An institutional COVID-19 initiative: creation of a biobank and serological data analysis in pre- and post-vaccination cohorts

Abstract

The COVID-19 pandemic has left a legacy in the management of health emergencies, but sentinel surveillance was relatively underused, despite its significant role in decision-making during epidemics. Here we describe a sentinel surveillance for anti-SARS-CoV-2 serology carried out on a cohort of 395 individuals at a Brazilian institution, from October 2020 to December 2022. A total of 1,507 serum samples were analyzed for IgG and IgA against SARS-CoV-2 Spike (S) or nucleocapsid (N) proteins, in the pre- and post-vaccination periods. The latter included two doses of CoronaVac (group 1, G1), or ChAdOx-1 or BNT162b2 (group 2, G2), followed by heterologous booster doses. In the pre-vaccination phase, 26.5% of the participants showed IgG reactivity for S and 13.7% for N. After the vaccines’ first dose, S IgG response was positive in 66.6% or 98% of G1 or G2 participants, respectively, whereas 100% of the participants showed S IgG positivity after the second dose, and S IgG and IgA after the booster. This initiative enabled the examination of viral transmission beyond hospital environments, which has rarely been explored, and established protocols for managing future emergencies. In addition, a serum bank and a comprehensive database are now available to the scientific community.

Key words
bank of sera; COVID-19; retrospective observational cohort study; serological surveillance

INTRODUCTION

In December 2019, the world faced the biggest health challenge of the last 100 years: the COVID-19 pandemic caused by the new coronavirus SARS-CoV-2 (Tan et al. 2020). Since its onset, 775 million cases and more than 7,000,000 deaths have been reported worldwide (WHO 2024). Vaccines against COVID-19 were rapidly developed and vaccination began one year after the description of the first cases of the disease (WHO 2024). Although mass vaccination is the most effective way to control the disease (Fiolet et al. 2022), mitigation policies, such as social distancing, masks usage, hygiene practices, and extensive testing, were enormously important, mainly until high immunization percentages were reached (Güner et al. 2020). Moreover, the need to manage an emerging pandemic that rapidly assumed global proportions required that many measures adopted in other health emergencies, such as influenza outbreaks, were employed (Marcenac et al. 2022).

Sentinel surveillance is a widely used strategy to deal with influenza outbreaks. This strategy is characterized by testing volunteer people across a given community, including those who did not present any disease symptoms, and without necessarily searching for a diagnosis. Its main goal is to discover unseen disease transmission. Although this approach has not been widely used during the COVID-19 pandemic, some sentinel studies carried out in different countries have generated robust epidemiological results that were very useful for decision-making (Vega-Alonso et al. 2023, Cooksey et al. 2022, Miyadahira et al. 2023). In Brazil, for instance, genomic surveillance identified that transition from Delta to the Omicron SARS-CoV-2 variants was faster in healthcare professionals than in other groups of the population (Padilha et al. 2023), while a serosurveillance in low-resource communities in Rio de Janeiro city revealed a seroprevalence much higher than expected in those populations (Brasil et al. 2022, Coelho et al. 2022)

The results obtained from sentinel surveillance become even more significant when there is some difficulty in implementing mitigation strategies, as occurs with workers in essential services who were unable to interrupt their activities during the first months of pandemic, a period characterized by few information and lack of mass diagnosis. Although nowadays the pandemic scenario is different, with more than half of the world’s population vaccinated (WHO 2024), we must consider that the different initiatives that took place during pandemics also provide valuable learning experience for addressing future emergencies.

In this perspective, our group at the Instituto de Bioquímica Médica Leopoldo de Meis of the Universidade Federal do Rio de Janeiro (IBqM, UFRJ) developed an in-house serological test (ELISA) that detects antibodies elicited by SARS-CoV-2 antigens (Fernandes-Siqueira et al. 2022a) to promote serosurveillance of our community. Here, we report a retrospective serological follow-up of a cohort of workers and students from IBqM, UFRJ, spanning the period before the introduction of vaccination in Brazil as well as after the participants undergo different vaccination regimens, namely two doses of CoronaVac, ChAdOx-1 or BNT162b2 as the initial vaccination protocol, followed by heterologous booster doses with ChAdOx-1 or BNT162b2.

