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Peer-reviewed

Enquiry Article

Consequence of the third dose of BNT162b2 vaccine on quantitative SARS-CoV-2 spike ane–2 IgG antibiotic titers in healthcare personnel

• Diego Rivera-Salinas,
• Yodira Guadalupe Hernández-Ruíz,
• Ana Gabriela Armendariz-Vázquez,
• Arnulfo González-Cantú,
• Irene Antonieta Barco-Flores,
• Rosalinda González-Facio,
• Laura Patricia Montelongo-Cruz,
• Gerardo Francisco Del Rio-Parra,
• Mauricio René Garza-Herrera,
• Jessica Andrea Leal-Meléndez,
• Miguel Ángel Sanz-Sánchez

Event of the third dose of BNT162b2 vaccine on quantitative SARS-CoV-2 spike i–two IgG antibiotic titers in healthcare personnel

• Maria Elena Romero-Ibarguengoitia,
• Diego Rivera-Salinas,
• Yodira Guadalupe Hernández-Ruíz,
• Ana Gabriela Armendariz-Vázquez,
• Arnulfo González-Cantú,
• Irene Antonieta Barco-Flores,
• Rosalinda González-Facio,
• Laura Patricia Montelongo-Cruz,
• Gerardo Francisco Del Rio-Parra,
• Mauricio René Garza-Herrera

x

• Published: March 2, 2022
• https://doi.org/10.1371/journal.pone.0263942

Figures

Abstruse

Background

Vaccination is our main strategy to command SARS-CoV-2 infection. Given the subtract in quantitative SARS-CoV-2 spike 1–2 IgG antibody titers three months afterward the second BNT162b2 dose, healthcare workers received a third booster six months after completing the original protocol. This study aimed to analyze the quantitative SARS-CoV-2 fasten one–2 IgG antibody titers and the condom of the third dose.

Cloth and methods

A prospective longitudinal cohort study included healthcare workers who received a tertiary booster half dozen months after completing the BNT162b2 regimen. Nosotros assessed the quantitative SARS-CoV-ii spike ane–2 IgG antibody titers 21–28 days later on the first and second dose, 3 months after the completed protocol, i–seven days following the 3rd dose, and 21–28 days later on booster administration.

Results

The cohort comprised 168 participants aged 41(ten) years old, 67% of whom were female. The 3rd dose was associated with an increase in quantitative antibody titers, regardless of previous SARS-CoV-two history. In cases with a negative SARS-CoV-2 history, the median (IQR) antibody titer values increased from 379 (645.4) to 2960 (2010) AU/ml, whereas in cases with a positive SARS-CoV-ii history, from 590 (1262) to 3090 (2080) AU/ml (p<0.001). The third dose acquired a lower number of total (local and systemic) agin events post-obit immunization (AEFI) compared with the first ii vaccines. However, in terms of specific symptoms such as fatigue, myalgia, arthralgia, fever, and adenopathy, the proportion was higher in comparison with the beginning and second doses (p<0.05). The most common AEFI later the 3rd BNT162b2 vaccine was pain at the injection site (n = 82, 84.5%), followed by fatigue (northward = 45, 46.iv%) of mild severity (due north = 36, 37.1%).

Determination

The third dose applied half-dozen months afterwards the original BNT162b2 regimen increased the quantitative SARS-CoV-ii spike one–2 IgG antibody titers. The booster dose was well tolerated and caused no astringent AEFI.

Citation: Romero-Ibarguengoitia ME, Rivera-Salinas D, Hernández-Ruíz YG, Armendariz-Vázquez AG, González-Cantú A, Barco-Flores IA, et al. (2022) Event of the 3rd dose of BNT162b2 vaccine on quantitative SARS-CoV-ii spike 1–two IgG antibiotic titers in healthcare personnel. PLoS 1 17(3): e0263942. https://doi.org/x.1371/journal.pone.0263942

Editor: Mohd Adnan, University of Hail, Saudi arabia

Received: October 28, 2021; Accepted: Jan 28, 2022; Published: March 2, 2022

Copyright: © 2022 Romero-Ibarguengoitia et al. This is an open access article distributed nether the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the manuscript and its Supporting Information files.

Funding: The authors received no specific Funding for this work.

