Effects of the COVID-19 pandemic on dental services in primary care in Maranhão, Brazil

This article aims to analyze indicators of the utilization of oral health services (UOHS) in primary health care in the state of Maran-hão, Brazil, before and during the COVID-19 pandemic. We conducted an ecological time series study. The unit of analysis was the state of Maranhão, and the exposure variable was the COVID-19 pandemic, dichotomized into pre-pandemic and pandemic. The outcome variables were the monthly rates per 1,000 population of three UOHS indicators: rate of preventive procedures (RPP-PHC); rate of urgent procedures (RUP-PHC), and rate of curative procedures (RCP-PHC). The data were collected from the Primary Health Care Information System (SIS-AB) and the Brazilian Institute of Geography and Statistics (IBGE) for the period from 2015-2022. The analyses were performed using the Seasonal Autoregressive Integrated Moving Average (SA-RIMA) model. The three indicators showed an upward trend up to January 2019. The pandemic caused a significant reduction in the RPP (Xreg = -6.55; p-value = 0.0008) and RCP (Xreg = -4.74; p-value = 0.0005), starting in the first semester of 2020 and continuing into the second semester of 2022, but did not influence the RUP (Xreg = -0.03; p-value = 0.12). The COVID-19 pandemic caused a reduction in preventive and curative oral health services in Maranhão.


Introduction
The inclusion of the first oral health teams (OHts) in the Family Health Program (FHP)/ Family Health Strategy (FHS) in the 2000s led to improvements in oral health indicators [1][2][3] .However, the role of oral health professionals working in primary health care (PHC) services was limited during the COVID-19 pandemic due to the measures adopted in response to the health crisis 4,5 and people's fear of exposure to the virus in dental surgeries 6 , leading to lower availability of and demand for public oral health services and, consequently, negatively affecting oral health indicators.
Studies in Brazil have highlighted the impact of the pandemic on the provision of oral health care under the country's public health system, o Sistema Único de Saúde (SUS) or Unified Health System.Da Cunha et al. (2021) compared the rate of hospitalization due to oral and oropharyngeal cancer before and during the pandemic, demonstrating that admissions dropped by 49.3% across the country between 2019 and 2020 7 .There is also evidence of the effects of the pandemic on access to oral health care in PHC 8 , the number of oral biopsies performed 9 , prosthetic treatments 10 , and dental appointments for children 6 .Santos et al. (2021) reported a reduction of 66% in outpatient dental procedures on the SUS between January and June 2020 and were the only researchers to investigate the effects of the COVID-19 pandemic on oral health care provision under the SUS across states.Although a decline in indicators was identified in states across all of Brazil's five regions, the highest reduction in dental treatments in PHC services was observed in Maranhão, one of the three states in the country with the lowest Human Development Indicators (HDIs) 11 .Maranhão was also one of the states that saw a rapid spread of the disease.During May 2020, the number of municipalities with confirmed cases increased from 15 to 212 (of a total of 217) 12 .
Studies are limited to comparisons of the average number of procedures performed in the first semester of 2020 and the same period in 2019.These studies used tests that fail to consider trends, seasonality, and residuals, which can lead to biased estimates of the effects of the pandemic on oral health indicators.In addition, it is not known whether the identified effects persisted in the second semester of 2020, when, to reduce the adverse effects of the pandemic on oral health, new resolutions encouraged dental surgeons to return to work activities, with the adoption of prevention and control measures for the treatment of suspected and confirmed cases of COVID-19 13,14 .
The aim of this study was to perform an interrupted time series analysis of indicators of the utilization of oral health services (UOHS) in PHC in Maranhão, one of Brazil's poorest states and the state that showed the largest reduction in availability of dental treatment before and after the COVID-19 pandemic.This analysis provides a more accurate quantification of the effects of the pandemic on oral health indicators due to the higher number of observations of indicators over time 15 .Our hypothesis is that the pandemic caused a decline in indicators, which persisted up to the second semester of 2022.