MATERIALS AND METHODS

This work consists of a retrospective observational cohort study approved by the local ethics committee (CEP approvals HUCFF/UFRJ – Hospital Universitário Clementino Fraga Filho/ Universidade Federal do Rio de Janeiro nº 35.303.120.5.0000.5257). All the participants had access to the informed consent form.

Study design

The cohort of this study consisted of 395 participants, members of IBqM, UFRJ, Brazil, whose serum samples were evaluated to detect antibodies against the spike (S) and nucleocapsid (N) proteins of SARS-CoV-2. The IBqM community was invited by email to participate in the study. All those over 18 years of age who accepted the invitation were selected to participate in the study, without exclusion criteria. On the day of the blood collection, they completed an identification form providing information on personal and clinical data. During the 27 months of monitoring (from October 2020 to December 2022), the participants were contacted via a messaging app to schedule blood collection. They had access to their serology results by email. In total, we analyzed 1,507 serum samples from two phases of the pandemic: the pre- and post-vaccination periods.

A total of 242 participants underwent blood collections during the pre-vaccination phase of the study, between October 2020 and April 2021. All these participants had at least one blood sample taken, with a second sample taken for those who tested negative in the first sample, for a total of 313 samples collected over the whole period. Importantly, although COVID-19 vaccination in Brazil started on January 17, 2021, vaccine application prioritized the population groups that were more exposed to infection or presented a higher risk of severe disease (healthcare and essential workers, homeless and indigenous people, and elderly people and people with chronic health conditions), being extended to the entire population according to the decrease in age (Santos et al. 2023). As few individuals in our cohort were included in the priority groups, 63% of the study participants received the first dose of the vaccine only in April 2021.

During the period between January 2021 and December 2022, 118 participants of the previous group plus 104 new volunteers (total of 222 subjects) participated in the serological monitoring after receiving CoronaVac, ChAdOx-1 or BNT162b2 vaccines against SARS-CoV-2. The general scheme of blood collections in this study phase is presented in Figure 1. All the participants underwent blood collection 15 to 30 days before receiving the first dose of the vaccine (D1). Post-vaccination collections were divided according to the immunization protocols adopted by the Brazilian Ministry of Health for each vaccine. Blood samples from the CoronaVac group (G1) were collected 20 days after D1, and 20, 60 and 90 days after the second dose (D2). Since the immunization protocol for ChAdOx-1 and BNT162b2 recommended 12 weeks between D1 and D2 (Ministério da Saúde, Brazil 2024), two blood samples were collected from G2 participants after D1: one between 20 and 45 days and another between 80 and 90 days after D1. The third G2 blood sample was collected 15 to 45 days after D2. Both G1 and G2 participants underwent the following additional collections: 6 months after receiving D1; 20 days and 3 months after receiving the first booster dose (D3); and 20 days after receiving the second booster dose (D4). Therefore, participants vaccinated with CoronaVac underwent a maximum of 8 blood collections, and those who received ChAdOx-1 or BNT162b2 underwent a maximum of 7 blood collections (Fig. 1).

Figure 1
Scheme of blood collection during the post-vaccination period. Schematic representation of blood collections for serological monitoring of participants who received CoronaVac (upper panel), or ChAdOx-1 or BNT162b2 (lower panel).

Serological analysis (ELISA)

The serological analyses carried out throughout this work were performed using an in-house ELISA previously established by our group (Fernandes-Siqueira et al. 2022a). In this assay, we quantified IgG and IgA antibodies against the SARS-CoV-2 trimeric Spike (S) and the N-terminal domain of the nucleocapsid (N) proteins. Briefly, 96-well plates were previously coated overnight at 4°C, with each of the antigens diluted in PBS (50 μL of a 4 μg/mL solution). After 1 h blocking with 3% BSA in PBS-T, the serum samples, diluted 1:50 in 1% BSA solution in PBS-T, were added to each well and incubated for 2 h, followed by the addition of the detection antibodies (anti-IgG or anti-IgA). The reactivity was quantified spectrophotometrically at 450 nm after the addition of the chromogenic substrate (3,3’,5,5’-tetramethylbenzidine dihydrochloride, TMB). The cutoff for each analysis was calculated as the mean ± 3 SD of the absorbance values of 42 pre-pandemic serum samples.

