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Acceptance & Hesitation

Three-year COVID-19 and flu vaccinations among medical residents in a tertiary hospital in Italy: The threat of acceptance decline in seasonal campaigns

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Article: 2252708 | Received 21 Jun 2023, Accepted 24 Aug 2023, Published online: 14 Sep 2023

ABSTRACT

The COVID-19 vaccination campaign in Italy started in December 2020, and, due to the Omicron variant’s emergence, a second booster dose was recommended for high-risk individuals and healthcare workers from July 2022. The aim of the study was to evaluate the vaccination coverages for the COVID-19 second booster dose and to identify predictors of its acceptance within the population of medical residents (MRs) of the Fondazione Policlinico Universitario “A. Gemelli” IRCCS (FPG) University Hospital. The study was conducted at FPG from October 4th to December 21st, 2022, and COVID-19 second booster dose and influenza vaccines were administered. The study analyzed collected data and conducted multivariate logistic regressions to explore potential predictors of vaccination adherence. The analyses performed were compared with the sample enrolled in FPG residency programs at the start of the COVID-19 vaccination campaign. 1968 MRs were involved in the 2022–2023 vaccination campaign (mean age 28.97, SD 3.44), and the second booster dose of COVID-19 vaccination coverage was low (18.80%). Almost all participants opted for co-administration of COVID-19 and influenza vaccinations, leading to a similar rate of influenza vaccination coverage (16.26%). Being a frontline resident, meaning a direct involvement in managing COVID-19 patients and vaccination campaigns, was the main predictor of vaccination adherence (OR 1.72, 95% CI 1.25–2.17). The dropping in influenza vaccination coverage in 2022–2023 and the low adherence to COVID-19 second booster dose among young physicians is concerning, calling for tailored vaccination campaigns and interventions.

This article is referred to by:
COVID-19 and flu vaccinations among medical residents in a tertiary hospital in Italy: Correspondence

Introduction

The COVID-19 pandemic still significantly affects global health and economy.Citation1–3 According to the existing evidence, vaccination is the main preventive measure that can prevent and reduce the spread of infectious diseases.Citation4,Citation5 COVID-19 infections, serious illness, and fatalities have gradually declined as vaccination coverage rates have increased.Citation6–10 Similarly, unvaccinated people continue to have the highest recorded rate of severe outcomes.Citation11–15 From December 2020 to November 2021, vaccination has contributed saving an estimated 470,000 lives among adults 60 and older in 33 countries throughout the WHO’s European region.Citation16 However, despite the widespread evidence of the effectiveness of vaccination, substantial differences in vaccination uptake for the primary vaccination cycle and booster doses can still be found between countries and population groups.Citation11,Citation15,Citation17

The vaccination campaign in Italy started in December 2020, shortly after the Food and Drug Administration and the European Medicines Agency authorized the emergency use of Pfizer-BioNTech’s vaccine (BNT162b2).Citation18–20 Initially, the vaccine was offered to healthcare and social care workers, staff and residents of residential care facilities, people aged 80 years and older and between the ages of 60 and 79, and individuals with an extremely high vulnerability (who had a notably higher risk of experiencing severe or fatal forms of COVID-19, due to preexisting conditions).Citation21 In the following months, subsequent to the increase in available vaccine doses, the vaccination campaign was gradually extended to the rest of the population.Citation21,Citation22 Considering the evolution of the national epidemiological situation, the administration of the third dose of the vaccine (first booster dose) was subsequently approved and started on September 27, 2021.Citation23 Given the critical role played by healthcare workers, it was deemed necessary to mandate the COVID-19 vaccination for this category. Initially, starting from April 1, 2021, through Decree Law no. 44/2021, vaccination with the primary cycle was made compulsory.Citation24 Subsequently, from December 15, 2021, the obligation was also extended to the administration of the third dose of the vaccine.Citation25

