Demographic, social, and clinical aspects associated with access to COVID-19 health care in Pará province, Brazilian Amazon

Internal social disparities in the Brazilian Amazon became more evident during the COVID-19 pandemic. The aim of this work was to examine the demographic, social and clinical factors associated with access to COVID-19 health care in Pará Province in the Brazilian Amazon. This was an observational, cross-sectional, analytical study using a quantitative method through an online survey conducted from May to August 2023. People were eligible to participate if they were current residents of Pará, 18-years-old or older, with self-reported diagnoses of COVID-19 through rapid or laboratory tests. Participants completed an electronic survey was developed using Research Electronic Data Capture (REDCap) software—The adapted questionnaire “COVID-19 Global Clinical Platform: Case Report Form for Post-COVID Condition”. Questions focused on access to COVID-19 treatment, demographic characteristics, COVID-19 vaccine and clinical characteristics. Respondent-driven sampling was applied to recruit participants. Multiple logistic regression was utilized to identify the associated factors. Overall, a total of 638 participants were included. The average age was 31.1 years. Access to COVID-19 health care was 68.65% (438/638). The participants most likely to access health care were those with moderate or severe COVID-19 (p = 0.000; OR: 19.8) and females (p = 0.001; OR: 1.99). Moreover, participants who used homemade tea or herbal medicines were less likely to receive health care for COVID-19 in health services (p = 0.002; OR: 0.54). Ensuring access to healthcare is important in a pandemic scenario.


Participants and selection criteria
People were eligible to participate if they were current residents of Pará, 18-years-old or older, with self-reported diagnoses of COVID-19 through rapid or laboratory tests.The exclusion criterion included people who did not have access to the internet or electronic devices to answer the questionnaire.

Study size
The calculations were performed in the population survey in the EpiInfo version 7.2.5.0 in the StatCalc module.For the sample calculation of the quantitative study, the following parameters were adopted: 777,901 people with COVID-19 infection in Pará; margin of error of 5%; 95% confidence interval, 38.6% frequency of people with reactive IgG who used preventative medication for COVID-19 9 (people who received preventive medication for COVID-19, including medicines that require a doctor's prescription -people who sought health care to treat COVID -19).The use of health care was not limited to people with moderate or severe symptoms, thus resulting in a minimum sample of 364 participants.This number quickly exceeded that of the online survey; therefore, it was decided to use the total number of people who responded to the questionnaire during the data collection period.

Study instrument (questionnaire)
To collect data, an adapted version of the "Global COVID-19 Clinical Platform: Case Report Form for Post-COVID-19 conditions" questionnaire from the World Health Organization was used 27 .The questionnaire (structured) was adapted and translated by researchers from three federal universities in different regions of Brazil to make the language clear and accessible to the general population.To make the questionnaire easy to complete, unnecessary reading effort was reduced, and a cohesive and coherent order was established between the questions.Participants took an average of 15 min to complete the questionnaire.The questionnaire was organized into six domains.For this study, only two domains were used: sociodemographic and clinical characteristics related to SARS-CoV-2 infection.
In the sociodemographic domain, the following variables were used: sex (female/male); traditional population (yes/no); age (years); skin color (black/brown/indigenous/white/yellow); education level (did not study/ elementary/high school/university); living in the state capital (yes/no); current job (unemployed/student/retired/ employed/self-employed); beneficiary of social programs (yes/no); tobacco use during the pandemic (yes/no); use of alcoholic beverages during the pandemic (yes/no); personal monthly income minimum wage (in reais) (equal or less than 1 salary/above 1 salary); marital status (married/common-law/divorced/separated/widowed/single).
In the clinical characteristics domain related to SARS-CoV-2 infection, the following variables were considered: number of COVID-19 reinfections that were laboratory confirmed (mean); year of first COVID-19 infection (2020-2021/2022-2023); chronic illness before COVID-19 infection (yes/no); and classification of the most serious COVID-19 infection (severe: was admitted to the intensive care unit or needed to be intubated/ moderate: had proven pneumonia or was hospitalized or needed oxygen support/mild: respiratory symptoms, but no pneumonia or shortness of breath); herbal medicines and homemade tea (yes/no); COVID-19 vaccine (yes/ no); number of doses of COVID-19 vaccine (mean); and COVID-19 infection before being vaccinated (yes/no).
In this study, we considered traditional populations of the Amazon as those inhabiting the waters, fields, and forest: quilombola remnants (Afro-descendants who live in specific territories), indigenous peoples and riverside dwellers, following the concept established by the National Policy for Comprehensive Health of Rural and Forest Populations 28 .