Competing interests: The authors have alleged that no competing interests be.

Introduction

In the first trimester of 2020, The World Health System (WHO) recognized the spread of SARS-CoV-2 equally a pandemic [i]. Its negative and severe bear on on society, the economy, and health due to its pregnant morbidity and mortality prioritized vaccine development to control the affliction worldwide. Many vaccines were adult for emergency apply [two]. The vaccines could lead to the development of spike-specific IgG antibodies confronting SARS-CoV-2, so serology assays have been used to detect the fasten protein domain antibodies induced past vaccination or prior viral exposure [3].

The vaccine blazon depends on its mechanism of activity. To appointment, the different SARS-CoV-two vaccines designs are: mRNA (BioNTech-Pfizer/BNT162b2, Moderna/mRNA-1273), adenovirus viral vector (Oxford-AstraZeneca/ChAdOx1, Gam-COVID-VAC/Sputnik V, Ad26.COV2.S/Jannsen, CanSinoBio/Ad5-nCoV), protein subunit (Novavax/NVX-CoV2373, Medicago CoVLP), whole-cell inactivated virus vaccines (Inova/CoronaVac, Sinopharm/ BBIBP-CorV), and Deoxyribonucleic acid vaccines (INO-4800 and ZyCoV-D) [iv].

The Pfizer and BioNTech vaccine, hereafter referred to as BNT126b2, was the outset SARS-CoV-2 vaccine to prove promising efficacy. On November xviii, 2020, it was proven to be 95% effective confronting symptomatic and severe disease [five]. As a result, in Dec 2020, the WHO and the Food and Drug Administration (FDA) authorized this vaccine for emergency use, the first SARS-CoV-two vaccine to receive emergency approval [6, vii].

The Centers for Disease Control and Prevention (CDC) and the U.South. Food and Drug Administration (FDA) have authorized a third BNT162b2 vaccine to the following individuals: 1) individuals > 50 years of historic period with a medical status; 2) individuals > 18 years of age, residents of a long-term healthcare facility; iii) individuals between the ages of 18–49 with a medical condition; and 4) employees and residents in healthcare facilities at high risk of SARS-CoV-2 exposure and transmission [eight, 9].

Immunity against SARS-CoV-2 induced with BNT126b2 vaccination provides a significant caste of protection. All the same, the duration of this protective immunity remains unknown. Many ongoing studies have focused on public concerns on the safety and efficacy of BNT126b2 over time [x]. Some studies have reported a significant antibody decrease three- and six months post-vaccination in individuals who completed the 2-dose regimen [x–12]. Farther, new strains of the SARS-CoV-two virus could develop if it continues to replicate and be transmitted, and some may even become resistant to a vaccine [5].

The question of whether there is a need for a third dose remains open up. Some countries have decided to apply a booster in severely immunocompromised individuals, but it is still unknown whether this would be necessary for the full general public [xiii]. Therefore, this written report aimed to measure SARS-CoV-2 spike 1–2 IgG antibodies in healthcare personnel vaccinated with the consummate ii-dose regimen of BNT126b2, and who received a third booster dose six months after the 2nd dose.

Material and methods

This was a prospective observational written report that followed the STROBE guidelines [14]. It analyzed a subgroup of patients who completed the two-dose regimen of BNT126b2 in early 2021 in Monterrey, Nuevo León, United mexican states. The report was canonical by the local Institutional Review Board (Ref.:26022021-CN-1e-CI) and conducted per the Code of Ethics of the World Medical Association (Declaration of Helsinki) for experiments involving human subjects.

The inclusion criteria for the patients' recruitment were: individuals of both genders between the age of 18 and 100 years one-time, who had accepted and signed an informed consent form, and had the intention of completing the BNT126b2 protocol. The patients were excluded if they did not consummate the established vaccine regimen or received another SARS-CoV-2 vaccine.

The report subjects were introduced to the enquiry protocol, specifying that it included a follow-up menstruum of an entire year, the determination of SARS-CoV-2 specific IgG antibodies also every bit the awarding of questionnaires. After agreeing, they signed a written informed consent class. Since this subgroup comprised healthcare personnel, in this country they were immunized against SARS-CoV-ii with BNT126b2 in early 2021. Since this protocol was canonical later on the application of the first BNT, 20-one days later on receiving this initial dose, the research team reached every participant to obtain a plasma sample for IgG antibody determination and the application of the outset questionnaire. This questionnaire had the purpose of recording the patient'south medical history, their status of SARS-CoV-2 infections before and after immunization, and identifying agin events post-obit immunization (AEFI) [fifteen, sixteen].

