ABSTRACT
With the pandemic, there has been a global reduction in influenza virus circulation, with WHO reporting, during 2021/22 season, laboratory testing positivity rate for influenza of less than 3%. Influenza surveillance systems anticipated a peak of influenza cases in the Northern Hemisphere during 2022/2023 season and the Italian Ministry of Health recommended the routinary co-administration of influenza with bivalent COVID-19 vaccines for the 2022/2023 season. At the Vaccination Hub of the University Hospital (UH) of Palermo, more than 700 subjects received influenza and COVID-19 booster doses in co-administration, during the 2021/2022 season. A cross-sectional study analyzing attitudes and factors associated with adherence to influenza and COVID-19 seasonal vaccines co-administration was conducted at the Vaccination Hub of the UH of Palermo, from October to December 2022. Among the 1,263 respondents, 74.7% (n = 944) received the co-administration of seasonal influenza and COVID-19 vaccines. The main reason reported for accepting it was confidence in the recommendations of the Health Ministry (41.3%). At the multivariable analysis, subjects aged ≤ 59 y old (AdjOR: 2.48; CIs95%: 1.89–3.65), male (AdjOR: 1.51; CIs95%: 1.27–1.75), Health-care professionals (HCPs) (AdjOR: 1.66; CIs95%: 1.08–2.57) and those who received co-administration during 2021/2022 (AdjOR: 41.6; CIs95%: 25.5–67.9) were significantly more prone to receive co-administration during 2022/23 season. From data obtained, the role of HCPs in accepting and then promoting co-administration of COVID-19 and influenza vaccines is crucial, as well as receiving co-administration in the previous season that represented the main drive for accepting it in the following seasons, supporting safety and effectiveness of this procedure.
Introduction
The emergence of Severe Acute Respiratory Syndrome by Coronavirus 2 (SARS-CoV-2) in late 2019, followed by its pandemic spread in 2020, had a major impact on the circulation of influenza viruses.Citation1
During the last two influenza seasons, 2020/2021 and 2021/2022, a dramatic reduction in cases of influenza-like illness (ILI) syndromes was observed globally.Citation2,Citation3
Multiple factors may have contributed to this epidemiological change, including nonpharmacological interventions, reduced population movement (both local and long-distance), possible virus–virus interactions, sometimes referred to as “viral interference.”Citation1
However, in countries within the temperate zone of the Southern Hemisphere, influenza surveillance showed an increase in confirmed influenza cases in the 2022 season: between mid-April 2022 and the end of July 2022, the weekly number of notifications of laboratory-confirmed influenza cases reported in Australia exceeded the five-year average data. After 2 years without circulation of influenza virus in Australia, the 2022/2023 season was characterized by a high peak of cases in June and it was dominated by influenza A (mainly A/H3N2).Citation2
In some areas of Australia, concurrent with the circulation of influenza A, there was an increase in respiratory syncytial virus (RSV).Citation2
In the 2022/2023 influenza season in Italy, the peak of influenza syndrome cases occurred earlier (48th-49th week), compared to previous seasons. This observation confirmed the prediction made in the Ministry of Health circular dated July 6, 2022, which recommended starting the influenza vaccination campaign in early October.Citation3
Furthermore, in December 2022, Europe witnessed the circulation of RSV alongside influenza viruses and SARS-CoV-2. This occurrence led to an increase in severe acute respiratory infections (SARIs) among vulnerable groups and placed significant pressure on health-care systems, earning the term “Triplendemic” in the ECDC Rapid Risk Assessment.Citation4
Vaccination represents the main public health intervention to reduce the burden of seasonal influenza disease.Citation5 Similarly, vaccination against COVID-19 is a primary intervention to tackle the ongoing pandemic.Citation6,Citation7
Regarding the Respiratory Syncytial Virus (RSV), in June and August 2023, the European Medicines Agency (EMA) recommended the approval for marketing authorization of “Arexvy” by GSK® and “Abrysvo” by Pfizer®, respectively.Citation8,Citation9
The two new vaccines are designed to provide active immunization for adults over 60 and “Abrysvo” also for passive immunization for newborns from birth to 6 months of age following maternal vaccination during pregnancy.Citation8,Citation9