Data collection
Participants completed an electronic survey using Research Electronic Data Capture (REDCap)® -software, including the adapted questionnaire "COVID-19 Global Clinical Platform: Case Report Form for Post-COVID-19 Condition".Respondent-driven sampling (RDS), which is a variant of the "snowball sampling" methodology that is widely used in online surveys, was applied to recruit participants [29][30] .Through this method, participants are encouraged to share the questionnaire link with other individuals who meet the study's inclusion criteria to respond to the survey via social networks, with WhatsApp® being the social network that was used in this study.
To reach the minimum sample size, students from health-related undergraduate programs in all of the municipalities of the state were recruited.They underwent a four-hour training session on conducting the online survey by using the RDS methodology and the clarification of questionnaire-related queries.Each student invited 10 individuals from their circle who reported of COVID-19 infection to participate in the research.For each respondent who completed the survey, they correspondingly referred another 10 individuals, thus creating reference chains that increased the recruitment cycles/waves and expanding the number of participants [29][30] .In this study, 201 students were recruited and divided among 31 training sessions.Each student recorded data in an Excel spreadsheet, which included the number of participants who they invited, how many people were referred by each invitee, and other factors.This process was repeated until researchers achieved the minimum sample for the study.
The completed questionnaires were hosted on the REDCap® platform, which is designed for online data management and features settings and tools that enhance organizational capacity and security for storing information.It is important to highlight that, given the nature of the online survey, all of the collected information was self-reported.

Variables
The response variable of the study was the question "How was your treatment/health care?".The answers to this question were "I was treated alone, without evaluation by a health care professional", "I was admitted to a ward", "I was admitted to an intensive care unit", "I was treated at home, with support from health care professionals via telephone or internet", "I received care in an outpatient clinic (the clinics provide specialized outpatient secondary care)", "I received care in a private hospital (agreement/health insurance)", "I received care in an emergency room or an emergency care unit", and "I received care in a health center (PHC)".The health center or basic health unit involves primary health care services provided by generalist health professionals, which can be offered by the government (free) or in private services.In Brazil, there are a large number of services offered by the government.
All of the responses in which participants stated that they received health care were grouped into a single response: "I received health care".The outcome is a dichotomous qualitative variable, "Received" or "Not Received (self-care)".The response event was "received".The independent variables included the variables that were included in the questionnaire, which are divided into the following domains: demographic, social characterization, and clinical characteristics.

Quantitative variables
The variables age, number of COVID-19 reinfections, and number of doses of the COVID-19 vaccine were analyzed as quantitative (continuous variables) independent variables.

Statistical methods
The data were extracted from REDCAP® and exported to Microsoft Excel®.Descriptive statistics, means, standard deviations, confidence intervals, absolute frequencies, and percentages were calculated.The result was presented by using texts, graphics, and tables.The 'nonresponse" variables were excluded from the statistical analysis, and no percentage was calculated.
The main hypothesis of the study, "factors associated with receiving treatment/health care (access to health care)", was tested by using multiple logistic regression.When considering the dichotomous nature of the response variable, binomial regression was initially used to assess the association between each independent variable and the dependent variable.All of the variables were tested in this model, and variables with a p value < 0.020 were selected for inclusion in the multiple logistic regression model (sex, traditional population, age, education level, living in the state capital, individual income, marital status, number of COVID-19 reinfections, chronic illness before COVID-19 infection, classification of the most serious COVID-19 infection, use of herbal medicines and homemade tea, and number of doses of COVID-19 vaccine).
In the final multiple logistic regression model, the variables with p values < 0.20 were analyzed together by using the backward elimination model.This involves the introduction of all factors that were selected in the first stage and at each stage of the regression and is automatically removed by the program until only factors with a p value < 0.10 remain (number of COVID-19 reinfections, sex, chronic illness before COVID-19 infection, classification of the most serious COVID-19 infection, and use of herbal medicines and homemade tea).
All p values < 0.05 were considered to indicate statistical significance.To interpret the results, quality tests, coefficient values of the independent variables, Z values, 95% confidence intervals, and odds ratios were considered in the regression.The analyses were performed by using the Bioestat 5.3®, Microsoft Excel®, and Minitab 20® programs.