Xx-one to 28 days afterwards receiving the second dose, the participants were scheduled to provide the second sample for IgG antibody determination and complete a similar questionnaire to that previously practical. The tertiary, fourth, and fifth IgG antibody samples were planned to be collected iii, six, and twelve months after completing the two-dose regimen of BNT126b2. The questionnaires applied at the time of the blood collections had the aim of establishing the evolution of any suspicious or confirmed SARS-CoV-2 infections.

The plasma sample required 10 to 15 ml of blood obtained per venipuncture. These samples were placed in sample tubes with ethylenediaminetetraacetic acid (EDTA) as an anticoagulant and stored at -80°C. The equipment used by the laboratory personnel to clarify the samples was the LIAISON SARS-CoV-2 S1 / S2 IgG antibody detection kit (Italy), which uses magnetic chaplet coated with S1 & S2 antigens. To determine the amount of specific anti-S1 and anti-S2 IgG antibodies against SARS-CoV-two in the plasma samples, the laboratory personnel used a chemiluminescence immunoassay (CLIA), with a sensitivity of 97.4% (95% CI, 86.eight–99.5) and a specificity of 98.5% (95% CI, 97.5–99.ii). The results were reported equally follows: <12.0 AU / ml was considered negative, 12.0 to 15.0 AU / ml was indeterminate, and > fifteen AU / ml was positive. The agreement in the detection of neutralizing antibodies is 94.four% [17, 18]. This kit is comparable to other commercial kits such as euroimmun and Roche and has been used in other studies past authors such every bit Fabrizio Bonelli et al., Maria Teresa Sandri et al., Riccardo Levi et al. [xviii–21].

Over the three-calendar month follow-up, at that place was a decrease in the amount of specific anti-S1 and anti-S2 IgG antibodies against SARS-CoV-ii. This finding raised concern among the healthcare personnel, leading them to seek a BNT126b2 booster on their own, thus infringing the original BNT regimen. Furthermore, six months after the two-dose BNT162b2 regimen, 168 participants received a third booster. Given the situation, ii additional blood samples were collected from the participants: 1–seven days afterward the booster (once the research team was notified), and 21–28 days afterwards the tertiary booster.

The variables we analyzed were age, gender, medical history, including the confirmation of a SARS-CoV-2 diagnosis (either with a nasal swab or serologic tests earlier and later the BNT126b2 shots), and the evolution of AEFI whatever dose of BNT126b2. The analyzed biochemical variables were SARS-CoV-2 quantitative antibodies 21–28 days subsequently the start BNT126b2 dose (S1), 21–28 days afterward the BNT126b2 2nd dose (S2), at the three-month follow-up after completing the two-dose BNT126b2 regimen (S3), and 1–7 days (S4) and 21–28 days after the BNT booster (S5).

The researchers reviewed the quality control parameters and the anonymization of the database. We presented results with descriptive statistics such every bit median, the interquartile range for quantitative variables, frequencies, and percentages for categorical variables. Group comparisons were established with Cochran'due south Q test for chiselled variables. The Mann Whitney U test was performed for the quantitative comparison of IgG antibodies between individuals with a positive vs. negative history of SARS-CoV-2 infection. Wilcoxon signed-range examination was performed for IgG comparison betwixt two fourth dimension points of BNT126b2 dose. Additionally, nosotros developed a mixed model in which the dependent variable was the antibody values. The reference group was the quantitative SARS-CoV-ii antibody total value 21–28 days after the start BNT126b2 dose (S1). Personal variation was constructed as a random effect, and every time antibodies were measured, discipline gender and history of SARS-CoV-2 represented the statistical stock-still effect. Completely missing random values were analyzed by consummate example assay. The statistical program used was SPSS, version 2. The analysis was two-tailed, and a p-value < 0.05 was considered statistically meaning.

