhile, 53% were working mainly in private clinics, whereas 36% were working in the public sector. The mean age ± SD of the respondents was 38 ± 11 years. Table 2 shows a demographic comparison between overall dentists working in Brazil and respondents who participated in the present survey. The distributions of responses by region, sex, and age were similar to the overall distributions of dentists in Brazil, except for a higher response rate from females and from Southern Brazil.

Fig 1

Factors influencing COVID-19 pandemic effects on dental practices.

(A) Over 10 days, 3,122 valid survey responses were received from all regions in Brazil. (B) The work statuses of ‘not working’ or ‘emergency only’ were more frequent in the less developed North and Northeast regions, and also in the Southeast (p<0.001). (C) Work status by sector: 52% of private dentists reported seeing less patients than usual, while most public dentists reported emergency appointments only (p<0.001). (D) Education level influenced how prepared professionals feel to assist COVID-19 patients (p<0.001). (E) Dentists who had confirmed contraction of COVID-19 themselves (6.4%) were more likely (p<0.001) to have assisted patients with COVID-19 (tested positive) than dentists who had not (0.7%). (F) Fear of contracting COVID-19 at work varied across regions, being higher in the North and Northeast regions than in other regions (p<0.001). (G) Fear of contracting COVID-19 at work was influenced by years in practice (p<0.001).

Table 1

Demographic and work practice characteristics of the respondents, Brazil, 2020 (N = 3,122).

Variable/category	n*	%	95% CI
Sex	3,116
Male	790	25.4	23.9; 26.2
Female	2,326	74.7	73.1; 76.2
Years in practice	3,121
≤10	1,496	47.9	46.2; 49.7
11–20	812	26.0	24.5; 27.6
21–30	501	16.1	14.8; 17.4
>30	312	10.0	9.0; 11.1
Postgraduate education (completed)	3,121
None	758	24.3	22.8; 25.8
Residency or advanced special training	1,530	49.0	47.3; 50.8
MSc or PhD	833	26.7	25.2; 28.3
Main work sector	3,051
Public	1,091	35.8	34.1; 37.5
Private	1,601	52.5	50.7; 54.2
Other	359	11.8	10.7; 13.0
Brazilian regional division	3,122
South	1,183	37.8	36.2; 39.6
Southeast	923	29.6	28.0; 31.2
Central-west	221	7.1	6.2; 8.0
Northeast	682	21.9	20.4; 23.3
North	113	3.6	3.0; 4.3
Current work status	3,056
As usual	119	3.9	3.3; 4.6
Lower patient volume	994	32.5	30.9; 34.2
Emergency appointments only	1,325	43.4	41.6; 45.1
Not working due to pandemic	546	17.9	16.5; 19.3
Not working due to other reasons	72	2.4	1.9; 3.0
Volume of weekly patients compared with pre-pandemic period	2,812
Increased or normal	62	2.2	1.7; 2.8
Reduced	2750	97.8	97.2; 98.3
Have you had online patient appointments during the pandemic?	2,832
No but I am willing to do	755	26.7	25.1; 28.3
No and I am not willing to do	1,159	40.9	39.1; 42.7
Yes, the overall experience was positive	726	25.6	24.1; 27.3
Yes, the overall experience was negative	192	6.8	5.9; 7.8
Impact of pandemic in work routine	3,048
No impact	17	0.6	0.3; 0.9
Low	99	3.3	2.7; 3.9
Intermediate	389	12.8	11.6; 14.0
High	926	30.4	28.8; 32.0
Very high	1,617	53.1	51.3; 54.8
Have work routine changes led to increased financial costs?	2,207
No	447	20.3	18.6; 22.0
Yes, but prices were not adjusted	1,432	64.9	62.9; 66.9
Yes, and prices were adjusted for patients	328	14.9	13.4; 16.4
Training for COVID-19 specific preventive measures	3,099
None	559	18.0	16.7; 19.4
Online training or general instructions	2,406	77.6	76.1; 79.1
Practical training	134	4.3	3.7; 5.1
Have you treated patients with a confirmed COVID-19 diagnosis?	2,401
No or do not know	2,275	94.8	93.8; 95.6
Yes	126	5.3	4.4; 6.2
How prepared do you feel to treat patients with COVID-19?	3,040
Not at all prepared	702	23.1	21.6; 24.6
Poorly prepared	670	22.0	20.6; 23.5
Intermediately	948	31.2	29.6; 32.9
Well prepared	547	18.0	16.7; 19.4
Very well prepared	173	5.7	4.9; 6.6
Do you fear to contract COVID-19 at work?	3,024
No	295	9.7	8.7; 10.9
Yes, a little	643	21.3	19.8; 22.8
Yes	781	25.8	24.3; 27.4
Yes, a lot	1,305	43.2	41.4; 44.9
Have you suspected or tested yourself for COVID-19?	3,093
No	2,517	81.4	80.0; 82.7
Suspect without test	314	10.2	9.1; 11.3
Negative test	213	6.7	6.0; 7.8
Inconclusive test	16	0.5	0.3; 0.8
Positive test	33	1.1	0.7; 1.5
Do you agree with current social distancing measures in your city?	3,104
Fully disagree	63	2.0	1.6; 2.6
Partially disagree	330	10.6	9.6; 11.8
Not agree or disagree	38	1.2	0.8; 1.7
Partially agree	1,001	32.3	30.6; 33.9
Fully agree	1,672	53.9	52.1; 55.6