From January 2021 to January 2022, it is estimated that approximately 8 million cases, over 500,000 hospitalizations, and around 150,000 deaths were averted in Italy thanks to the COVID-19 vaccination.Citation26

The changing in the epidemiological scenario, related to the emergence of the Omicron variant and the concerns about vaccines’ effectiveness,Citation27–31 led the Italian Ministry of Health to advise the administration of a fourth dose (second booster dose) of the COVID-19 mRNA vaccines on July 11, 2022, first to high-risk individuals (age ≥60 years or ≥12 years with concomitant/preexisting conditions),Citation32 and then to healthcare workers and other population groups.Citation33 This decision was based on the assumption that the benefits of a booster dose’s ability to prevent transmission and disease would outweigh any potential risks.Citation34 According to recent studies, four doses of BNT162b2 are more effective than three doses at preventing SARS-CoV-2 infection and severe disease.Citation8,Citation35–37 The European Centre for Disease Prevention and Control (ECDC) declared that it is currently not possible to establish the maximum duration of protection provided by the fourth dose nor a superiority in effectiveness of bivalent booster doses over monovalent ones, because of the short follow-up times of the existing research.Citation11 Moreover, looking ahead to the future vaccination campaign, the ECDC released interim public health considerations for COVID-19 vaccination roll-out during 2023, using mathematical modeling to analyze scenarios of campaigns restricted to once/twice a year and to the population aged 50 years and above and 80 years and above.Citation38

Concerning the second booster dose, as of March 8th 2023, about one-third of eligible beneficiaries have received it.Citation39 The administration of the second booster dose has never been issued as compulsory by the Italian government, in contrast to the previous three doses.Citation24,Citation25 Moreover, the compulsory vaccination expired with DL n. 162/2022 as of November 30, 2022.Citation40

The importance of health workers, including medical residents, in vaccination programs is well known;Citation41,Citation42 nevertheless, there is evidence of their hesitancy toward vaccinations, including the COVID-19 vaccine.Citation43,Citation44 Similarly, it has been discovered that the vaccination barriers of healthcare workers are similar to those of the general population and include doubts about the COVID-19 vaccine’s rapid development and worries about its efficacy.Citation44–46 The acceptance of vaccination, on the other hand, was linked to previous vaccination behaviors, higher levels of education and knowledge of COVID-19 and its vaccine.Citation43,Citation46–49

The issue of vaccine hesitancy among healthcare workers extends beyond COVID-19 vaccination and is also evident concerning influenza vaccination, historically characterized by lower coverage rates than desired.Citation50 Initially, it appeared that COVID-19 could be a driver of influenza vaccination, but this was challenged in last two years’ vaccination campaigns.Citation51–53 Since WHO established that COVID-19 vaccines can be co-administered with other vaccines, including influenza,Citation54 the Italian Ministry of Health has authorized the influenza vaccine co-administration with other vaccines.Citation55 The possibility of co-administration offers a positive lever for increasing coverage.Citation56,Citation57 Therefore, the two coverages (COVID-19 and influenza) should be evaluated together, for the possible reciprocal influence on vaccination adherence. Co-administration rates vary in different settings, but a high frequency of co-administration has been reported, with an important part of the variability explained by the conduct of awareness campaigns.Citation58,Citation59

The aim of the study was to evaluate the vaccination coverage for the COVID-19 second booster dose and the flu vaccine, and to identify predictors of its acceptance within the population of medical residents of the Fondazione Policlinico Universitario “A. Gemelli” IRCCS University Hospital.

Materials and methods

A database was created containing information about the 2022–2023 COVID-19 (fourth dose) and influenza vaccination campaign of medical doctors in a residency program at a tertiary teaching hospital in Italy (Fondazione Policlinico Universitario A. Gemelli IRCCS, hereinafter FPG). The vaccines used were respectively the Pfizer-BioNTech “Comirnaty” for COVID-19 and the Sanofi Pasteur quadrivalent “Vaxigrip Tetra” for influenza: the first was administered as a second booster dose (fourth dose), following the administration of a first booster dose or natural infection diagnosed by means of a molecular or rapid swab at least 4 months prior to the start of the vaccination campaign at FPG, according to the updated guidelines on boosters with RNA-bivalent vaccines during the anti-COVID-19 vaccination campaign of the Italian Ministry of Health; the second, was provided in the context of the annual vaccination campaign against influenza.