Results

One hundred and 60-viii (168) recruited participants received a three-dose BNT126b2 regimen, and 113 (67.3%) were female person. Their mean (SD) age was 41 (10) years. The most common comorbidity was obesity (44, 26.2%), followed by dyslipidemia (15, viii.9%) and hypertension (14, 8.3%). Table ane shows the participants´ medical histories every bit referred in the offset questionnaire. The fourth dimension (SD) between the start and 2nd BNT126b2 vaccines was 31 (iv) days, and betwixt the second and third dose, it was 166 (12) days.

History of SARS-CoV-2

In terms of previous SARS-CoV-2 diagnoses, 95 (56.5%) of the participants reported never having the infection. 70-three (43.5%) participants referred a SARS-CoV-2 diagnosis before vaccination and 21–28 days afterward the third BNT booster. Before vaccination, at that place were 65 (38.7%) healthcare workers with one confirmed SARS-CoV-ii infection, and 7 (4.2%) that had been infected twice. In that location were three (1.8%) participants with a SARS-CoV-2 diagnosis betwixt the first and second BNT doses, 1 (0.6%) between the second and 3rd BNT doses, and none after the third dose. Table 2 shows the history of SARS-CoV-2 infection amidst participants, in frequencies and percentages.

Antibody titers

The median (IQR) quantitative SARS-CoV-2 spike 1–2 IgG antibody titers (AU/ml) obtained in the healthcare personnel with no history of SARS-CoV-2 infection (n = 95) was 1350 (1224.0) afterwards 21–28 days of BNT162b2 second dose, and in subjects with history of SARS-CoV-two (n = 73), 2390 (2540.0), p = 0.002. 3 months afterwards two doses, antibiotic concentrations decreased 84.8% and 84.four%, in negative and positive SARS-CoV-2 participants, respectively. After 21–28 days of BNT162b2 3rd dose, AU/ml IgG titers increased to 2960 (2010.0) and 3090 (2080.0) in subjects with negative and positive history of SARS-CoV-2 respectively (p = 0.377). If we compare the IgG titters 21–28 days after second with 21–28 days afterward tertiary BNT162b2 dose, in both groups (positive and negative history of SARS-CoV-2 infection), there is a statistical increment (p<0.001).

Tabular array 3 presents the median (IQR) of the quantitative SARS-CoV-2 IgG antibody titers once the participants were divided into two groups according to their history of SARS-CoV-two infection.

Fig ane shows boxplot schemes of the quantitative SARS-CoV-two spike 1–2 IgG antibody titers confronting SARS-CoV-2, to compare the results between groups with a negative or a positive SARS-CoV-2 history.

Quantitative SARS-CoV-2 spike ane–ii IgG titers afterwards the first and second dose, 3 months, 1–7 days later the third dose, and 21–28 days following a BNT162b2 booster, dividing the population into two groups according to the SARS-CoV-2 history.

Nosotros created a mixed model in which IgG levels 21–28 days after the BNT162b2 start dose were considered as the reference for comparisons. This model showed a divergence in terms of patient gender since females had higher antibody titers (β = -652.3, p = 0.021). In improver, a higher BMI was associated with an increase in antibiotic levels (β = 74.5 p = 0.02). There was a positive issue in subjects with a positive SARS-CoV-2 history (β = 1147.nine, p< 0.001), and the antibody levels changed over time (p<0.01). When we compared the antibody titers 21–28 days subsequently the 2d and third doses, at that place was a greater increase after the latter dose (β = 591.5, p = 0.004 and β = 1782.three, p< 0.001, respectively). Tabular array 4 and Fig 2.

Event of each BNT126b2 dose, showing an increment in quantitative SARS-CoV-2 spike 1–2 IgG antibodies. Variables such every bit a positive SARS-Cov2 infection history, female sex, and a high BMI led to a greater increase in antibody titers.

Adverse events following immunization (AEFI)

AEFI were reported after the first, 2d, and third BNT doses; the everyman total number of events were reported after the tertiary BNT162b2 dose (north = 140, 83.0%; n = 133, 79.1%; and n = 97, 57.7%, respectively) (p<0.001). After the starting time and 2nd BNT doses, AEFI developed most frequently within the first four hours after application (n = 116, 82.8%; and north = 59, 44.4%, respectively), whereas after the third vaccine, AEFI were reported 5 to 24 hours subsequently (north = 56, 57.vii%). Their severity was referred to as very mild later on the start and 2nd BNT doses (due north = 95, 67.eight%; and n = 57, 42.8%, respectively), and mild subsequently the third BNT booster (n = 35, 36.0%).