Methods study design
We performed an interrupted time series analysis, where data are collected before and after an event to quantify the effects of interruptions occurring in the data series 16,17 .The data were collected from databases in the public domain and the unit of analysis was the state of Maranhão.

study location
Maranhão is located in the Northeast region, which is part of the Legal Amazon.It has a population of 7,075,181 inhabitants and is the country's eighth largest state, with an area of 329,642,182 sq km 18 .The latest data show that PHC coverage in the state in 2020 was 87.75%, while oral health team coverage rose from 62.75% in 2015 to 71.88% in 2021 19,20 .

study variables and data sources
The exposure variable (interruption in the time series) was the COVID-19 pandemic, considered a dichotomous variable, where the value "0" represents pre-interruption (January 2015 to March 2020) and value "1" is the point of interruption (April 2020 to December 2022).This categorization was adopted considering that the effects of the pandemic began in April, the month after the notification of the first case of the disease in the state, according to the disease bulletins available on the website of the Maranhão State Department of Health (SES-MA) 21 .
The outcome variables were the monthly rates per 1,000 population of three UOHS indicators: rate of preventive procedures (RPP-PHC); rate of urgent procedures (RUP-PHC), and rate of curative procedures (RCP-PHC).The numerator data were obtained from the Primary Health Care Information System (SISAB) for the period 2015-2022 and the denominator data were derived from census population projections provided by the Brazilian Institute of Geography and Statistics (IBGE).The procedures in each category (preventive, urgent, and curative) are shown in Table 1.

Data processing and statistical analysis
A brief descriptive statistical analysis of dental procedures was performed, estimating measures of central tendency (means) and dispersion (standard deviation and minimum and maximum values).The interrupted time series was analyzed using the Seasonal Autoregressive Integrated Moving Average (SARIMA) model.
SARIMA is employed with non-stationary seasonal time series and comprises the parameters p, d, q (P, D, Q): AR: (p = degree of the autoregressive part); I: (d = degree of the first difference); MA: (q = degree of moving-average part); and S: (P, Q and D relative to seasonality).The analysis was divided into three stages: 1) Identification of the appropriate model, visualizing the series breakdown process; 2) Estimation of best-fitting model parameters, considering the parsimony analysis of specific criteria and residual autocorrelations; and 3) Application of the model using interruption analysis 22 .
The identification of the appropriate model commenced with a random exploratory analysis of trends, seasonality, and residual values.The Kwiatkowski-Phillips-Schmidt-Shin (KPSS) test was then applied, adopting a 5% significance level and null hypothesis of series stationarity.The automatic ndiffs command from the urca package was used to estimate the number of differences required to make the time series stationary 23,24 .
An initial estimation of the model parameters was performed using parsimony analysis of the smallest values for the Akaike information criterion (AIC) and Bayesian information criterion (BIC), mean absolute percentual error (MAPE), and root mean squared error (RMSE) resulting from parameter combinations [23][24][25] .To determine the final model, we used the automatic auto.arima command from the forecast package to indicate the best-fitting model, based on combinations of unit root tests, AIC minimization, and maximum likelihood estimation.Both determinations coincided, confirming the accuracy of the selection of the adjusted model.
The adjustment of the model involved the removal of trend and seasonality, reducing differences between model values and observed values to close to zero 23,24 .The application of the model was tested using the series interruption coefficient (alpha = 5%).
The time series was tested for residual autocorrelations using the Ljung-Box and Box-Pierce tests, adopting a 5% significance level 24,25 .All analyses were performed using the R programming language for statistical analysis and RStudio Desktop version 1.3.1093.