Both vaccines were provided for free. Data on vaccinations performed were recorded on FPG’s internal databases linked with the medical doctors’ matriculation number. The information was pseudonymized and processed in accordance with the relevant regulations and consent agreements. At FPG, the 2022–2023 COVID-19 and influenza vaccination campaign was conducted from October 4th to December 21st 2022 in four vaccination sessions, each consisting of two midweek days when the hospital vaccination center was open from 8 a.m. to 4 p.m. MRs were notified of the vaccination campaign through an e-mail sent to their institutional account and they were free to choose vaccination within their residency hospital or at another vaccination center.

The evaluation of the vaccination status variable took into account the occurrence of natural infection, as required by regional and national directives. In particular, subjects with a previous infection which occurred more than four months before the vaccination campaign were considered eligible for vaccination, while subjects with a previous infection less than four months before the vaccination campaign were excluded from the inferential analysis. No antibody investigations have been conducted to study immunity.

The sample was descriptively analyzed for demographic variables such as gender, age, year of residency, medical specialization school, COVID-19 vaccination status, COVID-19 vaccination within or outside the residency hospital, day of COVID-19 vaccine, previous COVID-19 infection contraindicating the vaccination, influenza vaccination status, influenza vaccination within or outside the residency hospital, day of influenza vaccination, and coadministration of COVID-19 and influenza vaccines during vaccine sessions. The residency field was coded into either frontline or not-frontline. Frontline MRs were considered those directly involved in managing COVID-19 patients or vaccination campaigns. Therefore, as in a previous work on MRs,Citation60 frontline residencies were: anesthesia and resuscitation; hygiene and preventive medicine; diseases of the respiratory system; infectious diseases; emergency-urgent medicine; internal medicine. Hygiene and preventive medicine was considered as frontline residency, because MRs were mostly involved as vaccinating doctors in the COVID-19 vaccination campaign.

Additionally, to account for differences in residency length, fourth- and fifth-year residents were combined for inferential statistics.

The data collected were compared with the sample enrolled in FPG residency programs at the start of the COVID-19 vaccination campaign and analyzed in a precedent work exploring the medical residents’ behaviors toward COVID-19 compulsory vaccination.Citation60 For the statistical analysis, the sample was reduced to the medical residents present in both databases (through duplicate analysis on matriculation numbers). The comparison led to the loss of data from residents who specialized in the year 2021–2022 (bearing in mind that in Italy medical specialization schools last between 4 and 5 years) and from new registrants in specialization schools during the year 2022–2023. Thirteen MRs have changed residency after the first booster dose, so they are included in the restricted sample despite being registered as first-year residents for their new discipline for the second booster dose. Descriptive analyses were repeated on this reduced sample, for the same variables considered for the 2022–2023 sample. Then, likewise, to explore potential predictors of vaccination, in or outside the residency hospital, multivariate logistic regressions were carried out with COVID-19 vaccination and COVID-19 vaccination performed within or outside the residency hospital as dependent variables, with a statistical significance of p < .05. The considered variables were gender, age, year of residency and frontline or not-frontline residency.

All analyses were performed using STATA software version 17 (Stata Corp, College Station, TX, USA). The study protocol was approved by the FPG Ethical Committee (ID3973).

