A prospective, descriptive longitudinal study with an analytical feature was conducted in two high-complexity public hospitals in the city of Recife, Pernambuco, Brazil. Between August 2020 and June 2021, individuals were recruited aged over 18 years, who were treated at outpatient clinics for patients, who have recovered from COVID-19. Admission to the outpatient clinic occurred by referral from the attending physician after hospital discharge, by spontaneous demand or after an invitation by telephone contact from the research team. The study was approved by the institutional Ethics Committee of the Hospital das Clínicas at the Universidade Federal de Pernambuco (CEP-HC-UFPE 46681521.7.0000.8807).

At the first consultation, after signing the informed consent form, participants completed a questionnaire regarding sociodemographic characteristics, symptoms, comorbidities, and the need for hospitalization and were also submitted to peripheral blood collection. Those with no real-time polymerase chair reaction (RT-PCR) results or with a negative RT-PCR result for SARS-CoV-2 were excluded, as were individuals who had been vaccinated for COVID-19.

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All RT-PCR tests for the detection of SARS-CoV-2 RNA, performed with nasopharyngeal swab samples, were analyzed at the Central Laboratory of Pernambuco (LACEN-PE).

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Individuals were divided into two groups: Severe Cases: defined as those who required hospitalization; and Mild Cases: defined as those that did not require hospitalization. The Severe Cases group was further stratified according to oxygen demand: non-invasive oxygen therapy (nasal catheter and non-rebreathing mask) and invasive (invasive mechanical ventilation). The longevity and serum level of antibodies were assessed at three moments in time after the onset of symptoms: up to 90 days, between 91 and 180 days, after 180 days. Of the 238 individuals included in the study, 145 provided a single peripheral blood sample and 93 provided two or more samples.

For measuring the serum concentration of IgG-S1, the EUROIMMUN anti-SARS-CoV-2 ELISA kit (Lubeck, Germany) was used, one of the first diagnostic tests with the EC mark (European Conformity) to be developed, and available worldwide. The principle of this methodology is to quantify specific IgG to protein peak 1 (S1) of SARS-Cov-2 through an immunoenzymatic assay, where the results are presented in absorbance (optical density). This kit demonstrated a cumulative sensitivity of 82.6% for the detection of IgG in samples collected after 14 days of RT-PCR and a specificity of 86.9% [17]. To perform the test, the manufacturer’s instructions were followed. The semi-quantitative test of the results was through the ratio between the absorbance level of the patient’s sample by the absorbance level of the calibrator (Ratio). Ratio results < 0.8 were negative, ≥ 1.1 positive, and ≥ 0.8 and < 1.1 were indeterminate for the presence of IgG-S1.

Statistical analysis

For the statistical analysis, SPSS 13 (Statistical Package for the Social Sciences) for Windows was used. The chi-squared test and the Kruskal-Wallis rank sum test were conducted to identify significant differences in the categorical variables between the groups. The Mann-Whitney test was used to compare quantitative data between the groups. All tests were two-tailed with a level of 0.05. Missing data were excluded for analysis. The odds ratio (OR) with a confidence interval was calculated.

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The variables included in the univariate analysis were as follows: hospitalization, sex, age, arterial hypertension, type 2 diabetes mellitus (T2DM), obesity, IgG-S1 antibody titers up to 90 days, between 91-180, and after 180 days. Variables that attained a level of p < 0.2 in the univariate analysis were entered in a linear regression model using the Enter method.

A quality control of the models was performed: the assumption of linearity and the quality of variance of the dependent variable across the range of values of the independent variable were assessed with scatterplots, and the assumption that the dependent variable is normally distributed was assessed with a normal probability plot (data not shown).

The researchers were not blinded when recruiting participants nor when they assessed the results. However, the tests for detecting IgG-S1 were completely blind, since identifying the biological samples did not define the stratification of the groups. Only the final analysis of the data revealed an overview of the results. Potential confounders were identified and controlled in the data analysis.

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