Sociodemographic characteristics
In this study, 438 (68.65%) out of 638 participants received health care for COVID-19, whereas the remaining 200 (31.35%)participants chose self-care (not received).The average age was 31.1 years (standard deviation [SD] = 11.9;95% CI: 30.2, 32.0), and the 18-to 32-year-old age group had the highest percentage at 66.3% (421).Among the participants, 68.3% (436) were female; 40.8% (258) were employed or retired; 35.9% (229) were selfdeclared students; 57.9% (357) had incomes less than or equal to the minimum wage; 74% (472) were unrelated (divorced, separated, widowed or single); 11.7% (74) were beneficiaries of social programs; and 3.5% (22) were people belonging to traditional populations (Table 1).Table 1 presents the results of the binary regression of the associations between sociodemographic characteristics and access status to COVID-19 health care in Pará Province in the Brazilian Amazon region.The results demonstrated that female participants were 1.62 times more likely to access/receive COVID-19 health care than male participants were (p = 0.007).As age increased, the chances of accessing/receiving COVID-19 health care also increased (p = 0.01; OR: 1.02).Variables with p values < 0.20 were selected for multiple regression, including traditional population, educational level, lives in the state capital, individual income, and marital status.

Clinical characteristics
Figure 2 shows the clinical characteristics and COVID-19 infection status of the patients.Regarding the year of first COVID-19 infection, 82% (519) of participants were diagnosed between 2020 and 2021, and 18% (114) of participants were diagnosed between 2022 and 2023.Only five (5) participants did not respond.The first year of COVID-19 infection was not associated with access to COVID-19 health care (p = 0.88; OR: 0.96; 95% CI: 1.13, 1.95).Regarding the presence of any preexisting chronic conditions before COVID-19 infection, among the 598 participants who responded to this inquiry, 86.8% (519) reported of no history of chronic ailments, whereas 13.2% (79) acknowledged of having some form of preexisting disease.Participants with a chronic disease were 2.38 times more likely to access health care than were those without any disease (p = 0.005; 95% CI: 1.30, 4.36).The majority of participants at 86.5% (552) were classified as having mild COVID-19 infection, whereas only 13.5% (86) had severe or moderate infections.Individuals displaying moderate or severe COVID-19 infection had an 11.2-fold greater likelihood of receiving health care than those exhibiting mild symptoms of the disease (p < 0.0001; 95% CI: 4.07, 31.2) (Fig. 2A).
Figure 2B illustrates the number of COVID-19 reinfections based on the utilization of health care.Among individuals who did not access health care (self-care), the mean number of reinfections was 1.29 (SD: 0.66), whereas among participants who received health care, the average was 1.47 (SD: 0.71) reinfections.The regression analysis demonstrated that the likelihood of receiving health care increased according to the number of COVID-19 reinfections (p = 0.004; OR: 1.48; 95% CI: 1.13, 1.95).
Figure 3 shows the association between the use of natural/alternative medications to treat COVID-19 and access to health care.Among these individuals, 631 participants responded to the inquiry regarding the utilization of herbal medicines and homemade tea, and 54.8% (347) chose not to use them, whereas 45.2% (286) reported of using these remedies.Individuals who used homemade tea or herbal remedies (p < 0.0001; OR: 0.54; 95% CI: 0.38, 0.76) were less likely to receive health care.
Figure 4B displays the number of vaccine doses according to access to health care.A total of 615 participants answered the survey, with an average of 3.3 vaccine doses (SD: 0.94).Among those who did not access health care (self-care), the average was 3.18 vaccine doses (SD: 0.92), whereas the average was 3.35 doses (SD: 0.94) among participants who received health care.The regression analysis demonstrated that the likelihood of receiving COVID-19 health care increased with the number of COVID-19 vaccine doses (p = 0.03; OR: 1.22; 95% CI: 1.01, 1.46).