RESULTS

The cohort demographic characteristics are presented in Table I. The participants’ median age was 36.5 years old (IQR 27-48), 68% (n=269) of them were women and 32% (n=126) were men. The ethnic-racial self-declaration revealed that most individuals consider themselves as “white” (71.6%; n=282), followed by “brown” (20.6%; n=82). Only 6.5% (n=24) self-declared as “black”, 1% (n=4) as “Asian” and 0.25% (1) as “indigenous”. The analysis of participants’ self-reported ABO blood types showed that the predominant blood group in our cohort was type O (40%, n=158), followed by A (35.4%, n=140). The B type is less predominant (10.8%, n=21) and the AB type is the rarest (2.5%, n=10). The blood type distribution in the cohort agreed with that reported in Brazil (World Population Review 2024). Curiously, 11.1% (n=44) of the participants were either unaware of or chose not to disclose their blood type. A total of 80 participants (20.5%) reported one or more comorbidities, with hypertension being the most prevalent (n=42). Among the participants who reported this comorbidity, 47.6% (n=20) were over 60 years, 30.9% (n=13) were between 40 and 59 years, and 21.4% (n=9) were under 40 years (not shown). The second most common comorbidity was lung diseases (23.7%; n=19), the majority of which being asthma (n=15) (not shown).

Table I
Subject demographics and clinical characteristics.

Characteristics
Age, average (IQR)		36.5 (27-48)
Sex, % (n)	Female	68 (269)
	Male	32 (126)
Ethnic-racial identification, % (n)	White	71.6 (282)
	Brown	20.6 (82)
	Black	6.5 (24)
	Asian	1 (4)
	Indigenous	0.25 (1)
ABO blood type, % (n)	O	40 (158)
	A	35.4 (140)
	B	10.8 (43)
	AB	2.5 (10)
	ND	11.1(44)
Comorbidities, %	Hypertension	10.6 (42)
	Lung diseases	7.3 (29)
	Diabetes mellitus	3.7 (15)
	Autoimmune disease	3.7 (15)
	Obesity	1.2 (5)
	Heart disease	1.2 (5)
	Immunosuppressed	1 (4)
	Other comorbidities	3.2 (13)

• IQR: interquartile range.

Pre-vaccination cohort analysis

Using an in-house ELISA developed by our group (Fernandes-Siqueira et al. 2022a) we evaluated IgG and IgA responses against SARS-CoV-2 S and N proteins in blood samples collected during the pre-vaccination phase of the study (October 2020 and April 2021, n=242 subjects and 313 samples). Figure 2A shows serum IgG or IgA reactivity against S or N proteins for each individual, with the data organized from the highest to the lowest IgG reactivity against S protein. Analyses of immunoglobulin reactivity in the complete pre-vaccination cohort revealed 26.5% positivity for S IgG, 16% for S IgA, 13.7% for N IgG and 5.1% for N IgA. The time course of seroconversion that the number of individuals testing positive reached the highest value of the pre-vaccination period between December 2020 and February 2021 (72 participants; Fig. 2b). This seroconversion profile agrees with that of COVID-19 case notifications in the whole Rio de Janeiro State (Secretaria de Saúde do Estado do Rio de Janeiro 2024), which show a pronounced increase between November 2020 and January 2021 (Fig. 2b). The shift of about one month observed between the two curves is explained by the fact that the data generated by the Rio de Janeiro’s health secretariat resulted from molecular tests at the onset of symptoms, while participants in our cohort attended blood collection 15 to 30 days after the onset of symptoms.

Figure 2
Serological panel and symptomatology of the cohort participants in the pre-vaccination period. a) Heatmap representing serum IgG or IgA reactivity against S or N, detected using an in-house ELISA (Fernandes-Siqueira et al. 2022a), in blood samples collected between October 2020 and April 2021. The grayscale used in the heatmap represents the optical density (OD) values obtained in the test, with the highest values represented in black, and the values similar to those obtained for the pre-pandemic sera represented in white. The results are organized from the highest to the lowest IgG reactivity against S protein. b) Comparison between the percentage of reactive tests for S IgG in our cohort (green) and the number of confirmed COVID-19 cases in the State of Rio de Janeiro (blue) between October 2020 and April 2021. Data provided by the Secretaria de Saúde do Estado do Rio de Janeiro (2024). c) Participants’ grouping according to symptomatology: no flu-like symptoms and no diagnosis (blue); flu-like symptoms without diagnosis (green); flu-like symptoms with a previous diagnosis of SARS-CoV-2 infection (light blue); and asymptomatic with a previous diagnosis of SARS-CoV-2 infection (gray). d) Participants’ S IgG positivity according to symptomatology and SARS-CoV-2 infection diagnosis. e) Positivity for S IgA, N IgG and N IgA among asymptomatic or symptomatic participants who were positive for S IgG. f) Symptoms declared by the participants showing: molecular diagnosis (PCR+) for SARS-CoV-2 (blue); detection of S IgG by serology (green); or negative result for S IgG (gray).