* Varies from total N because of missing data for different questions. CI: confidence interval.

Table 2

Distribution of dentists working in Brazil by sex, age, and region (%) compared with the survey participants, Brazil, 2020 (N = 3,122).

	Dentists working in Brazil*	Survey respondents
Sex
Male	43.9	25.4
Female	56.1	74.7
Age
≤30	25.2	32.7
31–40	32.2	33.4
41–50	23.6	20.4
51–60	14.1	9.9
>60	4.9	3.5
Brazilian region
South	16.1	37.8
Southeast	52.8	29.6
Central-west	8.8	7.1
Northeast	16.6	21.9
North	5.7	3.6

*Data obtained from official reports [2, 12].

Dental care coverage

Current work status was reported to be affected by 94% of the respondents. Only 2% reported normal or increased patient volumes. Not working/emergency only statuses were more common among dentists working in the less developed North and Northeast regions, and also in the Southeast region (Fig 1B). Interestingly, 59% of respondents reported be willing to assist or having already assisted patients online, and 26% regarded such virtual consults as being positive experiences.

The proportion of dentists who reported not seeing patients at all due to the pandemic was similar between public and private networks (Fig 1C). However, whereas only 52% of private dentists reported seeing less patients than usual due to the pandemic, 76% of public clinic dentists reported maintaining only emergency appointments, yielding a significant difference on the effect of the pandemic on the volume of patients treated weekly (Table 3). Before the pandemic, the public network covered more patients per dentist. During the pandemic, reductions in weekly dental care levels were reported to be 23 patients/private dentist and 39 patients/dentist in the public network.

Table 3

Mean numbers of patients treated weekly per dentist by work sector (standard deviation), before and during the pandemic, Brazil, 2020 (n = 2,534 dentists*).

	Public network	Private practice	Total
Before pandemic	47.3 (19.7)	34.2 (20.8)	39.6 (21.3)
During pandemic	8.6 (8.6)	11.7 (13.6)	10.2 (11.8)
Difference**	38.7 (18.6)	22.5 (17.8)	29.2 (19.8)

*Varies from total N because of missing data for different questions.

**t-test (p<0.001).

The effects of COVID-19 confirmed-case and death rates on the numbers of patients assisted (Table 4) showed dentists seeing two fewer patients/week for each 1000 cases per one million inhabitants, and three fewer patients/week for each 100 deaths. This effect was more pronounced in the public network: 2.45 and 3.25 fewer patients were seen each week for every 1000 cases or 100 deaths per one million inhabitants, respectively. In this analysis, the number of patients seen by dentists working in private practice was not significant.

