Factors associated with the SARS-CoV-2 infection among health professionals from university hospitals

Objective: to investigate factors associated with the SARS-CoV-2 infection among health professionals from university hospitals. Method: a multicenter, mixed approach study with concomitant incorporated strategy, carried out with 559 professionals in the quantitative stage, and 599 in the qualitative stage. Four data collection instruments were used, applied by means of an electronic form. The quantitative analysis was performed with descriptive and inferential statistics and the qualitative data were processed by means of content analysis. Results: the factors associated with the infection were as follows: performance of the RT-PCR test (p<0.001) and units offering care to COVID-19 patients (p=0.028). Having symptoms increased 5.63 times the prevalence of infection and adhering to social distancing most of the time in private life reduced it by 53.9%. The qualitative data evidenced difficulties faced by the professionals: scarcity and low quality of Personal Protective Equipment, work overload, physical distancing at work, inadequate processes and routines and lack of a mass screening and testing policy. Conclusion: the factors associated with the SARS-CoV-2 infection among health professionals were mostly related to occupational issues.


Introduction
With slightly more than two years of pandemic, the World Health Organization (WHO) confirmed the milestone of 500 million cases of the disease by the SARS-CoV-2 virus (COVID-19) and more than six million deaths, worldwide (1) . Throughout this time, Brazil presented heterogeneous situations in relation to the SARS-CoV-2 infection, with disease acceleration and de-acceleration periods in the most diverse states and municipalities.
In August 2022, it was the second country with the highest number of deaths recorded, totaling nearly 680,000, only behind the United States (1) .
In this health crisis context, the health systems played a fundamental role and health professionals faced extremely challenging work environments. Despite the strong feeling of ethical duty to work, health professionals endured concerns related to their own safety (2)(3) .
Occupational exposure is an important form of SARS-CoV-2 transmission and the hospital environment is considered as with high risk for contamination due to the hospitalization of patients infected with SARS-CoV-2, whether symptomatic or not (4) . Control over spread of the virus among health professionals became fundamental, both because of the potential for lives lost and because of the sustainability of the health systems that, to a large extent, depend on the health of these workers. In addition to that, infected health professionals can become transmission vectors to other peers and to susceptible patients (5) .
From the beginning of the pandemic, the main protection measures recommended by the WHO involved hygiene care and social distancing, which started to be recommended at the global level. In relation to the health services, the use of standard precautions (SPs) stands out, which are measures that should be resorted to in the care provided to all patients, regardless of their diagnosis.
SPs are measures historically adopted for the protection of health professionals against biological risk. During the pandemic, they were widely fostered as a strategy to prevent patient-professional transmission. Studies that analyzed the behavior of SARS-CoV-2 transmission in China at the beginning of the pandemic suggest that the adoption of protective measures combined with training and workload adequacy are effective in controlling SARS-CoV-2 transmission among health professionals (4) .
It is believed that researching factors associated with the SARS-CoV-2 infection among health professional is important to understand the impact of the disease on this population group. In addition to that, the identification of difficulties faced during this period can assist in devising future strategies to mitigate illness and death among health professionals in periods of similar health crises. The hypothesis according to this test is that unfavorable working conditions and protection measures are associated with SARS-CoV-2 infection among physicians and Nursing professionals.
Given the above, the following questions emerge: (1) Which are the factors associated with the SARS-CoV-2 infection among physicians and Nursing professionals from university hospitals? (2) Which were the difficulties found in relation to the protective measures during the COVID-19 pandemic in university hospitals?
The main objective of the current study was the following: To investigate factors associated with the SARS-CoV-2 infection among health professionals from university hospitals. And, as secondary objectives, it sought to: assess adherence to the standard precautions and identify difficulties found in terms of the protective measures by health professionals during the pandemic.

Study design
A multicenter study with a mixed approach and a concomitant QUANT (qual) incorporated strategy, conducted between September 2020 and October 2021. With this research strategy, it was sought to obtain analysis perspectives of the different types of data, contemplating the study objectives, considering the quantitative study as the main database of the research and the qualitative stage with secondary weight.
In order to ensure methodological rigor of the study, the Mixed Methods Appraisal Tool (MMAT) (6) was used and the internationally recognized Standards for Quality Improvement Reporting Excellence (SQUIRE) guide was followed to prepare the manuscript.

Setting
The scenario was comprised by five large-size university hospitals (with 151 to 500 beds), all reference for the treatment of COVID-19, located in the Brazilian South region, in the states of Rio Grande do Sul-RS, Santa

Population
There were 19,491 health professionals (physicians, nurses, nursing technicians and assistants) working in these hospitals when data collection was initiated.
criteria were informed to the participants when they were invited to take part in the research.

Definition of the sample
Convenience sampling was used to select the participants. All the workers with an email address registered at their institution were invited to take part in the study. Those who voluntarily agreed to fill in the data collection instruments comprised the final sample, totaling 559 professionals in the quantitative stage.
The sample of the qualitative stage was comprised by the physicians and health professionals who took part in the quantitative stage and answered the open questions included in the instrument (n=546). Health professionals working as managers or in infection control, workers' health and permanent education services were also included, totaling 599 professionals. Thus, the qualitative data sample was closed due to saturation (7) ; in other words, all the participants who answered the open questions were included in the study.