The vaccination campaign against COVID-19 in Italy started on December 27, 2020. As of January 14, 2023, Italy has administered 143,534,102 anti-COVID-19 vaccine doses. Approximately 48,071,760 (90.2% of the over-12 population) have completed the primary vaccination cycle. Additionally, 41,944,802 people (87.93% of those eligible) have received booster/additional doses, and 7,391,036 individuals (38.66% of the booster dose-eligible population) have received a second booster dose. Furthermore, 1,535,596 anti-COVID-19 vaccine doses were administered to 5–11-year-olds, covering 42% of this age group.Citation10,Citation11
In Italy, the recommendation for co-administration COVID-19 and influenza vaccines contextually in the same vaccination session was introduced in the 21/22 season; and also for the 2022/2023 season, the Ministry of Health confirmed the opportunity for co-administration of all influenza vaccines available with COVID-19 vaccines updated against BA.4/BA.5 Omicron variants where sustainable.Citation1,Citation12
Indeed, it has been observed that co-administration of COVID-19 and influenza vaccines preserves the immune response to both vaccines without any safety concerns.Citation13–16
Guidelines issued by the United States Centers for Disease Control and Prevention (CDC) state that COVID-19 vaccines can be administered independently of the timing of other vaccines, including seasonal influenza vaccines (SIV). The World Health Organization (WHO) suggests that co-administration of any inactivated SIV and any approved COVID-19 vaccine is a feasible option due to its logistical simplicity and the potential for increased coverage.Citation17,Citation18
Similar recommendations have been provided by public health authorities in other countries, including, France, Germany, Spain, Finland, the UK, and Russia.Citation19–24
The primary objective of the present study is to assess the acceptance of influenza and COVID-19 vaccines co-administration and the reasons behind non-administration or successful co-administration at one of the major vaccination Center of Sicily, at the University Hospital of Palermo. Sicily, with approximately 5 million inhabitants, is the fourth most populous Italian region, and Palermo is the most populous Sicilian Province with 1,2 million inhabitants.Citation25
The vaccination unit of the University Hospital of Palermo is one of the region’s key vaccine hubs. For the past 2 years, it has been one of the few centers in the region offering the co-administration of COVID-19 and influenza vaccines. Over the last 5 years, the center has administered approximately 3,000 to 4,000 SIV doses per season.
Since December 2020, it has administered around 80,000 of COVID-19 doses. Additionally, the Palermo UH is the sole hospital in Western Sicily with an outpatient vaccination unit, serving health-care workers, employees, inpatients, and the general high-risk population.
Currently, several COVID-19 vaccines are authorized by the European Medicines Agency (EMA) and the Italian Medicines Agency (AIFA).
During the study period, the following vaccines were used ():
mRNA-1273 (Moderna®);
BNT162b2 (Comirnaty®);
NVX-COV2373 (Nuvaxovid®).
Table 1. COVID-19 and influenza virus vaccines used during the study period.
These vaccines are licensed and recommended in active and free of charge offer, for different age and at-risk groups in accordance with available evidence on efficacy and safety.Citation9
For the 2022/2023 influenza season, the Italian Ministry of Health recommended in active and free of charge offer, several influenza vaccines.Citation1 During the study period, the following influenza vaccines were used in Sicilian context among adult population ():
QIV quadrivalent split virion inactivated vaccine – Vaxigrip Tetra® and QIV – Fluarix Tetra® both indicated in adults and children from 6 months old;
VIQcc – Flucelvax® quadrivalent inactivated cell culture vaccine indicated in adults and children from 2 y of age;
VIQhd – Efluelda high-dose vaccine® indicated in adults 60 y of age and older.
VIQa – Fluad Tetra® quadrivalent adjuvanted inactivated vaccine indicated for people aged from 65 y ().
In order to design effective targeted health promotion interventions, it is useful to quantify public acceptance of COVID-19 and SIV co-administration or combined vaccines.
Methods
A cross-sectional study was carried out from October 2022 to January 2023 to investigate the knowledge, attitudes, and acceptance rate of COVID-19 and influenza vaccines among patients attending the vaccination unit of the University Hospital of Palermo during the 2022/2023 influenza and COVID-19 vaccination season.