Table 4

Effect of numbers of confirmed COVID-19 cases and deaths* on differences in numbers of patients seen by work sector, Brazil, 2020 (n = 2,534 dentists**).

	Effects on decreases in numbers of patients seen
Overall	β	95% CI	P-value	ICC1	ICC2
1000 cases/million inhabitants	1.96	0.43; 3.49	0.012	0.101	0.086
100 deaths/million inhabitants	2.90	0.80; 5.00	0.007	0.101	0.085
Public network
1000 cases/million inhabitants	2.45	0.55; 4.36	0.012	0.151	0.144
100 deaths/million inhabitants	3.25	0.98; 5.52	0.005	0.151	0.137
Private practice
1000 cases/million inhabitants	1.12	-1.55; 3.78	0.410	0.151	0.144
100 deaths/million inhabitants	2.34	-0.95; 5.62	0.163	0.151	0.137

*Multilevel linear regression model considering all 26 different Brazilian states and the federal district. CI, Confidence Interval; ICC, Intraclass Correlation Coefficient

1Null model

2Adjusted model.

**Varies from total N because of missing data for different questions.

Routine and economic burden for dentists

The impact of the pandemic on clinic routines was considered high or very high by 84% of respondents (0.6% reported no impact). Though 80% of respondents reported increased financial costs, only 15% adjusted prices for patients. The pandemic required infrastructural changes in the work setting for 74% of dentists. Most had new types of PPE available for all clinical appointments, including face shields (84%), N95 masks (71%), and disposable coats (66%). Patient screening became more expensive and time consuming due to antimicrobial mouthwashes (46%), completion of COVID-19 questionnaires (35%), and temperature monitoring (24%) mainly. For 35% of respondents, N95 masks were the predominant mask used (with at least half of patients).

Behavior of dentists during pandemic

As reported in Table 1, more than four out of five dentists reported undergoing at least some training in COVID-19 preventive measures, though fewer than one in twenty participated in practical in-clinic training. While almost a quarter of respondents reported feeling well/very well prepared to treat patients with COVID-19, only 5.3% had done so (Table 1). Perception of preparedness to provide care for COVID-19 patients was influenced by education level (Fig 1D). It was more common for dentists who treated patients with COVID-19 to also have COVID-19 (6.4%), than for those who had not seen COVID-19 patients (0.7%) (Fig 1E). Testing was also more frequent for dentists who had seen COVID-19 patients. Although 90% feared contracting the disease at work, only 8% indicated that they had been tested for COVID-19 (1.1% had a positive test). Fear varied among regions, being particularly elevated in the North and Northeast (Fig 1F), and with years in practice (Fig 1G). Fear of contracting COVID-19 at work related positively to the numbers of cases and deaths reported in the state in which the respondent was working. Each 1000 cases per million inhabitants and each 100 deaths per million inhabitants increased the odds of having fear to contract COVID-19 (Table 5). Likewise, MOR indicated that, compared to dentists in less impacted states, dentists practicing in more highly impacted states had a more than 30% greater likelihood of fearing that they may contract COVID-19 and were more than twice as likely to be offering emergency only appointments or to be closed altogether rather than maintaining a usual or even reduced volume of patients with full-service availability. For each 1000 cases and each 100 deaths per million residents in the state, the likelihood of not working or treating emergencies only, as opposed to working with a reduced or typical patient volume, increased by 36% and 58%.

Table 5

Effect of numbers of confirmed COVID-19 cases and deaths* on fear of contracting COVID-19 at work and current work status, Brazil, 2020 (n = 3,021 dentists**).

Variable	OR	95% CI	P-value	MOR1	MOR2
Fear to contract COVID-19 at work (ref: none/a little)
1000 cases/million inhabitants	1.18	1.01; 1.39	0.039	1.42	1.32
100 deaths/million inhabitants	1.25	1.02; 1.52	0.029	1.42	1.34
Work status (not working/only urgencies vs. normal/reduced frequency)
1000 cases/million inhabitants	1.36	1.00; 1.86	0.050	2.50	2.28
100 deaths/million inhabitants	1.58	1.06; 2.38	0.026	2.50	2.22

*Multilevel logistic regression model considering all 26 different Brazilian states and the federal district. CI, Confidence Interval; OR, Odds Ratio; MOR, Median Odds Ratio

1Null model

2Adjusted model.