The most mutual AEFI resulting from the three administered vaccines were pain at the injection site (n = 131, 93.6%; n = 119, 89.v%; and due north = 82, 84.0%, respectively), followed past headache (north = 51, 36.4%; n = 58, 43.6%; and 43, 44.iii%, respectively), and fatigue (due north = 38, 27.one%; due north = 54, 32.1%; and n = 45, 46.4%, respectively). Specifically, when comparing the AEFI later on each dose, fatigue, myalgias, arthralgias, fever, and adenopathy were proportionally more frequent post-obit the third dose, than with the 2-dose regimen (p<0.05). Table five shows the AEFI reported by the participants in frequencies and percentages, and Tabular array 6 shows the time of their presentation and their severity.

Discussion

The purpose of this study was to analyze the quantitative SARS-CoV-2 fasten 1–ii IgG antibiotic titers over six months later completing the established BNT126b2 vaccination regimen, and 21–28 days following a third BNT126b2 dose practical half dozen months after the 2nd dose. 3 months after the second dose, antibodies decreased in comparison with the titers determined 21–28 days after the second dose. In addition, in the sample nerveless 1–7 days later the third dose—equivalent to the sample after six months of the complete regimen -, the antibody titers were lower than those reported 21–28 days after the 2nd dose.

Previous studies accept demonstrated a decrease in the quantitative SARS-CoV-2 spike i–2 IgG antibody titers after completing the BNT126b2 protocol, regardless of the patients´ SARS-CoV-ii history. Alejo Erice et al. reported a 58% decrease in the quantitative SARS-CoV-ii spike 1–2 IgG antibody titers later three months [22].

In addition, the written report conducted by Julien Favresse et al. referred a decrease in antibody titers 56 to 90 days after the 2d BNT162b2 vaccine, in participants that were seronegative and seropositive at the showtime of the study [11]. Our study was concordant with these previous investigations in terms of the subtract in the quantitative SARS-CoV-2 spike one–two IgG antibiotic titers observed in the third sample. Three months after completion of the BNT162b2 protocol, antibodies decreased 84.8% and 84.4% in negative and positive SARS-CoV-two infection participants, respectively.

20-one to 28 days later on the assistants of the third BNT162b2 booster, the quantitative SARS-CoV-2 fasten i–2 IgG antibiotic titers increased drastically. Participants with a negative SARS-CoV-ii infection increased their antibody titers over six-fold in comparison with the previous results obtained one–vii days after the third dose; in positive SARS-CoV-ii infection cases, titers increased iv-fold. According to our mixed model, when we compared the estimates from days 21–28 afterwards the second dose and 21–28 later on the tertiary dose, there was a greater increment in antibody levels afterward the third dose.

In a study in which heart transplant recipients were vaccinated with a 3rd BNT162b2 dose, Yael Peled, et al. reported a three-fold increase in anti-receptor binding domain antibodies, despite immunosuppressive therapy [23]. Additionally, according to Yinon Grand Bar-On et al., after a third BNT162b2 booster dose was administered to an Israeli group of individuals over lx years of age, the rates of confirmed SARS-CoV-ii infection and severe illness decreased in comparison with a control group immunized with the original BNT162b2 2-dose regimen [24]. Given these situations and our findings, a regimen of iii homologous BNT162b2 doses regimen in which the third dose is administered six months later on the second vaccine, provides a benign upshot in terms of a positive humoral immune response confronting SARS-CoV-ii infection.

During the half dozen months before the 3rd dose, we noticed an increment in the quantitative SARS-CoV-two spike 1–ii IgG antibody titers amongst participants with a positive history of SARS-CoV-2, in comparison with those with a negative history. Interestingly, in the results obtained 21–28 days after the third booster dose, the divergence betwixt the participants with a positive or negative SARS-CoV-2 history was not as perceptible equally with the beginning 2 vaccines. This suggests that later the third dose, participants with a negative SARS-CoV-ii history take the aforementioned level of humoral amnesty as those previously exposed to a SARS-CoV-ii infection.