Sociodemographic and clinical characteristics: multiple logistic regression model
In the final model (Table 2), all of the variables that were selected in the previous step were analyzed together.The participants most likely to access health care were those with moderate or severe COVID-19 (p = 0.000; OR: 19.8) and females (p = 0.001; OR: 1.99).Moreover, participants who used homemade tea or herbal medicines were less likely to receive health care for COVID-19 in health services (p = 0.002; OR: 0.54).

Discussion
In this study, the concept of access to health services was used to examine the realized access (effective use of services) 19 and associated factors 19,[21][22] .The results indicated that the individuals most likely to access COVID-19 A high proportion of participants had access to COVID-19 health care.This result may be related to the characteristics of the sample but also to the universal health system in Brazil, which has a large capillarity through the PHC 12 .
This study considered the type of physical access in establishments of public and private health networks at all levels of health care and virtual access.The characteristics of the population are important aspects in studies on access, and such aspects can facilitate or be barriers to access 19 .In this study, the predisposing factors included education, age, ethnicity (traditional population), current job, marital status, and sex.The enabling factors included income, participation in social programs, residence in the capital city, and availability of health services such as vaccines, including doses and COVID-19 diagnosis.Need factors 19 included chronic conditions, the use of alcohol and tobacco, and mild to severe COVID-19.

Sociodemographic characteristics
The state of Pará encompasses several municipalities characterized by the poorest income, employment, and social indicators in Brazil [25][26] , thus leading to a disproportionate impact of COVID-19 on its population, particularly affecting vulnerable people [10][11] .The province of Pará has several cities characterized by the lowest income, employment and social indicators in Brazil [25][26] .These characteristics of the social and health structure are aspects that increase the population's risk for COVID-19 infection and its outcomes, particularly affecting vulnerable individuals [10][11] .
The specific characteristics of these municipalities and their populations played a significant role in both the spread of cases and the accessibility of health services during the pandemic.In these poor areas, residents experienced higher mortality rates from COVID-19.The failure to collect diagnostic samples was 3.07 times more frequent in these locations, and there was a 140% shortage in the availability of computed tomography scans 31 .A study conducted in Brazil highlighted an increased death rate among younger age groups in the most deprived municipalities, especially among individuals under 40-years-old who belonged to indigenous backgrounds.This observation led to the conclusion that levels of deprivation significantly hindered the prompt referral of patients to appropriate care 32 .
In the present study, multiple logistic regression analysis demonstrated that among the sociodemographic variables that were examined, only sex exhibited statistical significance within the final regression model.Notably, despite including other variables such as age, traditional population, educational level, residence in the capital, individual income, and marital status in this analysis, only sex was statistically significant.
Contrary findings have been observed in studies conducted across the Amazon region [9][10][11] .These studies, which were conducted during the initial and subsequent waves in Belém 10 , among the Waraó indigenous community 11 and in the population of Manaus 9 , did not establish a clear association between sex and the incidence of COVID-19.However, in Germany, there was an identified correlation between COVID-19 and male sex, particularly among symptomatic individuals who accessed care at health care facilities 33 .Similarly, in Australia, men display a greater risk of hospitalization than women 34 .In contrast, a study in Jordan reported that the majority of hospitalizations were among women 35 .
In Brazil, a study examining the risk factors associated with hospitalization and mortality due to demographic, clinical, and socioeconomic variables demonstrated that, in general, males exhibited greater odds of death than females did.However, postpartum patients who were admitted to hospital wards were found to have increased odds of mortality 32 .
Access to health care services by women is a facet of health system performance that goes beyond mere availability; it is contingent upon the effective utilization of these services.This access is influenced by various factors, including the societal roles and rights attributed to women, cultural and religious norms, and the structure of health care financing models [36][37] .A specific study identified several contributing factors to the lower access of women to health care services, COVID-19 levels of women's empowerment, financial access, and educational opportunities.This disparity has led to the underreporting of COVID-19 cases and fatalities among women 37 .
In Brazil, the universal model of the health care system, which offers free access to the entire population, serves as a mechanism to alleviate the barriers imposed by the necessity of payment for health care services 12 .Notably, women in this country tend to visit health services more frequently than men, whether for preventative treatments or nonchildbirth-related hospitalizations.Urban areas demonstrate greater coverage by health plans for women, whereas in rural regions, women tend to rely more on the public health system, and men tend to allocate more of their resources to healthcare [38][39] .An understanding of the exacerbation of sex inequalities during pandemics is crucial.Within a pandemic context, among various factors, the inaccessibility of health services can significantly heighten women's vulnerabilities during a crisis [40][41] .Multiple analyses of children with    42 .
The sample had a greater number of participants with a high level of education; specifically, most participants had a lower income, and 35.9% were currently studying.A high rate of access to health services was also found in a study with a sample of participants with high education and income.However, it was observed that a preexisting relationship with a primary care provider was critical to receiving access to a health care provider and medication during the COVID-19 pandemic 21 .
However, vaccination against COVID-19 and the number of doses were not significant in the final regression model.There is a high percentage of vaccinated people.This result may be related to the vaccination strategy that was adopted in the country, which began with priority groups and later expanded to the entire population.In this country, this specific protection measure has universal and free access, which is financed by the government.The history of vaccine acceptance in Brazil and mandatory vaccination for COVID-19 led to 70% coverage in 2021 and approximately 60% coverage in the Northernregion 30 .