**Varies from total N because of missing data for different questions.

Discussion

Here, we report the findings of the first survey, to the best of our knowledge, in which both email and Instagram social networking campaigns were used to reach healthcare professionals. Details on the populations participating in the survey that were recruited by different approaches were addressed in a separate report [15]. Although the use of social media in research has been discussed [16-18], there is scarce information regarding its use to recruit hard-to-reach populations [19-21]. A combined strategy was important to recruit dentists working in both public and private networks, and doing so allowed us gather one of the largest samples to date for a COVID-19 survey in the dental field [4, 5, 7, 22–26]. The pandemic may have facilitated our recruitment owing to people spending more time at home and on social media [27]. Online surveying methods are particularly important during this time when sanitary measures prevent traditional research approaches [15].

This report in concentrated on the early COVID-19 impacts to the dental sector in Brazil. The present results provide early evidence of three major aspects being at stake in dentistry in the new pandemic epicenter. First, differences in care coverage between public and private clinics suggest an intensification of regional and socioeconomic inequalities. Second, although dentists have a similar fear of contracting COVID-19 at work as other healthcare providers, they seem to report feeling less prepared to assist patients [28]. Third, dentists have adopted new routines and incurred increased costs, which eventually will be transferred to patients in the private network, or paid by the government in public clinics. The scenario is aggravated by disjointed responses from the Brazilian government and the associated lack of an effective coordinated national response to the pandemic [29]. The multi-level analysis showed that mounting COVID-19 case and death counts are affecting dentists’ behavior in the new pandemic epicenter. Other studies also have observed that the pandemic is bringing fear to dentists at work. In a survey [5], 85% of respondents reported feeling afraid when heard news about COVID-19 caused deaths. In addition, 92% were afraid of carrying the infection from offices to their families. The aerosolized cloud in dental offices is a constant reminder of danger. Training in preventive measures and the use of up-to-date screening methods may be appropriate first steps for dentists to feel better prepared to attend to COVID-19 patients. Individual cognizance and knowledge of pertinent information are important factors in healthcare workers feeling confidence in dealing with and overcoming the pandemic [28].

Brazilian dental sector stakeholders seem to be paying diligent attention to the ongoing situation. Dental councils and sanitary agencies have already released important guidance documents in the meantime. The vast majority of our study respondents (91%) indicated that they are following official regulatory standards in their new routines, and that they, by and large, have made substantial efforts to cope with the new clinical requirements. In corroboration, studies in other countries [5, 30] addressed that the fear of dentists in getting infected from COVID 19 could be mitigated by dentists and the dental team carefully following recommendations from regulatory authorities. While patient appointment volumes reported in May were significantly below from pre-pandemic levels, our data indicate that Brazilian dentists are open to the incorporation of telehealth programs, which may, despite its associated challenges, be a good strategy for mitigating the impact of the pandemic, while improving preventive actions and reducing unnecessary referrals [31]. A survey in Italy [4] reported that only 37% of dentists considered telehealth as a valid program, and less than 13% reported to have used it before. In contrast, 46% of dental practitioners believed that digital dentistry could be used more often in the post-pandemic period. A recent article [32] recommended the implementation of fully digital approaches during the COVID‐19 pandemic to limit infection risks, whenever possible. Another report suggested that although the pandemic has caused many difficulties for provision of dental care, an opportunity is established for dental educators to modernize their teaching approaches using novel digital and online communication [33].