Data collection
Data col l ecti on took pl ace onl i ne from

Instruments used to collect the information
The data were collected by means of four instruments. The first contained sociodemographic data Brazil (8) . The scale is of the Likert type, its score varies from 1 (Always) to 5 (Never), its items are added up and a mean value is calculated, in order to provide a final score that varies between 1 and 5. The higher the pandemic. After this review, the instrument was sent to the study participants.

Study variables
The dependent variable of this study was SARS-

Data treatment and analysis
The quantitative data were organized in an electronic spreadsheet in the form of a database, using  The variables with significance values below 0.20 were included in the multiple model and a 5% significance level was adopted to maintain them in the final model, with "backward" selection of the variables.
The qualitative data were submitted to content analysis (9) . The following stages were performed: 1) pre-analysis: organization of the dataset to be analyzed in order to render the initial ideas operational and systematize them; 2) exploration of the material: from the in-depth reading of the analysis material, seeking to establish categories and/or subcategories and 3) treatment of the results: it took place when the categories were worked on based on the authors of the literature review, adding to data interpretation by the researchers (9) . The MAXQDA ® software was used to assist in data organization, categorization and analysis.
To ensure reliability of the qualitative data analysis, periodic meetings were held between the research team and members of the research group not involved in the survey to present the synthesis of the main findings obtained and discuss analytical possibilities. Through this discussion of peer analyses, it was possible to ensure consistency between the empirical data and the interpretations that were being constructed in the light of the researchers' subjectivity and relevance for the research question and objectives (9) .
Integration of the quantitative and qualitative data aimed at complementarity of all the information, seeking explanations for the quantitative findings based on the analysis of the qualitative data. The interpretation stage was conducted by means of incorporation, after separately analyzing each of the data sources. The integration obtained was represented by means of an illustrative joint exposition diagram (10) . were identified by codes consisting in the letters "B", "Ph", "NT", "NA" and "M" for nurses, physicians, nursing technicians, nursing assistants and managers and professionals from the infection control, workers' health and permanent education services, followed by numbers associated with the order in which the questionnaire was received. Table 1 shows the characterization of the participants in each of the study stages, verifying certain predominance of professionals belonging to the female gender and with a partner. In relation to work, most of the participants were Nursing professionals and had their employment contracts ruled by the Consolidation of Labor Laws (Consolidação das Leis do Trabalho, CLT).     RT-PCR = Reverse Transcriptase Polymerase Chain Reaction; † † PRA = Adjusted Prevalence Ratio = "SARS-CoV-2 Infection" + "Institution" + "Employment contract" + "Direct assistance to suspected or confirmed patient" + "Type of test" + "The service treats COVID-19 patients" + "Symptoms suggestive of COVID-19" + "Social distancing in the private life activities" The qualitative data contributed important subsidies to deepen understanding of these phenomena, as some difficulties faced for the protection of health professionals during the pandemic were identified in these hospitals. In item 2, "Work process, organization and routines", frequent changes and non-uniformity in the guidelines were some of the difficulties identified. "Distancing in the work environment" was the third item and evidenced the obstacles to implement distancing in the hospitals.

Results
The fourth item, "Work overload", shows conditions that led to an increase in the health professionals' workload during the pandemic. In item 5, "Screening and testing policy", some failures in relation to the screening of patients and professionals were evidenced in the institutions, in addition to difficulties in terms of COVID-19 testing. Figure 1 presents the participants' testimonies representing each item that comprises the qualitative results.

Difficulty identified Use of Personal Protective Equipment
Shortage and low quality of the equipment

Leaves and insufficient staffing
Our greatest difficulty was the number of employees, due to leaves related to COVID-19. Temporary selection processes were opened and not enough people were hired to meet the need. This generated a tight schedule, work overload, stress and, consequently, problems in interpersonal relationships. (M41, Hospital B)

Difficulty identified Screening and testing policy
Screening and testing of the professionals    (11) .

The number of colleagues (from all sectors) who come to work with COVID-19 symptoms is shocking. I suggest a daily
In the state of Ceará, a study conducted only with nurses identified 25% prevalence of COVID-19.
In this same study, hospital nurses were 1.66 times more likely to have the infection than their Primary Care counterparts (12) .
In 13 European countries, the prevalence of SARS-

CoV-2 among health professionals, between February and
August 2020, showed strong heterogeneity with rates varying from 0.7% to 45.3% (13) . Hospitals in Wuhan, China, reported infection rates of 3.5% to 29% among health workers at the beginning of the disease outbreak, when the protective measures were still inconsistent (14) .
It was identified that Nursing professionals had more positive SARS-CoV-2 cases when compared to physicians.  (15) .