Clinical characteristics
In the current study, individuals demonstrating moderate or severe clinical manifestations of COVID-19 were more inclined to access health care.Previous research has indicated that systemic and pulmonary clinical manifestations are linked to hospitalizations 35,43 .
The clinical manifestations of COVID-19 infection are needed.The availability of resources, which represents an enabling factor, is closely related to the need factor 19 .This effect was also observed in a study performed in the United States of America, which demonstrated that demographic factors, such as ethnicity and language, were associated with reduced access to health care, more severe COVID-19 infection on admission and mortality.A high proportion of Hispanic participants who did not have a health record prior to hospitalization were observed compared to non-Hispanics 44 .A previous study demonstrated that among those hospitalized for COVID-19, a lack of health insurance also impacted the use of resources, such as oxygen and physiotherapy, for treatment and care after hospital discharge 45 .
Geographic accessibility also contributes to the utilization of health services.In severe COVID-19 infections, the type of health service and the availability of physical resources for treatment have a direct impact on access 22 .Addressing individuals with severe and moderate clinical manifestations of COVID-19 necessitates adequate infrastructure, essential equipment, supplies, and a competent cadre of health care professionals 35,[43][44][45] .However, within the context of the present study, the northern region had the lowest number of beds per thousand inhabitants in Brazil during the COVID-19 pandemic.Despite this, it experienced the most significant average increase in intensive care unit beds across the country.Among the 27 Brazilian states, Pará ranked sixth for the state with the lowest number of intensive care unit beds and third for other beds, with 0.15 and 1.87 beds per 1,000 inhabitants, respectively.Additionally, it registered the lowest number of nurses per thousand inhabitants (1.03) in Brazil, and the Amazon region experienced the lowest number of medical doctors (2.02 per 1,000 inhabitants) 31 .The distribution of increased resources, such as beds and mechanical ventilators, was unequal in the Brazilian Amazon region and within states, with urban areas and capitals having more abundant access to these resources 5,43,46 .These disparities in health care provision significantly impact access to health care services 36 .
Acute COVID-19 infection, similar to chronic disease, does not depend on continued care over time.It is an acute, episodic infection for which resources are available for immediate treatment [42][43][44][45] .A previous study estimated that 41% of the vulnerable population in 20 cities of Brazil, including Belém, lives farther than 5 km from a health service to admit patients in severe condition due to COVID-19 infection.Health services with intensive care unit beds and ventilators, which are essential for treating severe COVID-19 infections, are more precarious in the peripheral areas of cities 22 .
This study demonstrated that the utilization of teas and herbal medicines was linked to a reduced likelihood of accessing health care services for the treatment of COVID-19.Inhabitants of the Amazon region regularly incorporate homemade teas and herbal remedies derived from local plants into their daily lives.These plants are utilized for various therapeutic purposes, thereby addressing conditions such as microbial infections, gastrointestinal disorders, and inflammation 47 .Similar practices are occurring globally, with populations elsewhere using medicinal plants for disease prevention and increasing consumption postdiagnosis in an effort to alleviate symptoms 48 .An understanding of the active ingredients present in plants that are used for therapeutic purposes is pivotal 49 .In this study, individuals exhibiting severe or moderate clinical manifestations also required and accessed health care within a health service.Therefore, identifying individuals or populations who are most in need of health care services is crucial for assisting in the preparation of health care network management and care protocols.Studies on access to health care have described the care provided by specialist physicians, nurses, general physicians, and health workers.The care provided by traditional healers was not described in these previous articles 20 .