Data from the identification form filled out by the pre-vaccination cohort participants revealed that 8,6% had flu-like symptoms and a molecular (PCR) or serological diagnosis for SARS-CoV-2; 34.2% had flu-like symptoms without a diagnosis; 55.7% did not have any flu-like symptoms; and 1.2%, although asymptomatic, were PCR- or serology-positive for SARS-CoV-2 (Fig. 2c). When we correlated the individuals’ clinical status with S IgG reactivity, we found that 100% of the participants who had a positive diagnosis of SARS-CoV-2 infection, as well as 38.8% of the symptomatic participants without a diagnosis, were positive for S IgG in our test (Fig. 2d). Interestingly, 11.1% of the asymptomatic participants were also positive for S IgG, reinforcing the importance of sentinel surveillance in mitigation policies. Among the asymptomatic participants who tested positive for S IgG, 62.9% also showed IgA reactivity against S, but only 22.2% were positive for N IgG and 11.1% for N IgA, while for symptomatic individuals who tested positive for S IgG, the rates of positivity for S IgA, N IgG and N IgA were 63.4%, 48.7% and 21.9% respectively (Fig. 2e). The double increase in N IgG and IgA could be linked to the onset of symptoms, but further investigation is needed to establish a direct link. Figure 2F shows the main symptoms reported by the symptomatic participants. In agreement with other reports in the literature (Pierron et al. 2020, Reses et al. 2021), anosmia and ageusia were the symptoms most frequently reported by the participants either previously diagnosed with SARS-CoV-2 infection or presenting positive serology in our test.

Post-vaccination cohort analyses

Between January 2021 and December 2022, a total of 222 subjects participated in the serological monitoring after receiving the CoronaVac (n=58) (group 1, G1), or ChAdOx-1 (n=145) or BNT162b2 (n=19) (group 2, G2) vaccines against SARS-CoV-2 (Fig. 3a). The Brazilian vaccination program started with CoronaVac and ChAdOx-1, followed by BNT162b2 and finally Ad26.COV2.S (Ministério da Saúde, Brazil 2024). In the first months of the vaccination campaign, CoronaVac corresponded to the majority of the doses administered, explaining why most of the individuals in our population received this vaccine from January to March (Fig. 3b). The rapid engagement of Bio-Manguinhos/Fiocruz Immunobiological Technology Institute in the entire production of ChAdOx1 enabled the distribution of this vaccine in Brazil to be largely expanded (Medeiros et al. 2022), explaining the predominance of ChAdOx1 among the vaccines received by our population after March (Fig. 3b). Finally, BNT162b2 was added to the vaccination campaign only at the end of April 2021, resulting in the administration of this vaccine to some participants after May 2021 (Fig. 3b). When asked about the adverse effects they experienced after receiving the vaccines, approximately 70% of the participants who received either the CoronaVac or BNT162b2 vaccines reported no adverse effects following either D1 or D2, whereas among the individuals who received the ChAdOx-1 vaccine, 59.1% (n=68) declared adverse effects from 24 to 48 hours after the first dose, and 26.9% (n=31) after the second dose (Fig. 3c). Moreover, 20.8% (n=20) of these participants experienced more prolonged adverse effects beyond 48 hours following the first dose of the ChAdOx-1 vaccine. Among the effects, nausea, fatigue, chills, and fever were the most commonly reported (Fig. 3d).