The low volume of patients reported being seen in the public network in Brazil may reflect a prioritization of PPE supplies for healthcare professionals providing medical treatment to COVID-19 patients as well as Ministry of Health directives to provide care for dental emergencies only. Another study showed similar findings in Spain [30], indicating a significant decrease in the number of patients seen by dentists during the national state of alarm; 86% of participants reported seeing up to five patients per week due to recommendations to treat only urgent situations. In the early stages of the pandemic worldwide, a shortage of PPE was also a significant concern. Lack or inadequate availability of PPE has been reported to potentially impose negative impact on the mental health of professionals [34], and may worsen the scenario. One could argue that pandemic-associated increases in the need for medical devices and PPE, and the emerging vaccine industry, should be favorable to business in the biomedical industry. However, in Brazil, this industry accounts for less than 43% of the national consumption production in general biomedical supplies [35]. KaVo, a major dental company worldwide, recently closed its manufacturing facilities in Brazil, which may be an early sign of employment loss in the sector. Government-aided measures to support PPE supply and biomedical industries could be necessary in the long term.

The present study also points out concerns with regard to economic burden associated with changes in routine dental practices. In corroboration, a prior economic analysis showed that COVID-19 mitigation/suppression measures will cause financial distress to private dental clinics in Germany [36]. A total 35% dentists participating in the present survey, for instance, reported that N95 masks were the predominant mask used (with at least half of patients). Taking into account the pre-pandemic volume of patients treated weekly by this sample (average 39.6 patients/dentist), and the ~348,000 dentists registered in Brazil, generalizing the figure of 35% of dentists treating at least half of their patients wearing N95 masks without re-use, dentists in Brazil can be expected to use some 9.6 million masks per month. Considering typical prices for surgical masks (0.4 USD) and N95 masks (2.92 USD) (quotes retrieved by authors and available in doi:10.17605/OSF.IO/DNBGS), the yearly cost of this simple PPE change would be ~290 million USD, which would amount to approximately 1.16 billion USD over a potential 4-year COVID-19 resurgence risk period [37].

It should be noted that our study design does not allow one to establish cause-effect relationships, thus our findings should be treated with caution. In addition, it should be considered that regional COVID-19 rates could be influenced by socioeconomic factors, which may additionally play a role on the behavior of dental professionals. Although the representativeness of the sample may have limitations, the distributions of responses by region, sex, and age were similar to the overall distributions of dentists in Brazil (Table 2), except for higher response rates from females and from dentists working in Southern Brazil. Notwithstanding, our sample variability was supported by the large numbers of responses received. A report from 2009 [12] showed that the proportion of female dentists in Brazil was in a rise, which also may account for the differences in sex observed between respondents here. The present findings also suggest that female dentists could be more likely to engage in survey research than male dentists, at least during the pandemic. Collecting responses by an open campaign on social media also imposes limitations [15], including a higher chance of recruiting dentists who were more afraid about the pandemic or more willing to cooperate with sanitary measures. The fact that the social media campaign was originated in Southern Brazil explains the higher proportion of respondents from the South region [15]. It is also worth mentioning that the South and Southeast regions, which have similar human development index and per capita income values [38, 39], represent the highest-income regions of Brazil.

Future studies will be necessary to monitor how dentists are coping with the pandemic. Data from this study may be useful as a baseline relative to future developments and useful in designing interventions. The scenario observed in May 2020 can be used for future observations on the impact and evolution of the pandemic to the dental sector in Brazil and Latin America, as well as potentially associated crises. Brazil is a big player in dentistry worldwide, with a particularly predominant role in Latin America. Unfortunately, given its concentrated effects in the public dental care sector, the pandemic appears to be contributing to a deepening of already marked inequalities in oral health within Brazil, and such effects may extend more broadly into Latin America. Inadequate public healthcare funding in the short to long term may increase the risk of exacerbating historical inequalities between regions in Brazil. Actions taken now will affect how Brazilian dentistry is regarded after the pandemic, and whether Brazil will be a good or bad example of dental practices, especially for neighboring countries. Even after the contagion curve is flattened, we can expect precautionary changes to dental clinic routines and associated stress to persist for years given that dental professionals will continue to be at high risk of exposure, especially in the event of a future resurgence. Ultimately, the outlook of the dental sector depends on political, professional, and personal actions in this turbulent period during which major aspects are at stake.