Results

In total, 1968 MRs were involved in the 2022–2023 vaccination campaign. The sample included 891 (45.27%) male and 1077 (54.73%) female MRs, and the mean age was 28.97 (SD ±3.44) years; most of the participants were in their second year of residency (46.34%) and were non-frontline HCWs (69.82%) (). Interestingly, less than 20% (370, 18.80%) of the MRs received the second booster dose of COVID-19 vaccine, and they received it mainly at FPG (323, 87.30%). Sixteen percent (320, 16.26%) of MRs was vaccinated for influenza. Moreover, despite the low adherence to COVID-19 vaccination, nearly 92% (1804, 91.67%) of the HCWs considered might have been eligible for vaccination, as they didn’t test positive for COVID-19 in the previous 4 months.

Table 1. Sociodemographic characteristics of the 2022–2023 sample.

Moreover, the distribution of vaccination adherence was uniform among the days on which the vaccination campaign was conducted, both for COVID-19 and for influenza vaccines.

Ninety-five per cent of participants chose the co-administration of the vaccines (i.e., performing both vaccinations on the same day).

In the logistic regression model, adjusting by gender and year of residency, being a frontline resident is a statistically significant predictor of adherence to COVID-19 vaccination (OR 1.71, C.I. 95% 1.35–2.17, p-value <.001). This aspect ceases to be a predictor of adherence in the model on the vaccinations at FPG (p-value 0.857) ().

Table 2. Logistic regression models for COVID-19 vaccination and COVID-19 vaccination performed within the residency hospital for 2022–2023 sample and reduced sample (*p < .05, statistically significant).

When considering the MRs registered for both years 2021–2022 and 2022–2023, a total of 1465 MRs were involved in both the vaccination campaigns (COVID-19 campaign 2021–2022 and COVID-19 – influenza campaign 2022–2023).

The participants consisted of 663 males (45.26%) and 802 females (54.74%) with an average age of 29.38 years (SD ±3.14). The majority of the MRs were in their second year of residency (859, 58.63%) and were not frontline HCWs (997, 68.05%).

The number of MRs, registered for both years 2021–2022 and 2022–2023, who received the second booster dose of COVID-19 vaccine was similar to the main sample of 2022–2023 campaign (262, 17.88%), and they received it mainly at FPG (236, 90.08%). Again, despite 90.38% of the interns were eligible for COVID-19 vaccination, as they didn’t test positive for COVID-19 in the previous 4 months, low adherence was documented.

Sixteen percent (233, 15.90%) of MRs received influenza vaccination.

Once more, the distribution of vaccination adherence was uniform among the days on which the vaccination campaign was conducted, both for COVID-19 and for influenza vaccines.

Finally, almost all participants (225, 95.34%) chose the co-administration of the vaccines.

The logistic regression model on the restricted sample showcased similar results to the main model, highlighting the frontline residency as the main predictor factor of vaccination adherence (p-value 0.003). However, the campaign at the residency hospital reached both frontline and non-frontline MRs, since no statistical difference was found in the groups in the model.

Discussion

The COVID-19 second booster dose vaccination coverage in medical residents that emerged from this study was 18%. The European Centre for Disease Prevention and Control estimated through mathematical models that a 50% reduction on vaccination uptake should be expected for the second booster dose of the COVID-19 vaccination compared to the first booster dose.Citation61 Considering that a study performed on medical residents in the same large Italian hospital highlighted an uptake close to 100%, this reduction has proven to be even more substantial in practice.Citation60 For what concerns workplace vaccinations other than COVID-19, the desired vaccination rate is considered to be 40%,Citation62 nevertheless, for the 2022–2023 anti-flu campaign described in this study, the vaccination rate among MRs was as low as 16%. The influenza vaccination coverage in physicians at the same hospital has been raising in the years preceding the COVID-19 pandemic, increasing from 19% for the season 2016–2017 to 34% in 2018–2019,Citation63 going as high as 54% for the season 2020–2021 during the first year of the COVID-19 pandemicCitation56 and then dropping back down to 24% for the 2021–2022 campaign.Citation51