Our mixed model showed interesting results in terms of patient gender and BMI. A study past Pellini et al. analyzed the differences between genders in the quantitative SARS-CoV-2 fasten 1–ii IgG antibody titers. Vii days following the second BNT162b2 dose, the researchers found that females developed a superior humoral response. Although our report had a longer follow-up menstruation as well as the analysis of plasma after a 3rd dose, the trend was like, since women developed college antibody titers than men post-obit immunization [25].

In terms of the BMI, we found an opposite event to that of Pellini et al. Nosotros found that a college BMI was associated with an increase in antibody levels. Since the prevalence of obesity in Mexico and Italy is unlike, nosotros believe that there might be a relation between a greater increase in antibodies and extreme values of BMI, either a high or depression BMI. Models based on cubic relations should be further explored [25].

The main concern with the application of the 3rd dose was the lack of information on the development of possible AEFI. Yael Peled et al. reported that 67% of participants who received a third BNT162b2 booster reported at least i AEFI of mild severity. The most common AEFI were pain at the injection site, fatigue, and headache, but no hospitalizations or emergency room (ER) visits (23) were necessary. Our report also constitute that the AEFI associated with the third dose were mild, and the about frequent were pain at the injection site, fatigue, and headache, with no associated severe complications such as hospitalization or ER visits. In comparison with the other doses, the total number of AEFI caused by the third dose was minimal; they decreased 30.seven% and 27.0% in comparison with those reported after the kickoff and second BNT162b2 shots, respectively.

To the best of our knowledge, no previous studies have shown the quantitative SARS-CoV-2 fasten 1–2 IgG antibiotic titer response to a 3rd BNT162b2 booster in not-immunocompromised patients. We believe that this report may contribute to farther the healthcare community´s noesis since we observed a positive humoral immune response to the third BNT162b2 dose in our healthcare personnel. This can pb to better protection amongst healthcare personnel and in groups that are vulnerable to severe illness by SARS-CoV-2.

Approval of the third BNT162b2 dose and its proven efficacy could also promote better command of the SARS-CoV-2 pandemic, providing greater immunogenicity among the vulnerable population. Consequently, the number of confirmed cases and hospitalizations in United mexican states could subtract.

A limitation to our report is the fact that the recruited group did non have a baseline sample obtained before the outset BNT162b2 dose considering our protocol was approved subsequently the health personnel had received the first dose. However, we believe that this report is significant since our population was not immunocompromised. Another limitation is that the analysis of the third dose's adverse events after immunization was only conducted in the curt term (21–28 days after the booster dose). We will keep following this cohort to determine any long-term AEFI related to the vaccine since nosotros have just reported the short-term AEFI in this study. Another limitation of this study was that the analysis used to measure out IgG did not discriminate between immunization or straight exposure to SARS-CoV-2. Finally, although the positive cyclopedia of quantitative SARS-CoV-2 spike i–two IgG antibody titers with neutralizing antibodies has been reported to be 94.4%, it would exist of involvement to mensurate the latter in our population [17, 18].

Conclusion

The third BNT162b2 booster dose has proven to increase the quantitative SARS-CoV-2 fasten i–2 IgG antibody titers with no severe curt-term AEFI. Despite its positive response, we must continue studying this cohort to constitute whether the antibody titers persist and SARS-CoV-ii infections and their consistent severe illness decrease.

BNT162b2 Pfizer/BioNTech is ane of the most studied vaccines due to its efficacy and worldwide application. After approving of its tertiary dose by the CDC and FDA, further enquiry on BNT162b2 and its new vaccination protocol will provide disquisitional data to the medical field, hence contributing to improve control of the pandemic. Our accomplice study may be considered significant since no other studies quantitatively measuring SARS-CoV-2 spike 1–ii IgG antibody titers in healthcare personnel had been found when this commodity was written.

We will go on pursuing our written report to written report farther findings that may provide more relevant data that could contribute to the control of the SARS-CoV-2 pandemic.

Supporting information

Acknowledgments

We are grateful to the laboratory squad, human resources, call center, technology, and maintenance personnel of the Hospital Clínica Nova, for their help in the logistics of this study.

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Source: https://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0263942

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