Ethical aspects
The study protocol was approved by the Maranhão Federal University Hospital's research ethics committee (code number CAAE: 35645120.9.0000.5086).

results
A total of 154,000, 1,848, and 124,447 preventive, urgent, and curative procedures, respectively, were carried out in Maranhão in January 2019, compared to only 5,324, 226, and 3,320, respectively, in May 2020.Preventive procedures were the most common type of procedure, with the total number of procedures in this category exceeding the sum of the other categories.Mean (± standard deviation) RPP, RUP, and RCP were 9.86 ± 5.00, 0.10 ± 0.03, and 7.47 ± 3.15, respectively (data not presented).
Although the three outcome variables showed variation throughout the time series, there was a predominantly upward trend up to 2019, followed by a reduction in rates in 2020.The findings show a regular six-monthly pattern in rates throughout the time series, with smaller monthly variations being observed in the final months of each semester (Figure 1).
Variations in rates were similar across the outcome variables, being greater in the first three months of the semesters and lower in the last three months.December had the lowest monthly variation across all dental procedures (Figure 2).

Discussion
This interrupted time series study analyzed the effect of the COVID-19 pandemic on the utilization of oral health services in PHC in Maranhão between January 2015 and December 2022.During this period, the pandemic caused a significant reduction in the number of preventive and curative procedures per 1,000 population (-6.54 and -4.74, respectively).Urgent procedures were not affected by the pandemic.
Preventive procedures were the most common type of procedure, which may be due to the focus on health promotion and disease prevention in PHC 26 .The highest rate of preventive procedures was observed in January 2019.This may be the result of public health and intersectoral    organization of oral health services and in patient demand.These trends may have been affected by staff leave patterns, school holidays, and end-ofyear festivities 27 .