During the anti-influenza vaccination campaign in the season 2022–2023, the decreasing trend of the previous campaign was maintained.Citation64 The overall low vaccination uptake could be due to the misinformation campaigns that have been carried out during the COVID-19 pandemic, and to the ever more present anti-vaccination movements, both leading to the rise of vaccine hesitancy.Citation65 Several studies have highlighted an alarming growth in this phenomenon among healthcare workers concerning the administration of the second booster dose of the COVID-19 vaccine, either at an Italian or international level: Della Polla et al. reported how, on average, the HCWs interviewed believed in the usefulness of the second booster dose in 6.7 out of 10 cases,Citation30 while Pal et al. indicated a vaccine hesitancy as high as 68.8% among HCWs toward the booster dose.Citation66

In this study, the lowering in the vaccination coverage was observed among a particular subgroup of HCWs, young medical residents, and this is especially concerning. Physicians represent a highly specialized profession and should be informed concerning the risks of communicable diseases more than the general population; furthermore, medical residents as the young workforce in healthcare should be sensible to misinformation and capable of discerning it from reliable sources.

Healthcare professionals can influence patients’ behaviors,Citation42,Citation67 therefore optimizing behavior change interventions that target obstacles to and facilitators of advised practice is the main challenge. Healthcare professionals’ behaviors can be influenced by a variety of factors, and understanding behavior change is essential for trying to maximize population health.Citation68

The COVID-19 vaccination adherence, highlighted as a virtuous behavior in a previous study on the same population, was not maintained in regard to the second booster dose, both on the temporal distribution and the overall adherence data. Interestingly, a temporal correlation was highlighted for the first booster dose: the MRs that decided to receive the first COVID-19 vaccination early (meaning shortly after it became available for them) also got the first booster dose early. On the contrary, the phenomenon was not observed for the second booster dose.

This evidence may be related to two main factors. Firstly, the loss of obligations related to vaccination, enacted in the DL 162/2022,Citation40 may imply the legislative framework as the main driver to the vaccination itself, even in a selected population as young healthcare professionals. This aspect may be amplified by the misinformation campaign that was almost uncontrolled during the first two years of the pandemic. The second aspect is the change in the epidemiological scenario, as, during the year 2022, the lowering of the indicators mainly affecting the healthcare organizations and workforce (hospitalization and deaths) could have influenced vaccination adherence. The lower occurrence of severe complications of the COVID-19 illness in daily practice could have led to a diminished sensibility to the topic and, therefore, to the reduced adoption of preventive measures. This could have been amplified by the fatigue that the COVID-19 pandemic has posed to health care workers.Citation69,Citation70 A third aspect is related to the medical liability system. Although the institution of compulsory vaccination is often accompanied by vaccine compensation programs and specific policies for nonadherents, the climate of insecurity dictated by the increase in medico-legal litigation has probably affected trust in preventive measures and vaccination coverage.Citation71–73 Therefore, the change in the epidemiological scenario, the end of the emergency in Italy as of March 31st 2022,Citation74 and the fact that the second booster dose was not compulsory, may have had a strong impact on the perception of vaccination benefits in MRs, leading to a decreased adherence. However, this should be considered in the context of a still ongoing pandemic at the time this campaign took place, as the WHO declared the pandemic over only in May 2023.Citation75 This further supports the knowledge that information campaigns are essential to raise awareness and encourage non-compulsory vaccinations, not only in the general population but even in healthcare workers.

Considering the decrease in adhesion to the vaccination campaign and the fact that the COVID-19 vaccination is not compulsory anymore, a more in-depth promotion and information campaign for influenza and COVID-19 vaccination may be needed, as promoting workplace vaccination campaigns has been proven to be an essential tool to increase adherence.Citation76,Citation77

Furthermore, considering that it has been reported that approximately 80% of COVID-19 patients developed one or more long-term symptoms,Citation78 defining long COVID, with a significant burden of disability, vaccination campaigns should be strengthened, as vaccination has the potential to reduce the frequency and severity of long COVID, although further studies are needed to clarify the incidence of long COVID in partially and fully vaccinated people.Citation79–83

However, even considering the apparently low vaccine uptake from the results, the vaccination campaign proved to be significantly effective at reaching non-frontline MRs and nullifying behavioral differences between frontline and non-frontline MRs. Specifically, the logistic regression showed a significant correlation between frontline MRs and vaccination uptake (looking at vaccination in general). Still, it was no longer significant in the regression regarding the FPG vaccination. Organisational aspects should be based on the goal of enhancing the inherent characteristics of the target population and designing information/training programs tailored for the more “resistant” populations.