Conclusions

This survey gathered 3,122 responses from all regions of Brazil in May 2020, when the country was a new pandemic epicenter and the contagion curve was escalating. The results provide early evidence of three major impacts of the pandemic on the dental sector: increasing inequalities due to care coverage differences between the public and private networks; the adoption of new clinical routines, which are associated with an economic burden for dentists; and associations of regional COVID-19 incidence/mortality with fear of contracting the disease at work. Constant monitoring of the situation is encouraged over the course of events in the ongoing pandemic.

Questionnaire (original language: Brazilian Portuguese).

(DOCX)

Click here for additional data file.

20 Aug 2020

PONE-D-20-21705

COVID-19 challenges to dentistry in the new pandemic epicenter: Brazil

PLOS ONE

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Reviewer #1: Partly

Reviewer #2: Partly

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Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #1: Yes

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Reviewer #1: This study aimed to assess COVID-19 pandemic effects on dental coverage, dental office routines and economic burdens, and the behaviour of dentists.

1. The sampling methodology is poorly described, for example, how do you know that a dentists (anonymously) belong to each state?

2. Covariates criteria and categories are simple and unclear, such as: did both the 1000 cases /100 deaths per million inhabitants in each state represent each state or a unit?

3. Data analysis are also simple and unclear, especially for multilevel models: what was ‘null model’? and what is difference ‘OR’ and “MOR’? were models adjusted for any covariates?

4. There is insufficient discussion of the relevance and the aim of the study following the findings/results.

5. Discussion section: it is short of strength and limitation reporting.

Reviewer #2: 1. Introduction doesn't cover enough background of research conducted so far on the topic.

2. Methods section is too lengthy and has many repeated explanations

3. The response rate is very low though the sample size is adequate. since its a national wide survey, the response rate is critical. so i would suggest to improve the response rate and subsequent analysis

4. Discussion is too general and not based on important findings of the study. I would suggest to compare findings with other countries. It is more important to discuss on how these findings helps for change in policy as mentioned in the manuscript. further discuss the impact of pandemic on dentistry in other countries.

5. Please check the references as some are repeated in the list.

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Reviewer #1: Yes: Xiangqun Ju

Reviewer #2: Yes: Dr Gadde Praveen

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23 Sep 2020

Editor:

Although manuscript is suitable for publication but it is poorly written. Authors must improve the presentation of the paper in line with reviewers comments.

R: We respect your editorial comments but we do not agree that the manuscript was poorly written. We agree, however, that some aspects could be clarified, and the text improved, by considering the inputs from reviewers. We have made efforts to edit the text according to all suggestions from the reviewers. It is good to have an external view and clarify our article, but we respectfully disagree the report was poor. We want to highlight that the paper addresses the impact of COVID-19 to Brazil, which sadly is still the pandemic epicenter by September 2020. This means that the scope of the article was kept to Brazil but, in accordance with suggestions placed by the reviewers, the pandemic scenario and challenges imposed to the dental sector in other countries were addressed.

Reviewer #1:

1. The sampling methodology is poorly described, for example, how do you know that a dentists (anonymously) belong to each state?

R: We disagree that methods were poorly described in the original paper. However, we have made efforts to improve clarity in all aspects raised by both reviewers. Information about the place of work of dentists, for instance, was available in the questionnaire submitted as a supplemental material. The instrument was a self-administered instrument, all responses were self-reported as detailed in the original manuscript. The participants were not asked to identify themselves but demographic data were collected and reported accordingly. In the original submission, the SURGE reporting guidance (Grimshaw 2014) was used for addressing important reporting aspects in the paper. Notwithstanding, we have revised the manuscript and included further details, now also addressing the CHERRIES reporting guideline (Eysenbach 2004) in order to cover all items that are considered relevant in online survey research. In our opinion, the sampling is adequately described, with enough details for one to understand how participants were recruited and responded to the questions presented in the survey. We have also recently published a methodological preprint manuscript (Moraes et al., 2020) addressing underlying data related to the methods used in this study. This information was addressed in the revised article and the study quoted in the references list.