Figure 3
Monitoring of cohort participants in the post-vaccination period. a) Participants’ grouping according to the vaccine protocol received (first and second doses): CoronaVac (green); ChAdOx-1 (blue); or BNT162b2 (light blue); b) Vaccine type received as the first dose each month. c) Occurrence of adverse effects declared by the participants after receiving the vaccines. d) Symptoms declared by the participants after receiving the vaccines. e, f) Heatmaps representing serum IgG or IgA reactivity against S or N proteins, detected using an in-house ELISA (Fernandes-Siqueira et al. 2022a) in blood samples serially collected (as shown in Fig. 1) between January 2020 and December 2022. The grayscale used in the heatmaps represents the optical density (OD) values obtained in the test, with the highest values represented in black, and the values similar to those obtained for the pre-pandemic serum samples, represented in white. The results are organized in ascending order of the S IgG OD value (see bars shown on the left). The heatmaps are grouped according to the vaccines received: e) CoronaVac; and f) ChAdOx-1 or BNT162b2.

The seroconversion follow-up after the participants underwent different vaccination regimens is represented as heatmaps in which each horizontal line corresponds to the results obtained for one of the cohort individuals over time (Figs 3e, f). In these figures, it is possible to identify the moment in which a given participant became positive for IgG or IgA antibodies against each of the tested antigens, as well as to correlate the four variables measured (IgG or IgA against S or N protein) simultaneously in the same individual. Before starting the post-vaccination follow-up, all the participants underwent a blood collection to verify the presence of antibodies against S and N proteins. We observed IgG reactivity to S in 20% of the G1 participants (Fig. 3e, first panel at the left) and 25% of the G2 the participants (Fig. 3f, first panel at the left), indicating that these individuals had previously been infected with SARS-CoV-2. After the first dose of the vaccines (D1), S IgG was detected in 66.6% of the G1 and 98% of G2 participants. On the other hand, S IgA was detected in only 4% or 6.9% of the G1 or G2 participants, respectively. After the second dose of the vaccines (D2), the percentage of S IgG detected increased to 100% in both groups, whereas S IgA appeared in 66% of the G1 and 96.9% of the G2 participants. Six months after receiving D1, S IgG levels decreased to 87.5% in G1 participants, whereas IgG reactivity to S was maintained at 100% in G2 individuals (Figs. 3e-f).

Previous studies have shown that immunization with the three vaccines used in this work, including CoronaVac, which uses the whole inactivated virus, does not elicit a significant serological response against the N protein (Bochnia-Bueno et al. 2022, Huergo et al. 2022). Therefore, the detection of N IgG in the population analyzed in the vaccination cohort may be an indicative of new cases of COVID-19 during the vaccination period. Before vaccination, 17.2% of the G1 participants and 11.6% of the G2 participants presented N IgG, while six months later, the percentage of N IgG positivity increased to 20% and 15.2% in G1 and G2, respectively. This suggests a low incidence of infection among vaccinated individuals, as the increase in N IgG positivity over time may be attributed to new cases rather than vaccine induced responses.

All participants who participated in post-vaccination monitoring in this study received the heterologous first booster dose (D3), following the immunization protocol adopted by the Brazilian Ministry of Health. This protocol involved individuals vaccinated with CoronaVac receiving either ChAdOx-1 or BNT162b2 vaccines, with those vaccinated with ChAdOx-1 receiving BNT162b2, and those vaccinated with BNT162b2 receiving ChAdOx-1. The booster dose was very effective in inducing the humoral immune response, with 100% of participants in both groups testing positive for S IgG and IgA. This high percentage was maintained for up to three months after D3 and after receiving the second booster dose (D4). Although these high levels of antibodies against SARS-CoV-2 attest that the booster dose promoted a very effective immunization, increased rates of N IgG were observed after D3 and D4 (66.6% and 76.4% in G1, and 51.4% and 62.9% in G2), suggesting an increase in COVID-19 cases during this period. However, none of those vaccinated participants declared severe disease symptoms, in agreement with several reports in the literature showing the reduction of disease severity in infection cases after vaccination (Antonelli et al. 2022, Tran et al. 2023, Malden et al. 2024).