Variable
The reduction in UOHS in Maranhão is consistent with the findings of previous studies in Brazil [6][7][8][9][10][11] .Santos et al. (2021) reported statistically significant reductions in outpatient dental procedures performed in Brazil when comparing the first semester of 2019 and the same period in 2020.Reductions in preventive actions were identified across all states, including those with a high HDI, such as the Federal District (-31.55%;p-value < 0.001) and Rio Grande do Sul (-49.09%;p-value < 0.001), and those with low HDI, such as Alagoas (-61.21%;p-value < 0.001) and Maranhão (-91.83%;p-value < 0.001) 11 .Reductions were more pronounced in states with low HDIs, corroborating the hypothesis stating that there is an association between poverty and social inequality and oral diseases 28 .In addition, it is possible that poorer states need more time to reorganize the safe provision of oral health services to ensure that indicators return to pre-pandemic levels.Further research is required to address this gap.
International studies have also noted a significant reduction in specialized curative procedures in private clinics, public health systems, and/or teaching clinics [29][30][31] .For example, in a study analyzing the medical records of patients of an integrated adult dental clinic linked to a degree in Dentistry offered by the Rey Juan Carlos University of Madrid, Gómez-Costa et al. (2022)  found that periodontal and endodontic treatments were the procedures most affected during the pandemic 31 .Another example is a study conducted in private dental clinics in Germany with different provider scenarios (low/high volume practice, low/high proportion of non-statutory insurance revenue; and low/high staff pool and costs).The findings show reduced utilization of all services, with reductions being more severe for prevention (-80% on average), periodontics (-76%), and prosthetics (-70%) 29 .
The fact that there were no significant differences in urgent procedure rates may be explained by the guidelines produced by health organizations around the world, which recommended the suspension only of elective non-emergency dental care 32,33 .In addition, patients suffering pain continued to seek urgent care despite the fear of visiting health facilities in the midst of a pandemic 6 .
A study in the University Center of Dentistry and Specialized Medicine in Poland found a significant increase in urgent surgical procedures when comparing two periods: pre-pandemic (1 February 2019-31 January 2020) and pandemic (1 February 2020-31 January 2021) 30 .The broad interpretation of what comprises urgent care and unclear codes on appointment forms are factors that may explain these controversial findings 34 .
Other long-term impacts of the pandemic include the aggravation of oral diseases.For example, the absence of oral cancer screening, which is performed during routine dental appointments, may have resulted in delays in diagnosis and treatment 35,36 .
Despite the resumption of elective dental care, vaccination of health workers and the general population, improvements in biosafety, teleconsultations, and the use of minimally invasive approaches 14,33,34 , it is evident that these strategies may not have been enough for indicators to return to pre-pandemic levels.
We recommend the organization of dental care to ensure the safe provision of services and enable a return to pre-pandemic levels.Based on published guidelines, measures that can be incorporated into everyday practice in primary care facilities offering dental services include: entry respiratory syndrome screening of patients and the provision of rapid tests for suspected cases; use of adequate personal protective equipment, including N95/PFF2 masks, goggles, face shields, lab coats, and disposable bouffant caps; reducing the number of scheduled appointments; increasing the frequency of cleaning and disinfection of surfaces; and ensuring well-ventilated and clean spaces, with large windows or the use of appropriate filters in air-conditioning units 4,5,13,14 .
Our study has some limitations.The selection of the best-fitting model may have been affected by the surveillance data available in the SISAB.However, this system is the official government data source and the professionals responsible for inputting data receive specialist training to avoid double entry and guarantee data quality, and data are validated to ensure internal consistency.This information system is also used by studies that provided support for health manager and professional decision-making 37,38 .While we chose to dichotomize the intervention to be able to analyze the data in the presence and absence of the pandemic, future research should analyze effects in different contexts, considering, for example, number of cases and deaths, the lockdown, and urban mobility rates.
Study strengths include the following: the study period covered three years of the pandem-ic, enabling the analysis of prolonged effects on indicators; the modeling technique employed increases the robustness of analyses of the effects of health interventions on indicators, using an automatic command (auto.arima) to select the best-fitting model based on a combination of multiple tests; we indirectly analyzed the effects of service planning during the pandemic.
It is concluded that the pandemic caused a significant reduction in preventive and curative dental procedures in PHC in Maranhão and that this effect continued up to the second semester of 2022.The results of this study contribute to a bet-ter understanding of the effects of the COVID-19 pandemic on oral health indicators in regions with low socioeconomic status.However, caution should be taken when making generalizations.
It is recommended that the discussion of strategies and modifications and adaptations to health facilities during the pandemic and post-pandemic in the case of new waves of the disease should be a constant process.The results of this study can also contribute to the reorganization of health services during states of public calamity and the revamping of the National Oral Health Care Policy.

Collaborations
FS Sousa contributed to the conception of the study, data collection, analysis and interpretation, manuscript writing and revision.EM Costa, ESM Rodrigues, and MBS Lopes contributed to data analysis and manuscript revision.EBAF Thomaz contributed to the conception of the study, data analysis and interpretation, and manuscript revision.All authors approved the final version.

figure 1 . 2 .
figure 1. Breakdown of the time series into indicators of utilization of oral health services in PHC in Maranhão, Brazil (2015-2022).Source: Authors.

table 1 .
Procedure categories and corresponding PHC dental appointment form codes included in the search strategy.

table 2 .
policies, such the School Health Program (PSE) and new National Primary Health Care Policy (PNAB), both enacted in 2017, and the publication of Ministry of Health guidance documents, including the book A Saúde Bucal no Sistema Único de Saúde (Oral Health under the Unified Health System) in 2018.The repetition of six-monthly trends where procedure rates always fall off at the end of the semester may be a result of seasonal trends in the Parameters of the best-fitting models for indicators of utilization of oral health services in PHC inMaranhão.Brazil (2015-2022).
AIC = Akaike information criterion; BIC = Bayesian information criterion; MAPE = mean absolute percentual error; RMSE = root mean squared error; box-Pierce and Ljung-box = tests for residual autocorrelations.Source: Authors.table 3. Effects of the COVID-19 pandemic on indicators of the utilization of oral health services in PHC in Maranhão, Brazil (2015-2022).