Grimshaw J. SURGE (The SUrvey Reporting GuidelinE). In: Moher D, Altman DG, Schulz KF, Simera I, Wager E, editors. Guidelines for reporting health research: A user’s manual. 1st ed. Hoboken (NJ): John Wiley & Sons 2014; 206–213.

Eysenbach G. Improving the quality of Web surveys: The Checklist for Reporting Results of Internet E-Surveys (CHERRIES). J Med Internet Res 2004; 6(3):e34.

Moraes RR, Correa MB, Daneris A, Queiroz AB, Lopes JP, Lima GS, Cenci MS, D'Avila OP, Pannuti CM, Pereira-Cenci T, Demarco FF. Email vs. Instagram recruitment strategies for online survey research. medRxiv 2020.09.01.20186262; doi: https://doi.org/10.1101/2020.09.01.20186262

2. Covariates criteria and categories are simple and unclear, such as: did both the 1000 cases /100 deaths per million inhabitants in each state represent each state or a unit?

R: The units of analysis of both variables related to 1000 cases/100 deaths per million inhabitants are the states. This was the reason for the adoption of multilevel models, i.e., to consider in the analysis individuals nested in the same cluster (states). This information was clarified in the manuscript in the following passage:

“For analysis purposes, data were converted into thousands of cases and hundreds of deaths per one million inhabitants in each state. The units of analysis of both variables are the states. Multilevel mixed effect models were used to test the association between the contextual variables related to the status of the pandemic in each state and dentistry-related outcomes. Outcomes included decrease in number of patients assisted weekly (numerical), fear of contracting COVID-19 at work (no/a little vs. yes/a lot), and current work status (normal/reduced vs. not working/emergencies only). Linear and logistic models were used for numeric and binary outcomes. The models considered two levels of organization: dentist (level 1) and state (level 2). β-coefficients and Odds Ratios (OR) were reported. Contextual level variance was assessed using intraclass correlation coefficient (ICC) for linear models and Median Odds Ratio for logistic models (α=0.05).”

3. Data analysis are also simple and unclear, especially for multilevel models: what was ‘null model’? and what is difference ‘OR’ and “MOR’? were models adjusted for any covariates?

R: The analyses were not adjusted by covariates because we have not hypothesized that individual factors would confound the association between the pandemic status in states and outcome variables. The Median Odds Ratio (MOR) is a measure of variance that can be attributed to a contextual level. It is analogous to the Intraclass Correlation Coefficient (ICC, also reported in the paper), being applied to binary outcomes. As stated by Merlo et al. (2006), “The aim of the median odds ratio (MOR) is to translate the area level variance in the widely used odds ratio (OR) scale, which has a consistent and intuitive interpretation. The MOR is defined as the median value of the odds ratio between the area at highest risk and the area at lowest risk when randomly picking out two areas the MOR can be conceptualized as the increased risk that (in median) would have if moving to another area with a higher risk.” In contrast, odds ratio (OR) was used as an effect measure in the logistic regression. Interpretation of each MOR and OR were provided in the results section. We do not believe that describing the explanation on what is the MOR in the manuscript is needed, but we do believe that the statistical models used, although may not be familiar to every researcher, were helpful in understanding the contextual effects on dentists-related outcomes. Results of contextual level variance of null models were added to the tables 4 and 5 according to your suggestion. Contextual level variances were estimated using ICC for linear models and MOR for logistic models. Both ICC and MOR were estimated for null (empty) and adjusted models, the tables now show both models.

Merlo J, Chaix B, Ohlsson H, et al. A brief conceptual tutorial of multilevel analysis in social epidemiology: using measures of clustering in multilevel logistic regression to investigate contextual phenomena. J Epidemiol Community Health. 2006;60(4):290-297.

4. There is insufficient discussion of the relevance and the aim of the study following the findings/results.

5. Discussion section: it is short of strength and limitation reporting.

R: The discussion section was improved to cover more aspects and implications related to our results. In addition, the revised Discussion section also compares our findings to those of studies conducted in other countries, as suggested by Reviewer #2. Discussion on relevance of findings was also improved, as well as on strengths and limitations of the study.