DISCUSSION

Viral elimination and mitigation policies during the first year of the COVID-19 pandemic were the most important strategies for controlling the disease (Oliu-Barton et al. 2021). Although the presence of antibodies against SARS-CoV-2 in the pre-vaccination period did not assure protection to justify the relaxation of quarantine or social distancing measures (West et al. 2021), the rapid implementation of serological tests is an important tool for the surveillance of viral spread and for the management of health emergencies (Novello et al. 2021). Here, we followed the serological response against SARS-CoV-2 antigens in a cohort of 395 healthy individuals over a 27-month period, before and after the vaccination. Although our cohort represents almost 80% of the entire IBqM social body, the small number of participants would represent a limitation for some data interpretation. Nevertheless, here we monitored seroprevalence outside hospital environments, which is unusually reported in the literature, especially before COVID-19 vaccines became available, representing important sentinel-like surveillance that tracks viral spread even in asymptomatic individuals.

The results obtained during the pre-vaccination period of our study indicated a low incidence of individuals with positive serology (26.1%) in the first year of the pandemic, as also reported for a similar cohort (Brasil et al. 2022, Coelho et al. 2022, Henriques-Santos et al. 2022). Nevertheless, we identified 11% of positive cases among asymptomatic individuals, which supported the recommendation of molecular testing and social distancing independently of the presence of symptoms. Indeed, the increase in seroconversion between December 2020 and February 2021 seemed to be related to the relaxation of protective measures during festive periods (Geenen et al. 2023), as well as the emergence of the first variant of concern, P1 (Carvalho et al. 2022). Additionally, the correlation between this observation and the increase in COVID-19 cases in the State of Rio de Janeiro reinforces the usefulness of serological tests to alert the growing number of infected people. Importantly, during the first year of the pandemic, the number of serological tests carried out worldwide, and especially in Brazil, was low because of their high cost and limited availability (West et al. 2021). In this context, the development of a lower-cost in-house ELISA (Fernandes-Siqueira et al. 2022a) by our group was crucial for conducting the tests during that period.

The safety and efficiency of the vaccination regimens using CoronaVac, ChAdOx-1, and BNT162b2, as well as the complementary booster doses, have been demonstrated in studies carried out in Brazil and other countries (Bochnia-Bueno et al. 2022, De Sousa et al. 2022, Shrotri et al. 2022, Paula et al. 2022). ChAdOx-1 and BNT162b2 promoted a stronger immune response when compared to CoronaVac (Romero-Ibarguengoitia et al. 2022, Lin-Wang et al. 2022, Fernandes-Siqueira et al. 2022b), although our data revealed that two doses of all three vaccines provided a good humoral response in our cohort. After D3 and D4, anti-S antibody levels remained quite high across the entire cohort, regardless of the vaccination regimen, which is consistent with findings from other studies (Gouvea et al. 2023, Yechezkel et al. 2023). Remarkably, the considerable increase in anti-N antibodies during this period possibly reflects the emergence of the highly transmissible Omicron variant (Jalali et al. 2022, Murari et al. 2022).

In conclusion, this study supports that monitoring seroconversion in a cohort composed of healthy individuals during a pandemic situation, before and after the implementation of different vaccination regimens, is a strategy that can be applied in the surveillance of immune coverage in new situations. This strategy can be applied to both small centers and larger populations, considering regional differences and government measures (Fawole et al. 2023, Muttamba et al. 2022). Our work also generated a biobank with over 1,500 serum samples, resulting from up to 8 blood samples collected from the same individual during different pandemic phases. Furthermore, this biobank, as well as its respective demographic and serological data, could be useful for the scientific community in future health emergencies.

ACKNOWLEDGMENTS

We would like to thank Lavinia Reif Correa de Oliveira and Lilian Cristine de Ferreira (UFRJ – Universidade Federal do Rio de Janeiro, Brazil) for helping with sample organization; Dr. Marcos Fleury and all the members of Laboratório de Análises Clínicas, Faculdade de Farmácia (LACFar, UFRJ, Brazil) for performing the blood collection and sample preparation; our colleagues from Instituto de Bioquímica Médica Leopoldo de Meis (IBqM, UFRJ, Brazil), for financial support and encouragement; all the members of Laboratório de Bioquímica de Vírus for providing recombinant N protein; and Dr. Leda Castilho research group (COPPE, UFRJ, Brazil) for kindly providing recombinant S protein. This work was supported by Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), Brazil [grant numbers E-26/211.128/2021, E-26/201.173/2021]; and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil [grant number 312650/2021-3].

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Publication Dates

• Publication in this collection
  21 Mar 2025
• Date of issue
  2025

History

• Received
  26 July 2024
• Accepted
  17 Dec 2024