Strengths and limitations
The utilization of the electronic questionnaire may have restricted the involvement of elderly individuals and those with lower levels of education.Furthermore, the nature of this study does not permit the establishment of a causal relationship between the assessed variables.The utilized sampling technique resulted in a sample that did not represent the education level of the population of Pará.However, it is important to know about access to care for COVID-19 infection in this group.

Figure 1 .
Figure 1.The location of the state of Pará © 2023 by Amanda Miranda (software ArcGIS 10.8, https:// www.arcgis.com/ index.html) is licensed under CC BY-ND 4.0.To view a copy of this license, visit.

Figure 2 .
Figure 2. Associations between clinical characteristics, COVID-19 reinfections and access status to COVID-19 health care.Figure 2A-Year of diagnosis, diagnosis of chronic disease and classification of infection*.2B-Number of COVID-19 reinfections (average).Pará.Brazil.2023.*Classification of the most severe COVID-19 infection (Severe: was admitted to the intensive care unit or needed to be intubated/Moderate: had proven pneumonia or was hospitalized or needed oxygen support/Mild: respiratory symptoms, but no pneumonia or shortness of breath).
was followed.The study was approved by the Research Ethics Committee of the Federal University of Paraiba Lauro Wanderley University Hospital under protocol number 5.826.893 and CAAE: 65929522.1.0000.5183.All of the participants signed the Free and Informed Consent Form.The authors did not perform experiments on humans and/or use human tissue samples/human data.The authors did not have direct contact with the study participants because the study questionnaire was administered via the internet, and the data were stored by REDCAP®, which guarantees security in terms of privacy and data storage.
All of the requirements proposed by Resolution 466 of 2012 of the National Health Council of Brazil were followed, as well as all of the principles established in General Personal Data Protection Law No. 13,709 of 2018 concerning personal data processing activities, as established in articles 6 and 7.The Declaration of Helsinki Vol.:(0123456789) Scientific Reports | (2024) 14:8776 | https://doi.org/10.1038/s41598-024-59461-1www.nature.com/scientificreports/

Table 1 .
Associations between sociodemographic characteristics and access status to COVID-19 health care Pará.Brazil.2023.COD crude odds ratio, CI confidence intervals, No Information, Ref. reference, SD standard deviation.*Minimum wage in Brazil in May 2023-R$ 1.320.00(US$ 260,15-quotation for the same period).

Table 2 .
Multiple logistic regression analysis of the associations between social, demographic, and clinical characteristics and access status to COVID-19 health care.Pará.Brazil.2023.AOR adjusted odds ratio, CI confidence intervals, Ref. reference.*Severe(was admitted to the intensive care unit or needed to be intubated), Moderate (had proven pneumonia or was hospitalized or needed oxygen support) and Mild (had respiratory symptoms, but no pneumonia or shortness of breath).COVID-19 infection demonstrated that being under 10 years of age, being a black or mixed race/ethnicity, and having a health condition prior to COVID-19 were associated with a greater likelihood of hospitalization