Studies conducted in several countries have shown
that Nursing professionals were the most infected (16)(17) .
Among the possible reasons for the high number of contaminated Nursing professionals, closer and longer contact with patients stands out, involving activities performed at the bedside such as drug administration and also the performance of higher risk procedures, such as aspiration of tracheal secretions, in addition to being the first response line in case of complications in the patients (16) .
It was also observed that the type of test associated with the infections was RT-PCR. The RT-PCR method (which detects the virus) has been approved by the WHO as the "gold standard" for diagnosis and detection of the disease. However, immune response tests are also important for determining protective immunity in several infected population categories (11) .
As for the symptoms, it was verified that most of the professionals (86%) who tested positive were symptomatic and having symptoms increased the prevalence of positive cases by 5.63 times. Even so, it is necessary to consider that 14% of the infection cases in this research were asymptomatic. In an analysis based on 15 studies, the researchers identified 40% pooled prevalence of health professionals infected by COVID-19, diagnosed with RT-PCR, who had no symptoms at the time of diagnosis (16) .
Although asymptomatic transmission is still controversial, the potential for silent transmission is still an issue that needs to be addressed efficiently.
Although a higher infection rate was not identified in professionals who worked in the exclusive areas for coping with COVID-19, those who tested positive for SARS-CoV-2 were active in units that offered care for cases of COVID-19 positive patients. This suggests that professionals in areas not exclusive to COVID-19 were also exposed to the infection and at greater risk due to the lower availability of Personal Protective Equipment (PPE) in these loci or to the lower adherence to use of these items and other protective measures. This hypothesis is corroborated by a systematic review of 46 studies which showed that most of the professionals positive for SARS-CoV-2, using RT-PCR, worked in hospital wards, followed by operating rooms and surgical services (16) .
A study carried out at a university hospital in Verona, Italy, identified that almost two-thirds of the health professionals with anti-SARS-CoV-2 seroprevalence were workers with a history of previous close contact with a COVID-19 case, in the hospital (18) .
In identified with this condition (16) .
In the current study, the difficulty maintaining distancing between professionals in the work environment during the pandemic was one of the main obstacles to protection pointed out by the managers, which may play an important role in transmission of the virus among these individuals. The professionals' co-living environments, such as cafeterias and rest areas were perceived as the most critical for virus transmission, partly due to relaxation of the protective measures in these places, but also due to the small physical space that favors crowding.
A number of authors point out that awareness raising strategies for changing routines and habits are highly relevant, even during meals and group meetings (4) .
In addition to that, the importance of distancing in potentially neglected situations, such as in elevators, public transportation means (buses or vans) and clinical meetings, need to be considered (19) . In university hospitals, maintaining this distancing can be especially challenging,  (20) .  (5) .
This study identified that work overload is one of the difficulties for the professionals' safety. During a pandemic, it is common for health professionals to work for many hours, without breaks and under significant pressure, increasing occupational exposure to the infectious agent and exposing workers to diseases and accidents. Thus, it is essential that the professionals have adequate and sufficient rest time to recover from physical and psychological wear out (5) .
In the participants' reports, it was identified that  (19) .
Other strategies that are considered important to control transmission in the hospital environment include the following: isolating cases of symptomatic professionals, testing them frequently, clear and easy communication, and simple and accessible protocols (4) .
In Italy, a country heavily affected by the pandemic, Physicians recommended screening health professionals at the beginning of the work shift and rapid testing of all those that presented any symptoms suggestive of the disease (even if mild or without fever) and also for contacts of suspected or confirmed cases (22) .

Testing of health professionals in pandemic situations
is an important tool for health care maintenance, as it provides early symptomatic treatment, enabling a shorter return to work, reducing absenteeism (23) . In this sense, the Brazilian Ministry of Health recommended that health services implement non-punitive policies, allowing professionals with respiratory infection symptoms to be distanced from work to undergo home isolation (21) , a measure that was adopted by the institutions that participated in this research.
The WHO recommended testing all health workers, even without symptoms, as one of the strategies to contain infection among such workers (24) . However, it was observed that a high percentage (21.8%) of the professionals who participated in the study had not been tested and/or were awaiting their results.
Problems in screening and performing tests among patients and professionals were also verified in a research study that sought to analyze the work environment of nurses from Brazilian university hospitals (25) . A study carried out at the national level between April and June 2020 identified that only 27% of the health professionals had undergone some type of testing for COVID-19 (23) .
This situation probably resulted from the operational limitations related to the supply of tests, considering the global shortage of inputs during a given period Rev. Latino-Am. Enfermagem 2023;31:e3918.
of the pandemic and due to slowness in processing the analyses (5) . In this sense, the difficulty of testing, especially in groups more vulnerable to infection, such as health professionals, constituted a significant barrier that prevented dimensioning the actual magnitude of the pandemic.
As limitations of this study, we can point to its crosssectional design, which makes it difficult to establish cause and effect relationships. In addition to that, the long data collection period can also be considered a limitation, especially given the rapid changes in the epidemiological scenario, in addition to the vaccination that was initiated during the study.