Reviewer #2:

1. Introduction doesn't cover enough background of research conducted so far on the topic.

R: The Intro section was revised to cover more research on the topic carried out in other countries. However, we want to highlight that the present study is a report on the challenges of COVID-19 pandemic imposed to the dental sector in Brazil, so the focus was kept to Brazil which, unfortunately, is still the pandemic epicenter as of September, 2020. Findings from other countries also were addressed in the Discussion section.

2. Methods section is too lengthy and has many repeated explanations

R: We understand your point but this comment is actually contrary to a comment placed by Reviewer #1, who indicates the methods were poorly described. We have made efforts to reduce the duplicity of information as much as possible. The methodology was described in full details to allow the reader to understand how the questionnaire was constructed and pre-tested, and how participants were recruited. This may also increase reproducibility of the methods, which is a topic that has been debated with emphasizes in science nowadays (Baker 2016). May we highlight that the methods section now includes two different reporting guidelines in order to cover all important aspects that are considered relevant in survey research: SURGE (Grimshaw 2014) and CHERRIES (Eysenbach 2004).

Baker M. 1,500 scientists lift the lid on reproducibility–Survey sheds light on the ‘crisis’ rocking research. Nature 533, 452–454.

Grimshaw J. SURGE (The SUrvey Reporting GuidelinE). In: Moher D, Altman DG, Schulz KF, Simera I, Wager E, editors. Guidelines for reporting health research: A user’s manual. 1st ed. Hoboken (NJ): John Wiley & Sons 2014; 206–213.

Eysenbach G. Improving the quality of Web surveys: The Checklist for Reporting Results of Internet E-Surveys (CHERRIES). J Med Internet Res 2004; 6(3):e34.

3. The response rate is very low though the sample size is adequate. since its a national wide survey, the response rate is critical. so i would suggest to improve the response rate and subsequent analysis

R: The response rates cannot be improved since the survey was conducted in May 2020. The issue was discussed in the text, and the fact that the study was conducted when Brazil was recently a new pandemic epicenter was highlighted. The pandemic scenario changes quickly and new responses collected now could not be considered belonging to the same context, which was as important aspect in the study, as discussed in a comment for Reviewer #1.

4. Discussion is too general and not based on important findings of the study. I would suggest to compare findings with other countries. It is more important to discuss on how these findings helps for change in policy as mentioned in the manuscript. further discuss the impact of pandemic on dentistry in other countries.

R: The discussion section was improved to cover more aspects related to our results compared to studies conducted in other countries, following your suggestion. Discussion on relevance of findings was also improved, as well as on strengths and limitations of the study.

5. Please check the references as some are repeated in the list.

R: We found one reference (Morita et al.) repeated in the list, thanks for noticing. The mistake was corrected. New references were quoted in the revised manuscript.

Submitted filename: Response to Reviewers.docx

Click here for additional data file.

30 Oct 2020

COVID-19 challenges to dentistry in the new pandemic epicenter: Brazil

PONE-D-20-21705R1

Dear Dr. Moraes,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

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Kind regards,

Srinivas Goli, Ph.D.

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Revisions approved by the reviewers and also satisfactory to me.

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: All comments have been addressed

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2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The answers to my questions were well addressed, and the manuscript has been improved and valuable. I have two comments to be considered as minor corrections:

1. Please add full name for ‘SURGE’ and ‘CHERRIES’ (Line 111, page 5)

2. What variables were adjusted for? Please introduce/explain adjusted models in both the Methods section (data analysis) and Table 4 and 5 (footnotes).

Reviewer #2: The article adheres to appropriate reporting guidelines and community standards for data availability

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Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: Xiangqun Ju

Reviewer #2: Yes: Dr. Gadde Praveen

17 Nov 2020

PONE-D-20-21705R1

COVID-19 challenges to dentistry in the new pandemic epicenter: Brazil

Dear Dr. Moraes:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

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