Specifically, the campaign was organized in the open-days modality, combining the offerings of influenza and COVID-19 vaccines. Ninety-five per cent of vaccinated people opted for the co-administration, showing great acceptability of this scheme. This tool helped to optimize resources and promote both vaccinations, increasing uptake and containing public health costs.Citation57

Venuto and colleagues found no statistically significant differences between the antibody response to single or combined vaccination, as well as adverse events, with almost the entire sample examined willing to repeat co-administration in future.Citation58 Considering the co-administration of COVID-19 and flu vaccinees, promoted at national level by the Italian Ministry of Health,Citation55 our results highlight in the MRs population an high propensity for co-administration, similarly to literature evidence,Citation58,Citation59 these studies have underlined a higher propensity than HCWs, and suggested that MRs might be a professional group in which to invest educational and training efforts to improve vaccine acceptance.Citation84

This paper should be considered in light of some limitations. Due to the fact that only available data on swabs taken or reported to the facility of affiliation were included in the COVID-19 test data used to calculate vaccine uptake latency, it is conceivable that these data were incomplete. Moreover, COVID-19 swab execution and reporting were not compulsory, possibly leading to under-ascertainment of cases. Additionally, since booking of vaccinations was conducted through an internal online booking system, it’s conceivable that some MRs weren’t reached by the e-mail communication disseminated by the health directorate. Furthermore, the comparison with adherence to the first booster dose should be considered in light of the change in the epidemiological scenario and the fact that the second booster was a non-compulsory vaccination for HCWs in Italy.

The three years considered are characterized by different COVID-19 epidemiological scenarios. The analysis presented in this article does not take into account the evolution of the burden of the disease, because the goal is not to offer a comparison of vaccination coverage over the years. The objective of the study, which we believe is the main innovation brought by this article, is to describe vaccination coverage for the second booster dose and explore whether the directives that established compulsive vaccination were able to maintain their effect, on the exact same population investigated in a previous article on the primary cycle and the first booster dose. In addition, this study investigates the influence of professional background and organizational factors on adherence. The change in the regulatory framework, while not particularly discriminatory in adherence to vaccination in the first two years of the pandemic, may have played a role in poor adherence during the third year.

More studies on the reasons and predictors of vaccination adherence are needed, underlining the different perspectives and needs of the different healthcare workers.

Conclusion

Healthcare workers are one of the target groups for vaccinations, due to their role in healthcare systems. The coverage for COVID-19 second booster dose and seasonal influenza vaccinations has been lower-than-expected for the second year in a row in the hospital considered in this research. Improving vaccine uptake should be a quality improvement goal in healthcare organizations and the experience reported in this research shows that compulsory policies can be an essential driver, establishing virtuous behavior in the population, but that this behavior is not maintained when vaccinations are only recommended. Co-administration is helpful in increasing coverage, but on its own it is not enough to promote vaccination. The decline in flu coverage among young doctors and the gradual stalling of COVID-19 vaccinations, in light of the unabated spread of the two infections, opens a scenario of concern and alarm for the future of seasonal vaccinations. It is of paramount importance to promptly reverse the trend. Awareness-raising campaigns targeting specific sub-populations could help promote good health practices among tomorrow’s health specialists.

Ethical approval and consent to participate

The study was approved by the Ethics Committee of the “Fondazione Policlinico Universitario A. Gemelli IRCCS” (Prot. No. 35880/22 of 16/11/2022, study ID 3973).

Informed consent was obtained from all subjects involved in the study.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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