Sample collection
Participants in this study were selected based on specific inclusion and exclusion criteria.
Inclusion criteria
We included individuals who presented themselves to the University Hospital of Palermo vaccination center for any vaccination procedure or counseling needs.
Exclusion criteria
Individuals excluded from the study comprised minors than 18 y.o. and those who were incapable of providing informed consent.
Questionnaire structure and administration
The anonymous, self-administered questionnaire was provided to patients referred to the vaccine center for any type of vaccine administration and was completed through a Google Forms® platform, protected by password and accessible only to health-care personnel involved in the study.
Questionnaire was administered during the observation period following vaccination to those subjects who matched inclusion criteria.
The questionnaire consisted of 20 items divided into the following sections:
Sociodemographic data: gender, age.
Employment data: whether the individual works in healthcare and if so, their specific health-care profession (Medical doctor; doctor in training; student trainee; other health-care worker; administrative worker in health-care institution; other).
Health status: the presence of comorbidity and the type of comorbidity, if applicable (cardiac diseases, neoplastic diseases, nephrological diseases, pulmonary diseases, hematological diseases, rheumatological diseases, and others).
Influenza vaccination: whether the influenza vaccine has been administered and if so, which type of influenza vaccine was given (QIV-cc, QIV-e, aQIV, QIVhd, and Fluenz tetra).
COVID-19 vaccination: if COVID-19 vaccine has been administered and, if so, which COVID-19 vaccine has been administered (mRna-1273 bivalent D614G/BA.1, mRna-bnt162b2 Bivalent D314G/BA.1, mRna-bnt162b2 Bivalent BA.4/BA.5, proteic subunit-NVX-CoV2373, Adjuvanted Recombinant Protein-based, mRna-1273 Bivalent BA.4/BA.5), and which dose was administered (first, second, first booster, second booster, third booster).
Knowledge about co-administration of influenza and COVID-19 vaccines: awareness of the possibility of receiving both vaccines (flu and COVID-19 vaccines) in the same vaccination session; source of information about co-administration (family doctor, pharmacist, pediatrician, social network, web, print newspapers, online newspapers, TV, scientific magazine government sites, family, colleagues, friends); any co-administration performed in the previous year (right arm and left arm); willingness or refusal to receive both vaccines simultaneously and the primary reason for accepting or refusing it.
The questionnaire, available as Appendix A, along with the informed consent and information about the study, was previously validated and approved by the Ethical Committee Palermo 1 on October 19, 2022.
Results
A total of 1,263 subjects vaccinated at Palermo University Hospital’s Vaccination Hub completed the questionnaire. The main socio-demographic characteristics and data related to the acceptance of the co-administration of COVID-19 and flu vaccines are shown in . The most represented age group was the 41–59-year old (42.9%; n.543), followed by the over 60-year-old age group (34.5%; n.436), with female respondents comprising the majority (51.4%; n.649).
Table 2. Socio-demographic characteristics and data related to the acceptance of the co-administration of COVID-19 and seasonal influenza vaccines of the 1,263 subjects interviewed at the vaccination hub of the University Hospital of Palermo, Italy.
The majority of respondents (72.8%; n. 920) reported having no comorbidities. Among 27.2% of the subjects who reported comorbidities, the following conditions were identified: cardiac diseases (33.1%; n.113), hematological diseases (6.4%; n.22), nephrological diseases (0.88%; n.3), cancer (7.04%; n.24), lung diseases (6.16%; n.21), rheumatic diseases (11.4%; n.39), and other diseases (34.9%; n.119). Among the subjects enrolled in the study, (40.1%; n.507) were health-care workers (HCWs), with medical doctors comprising the majority (60.4%; n.306), followed by other HCWs (nurses, obstetricians …) (22.5%; n.114) ().
Regarding the knowledge, attitudes, and practices of respondents about influenza and COVID-19 vaccinations, 80.8% (n.1020) reported receiving both vaccines and 98.3% (n.1241) received the respective vaccines. Additionally, 87.7% (n.1107) of subjects were aware of the possibility of coadministering the two vaccinations. Only 16.6% of the participants obtained information about co-administration from scientific journals or government sites (WHO, CDC, etc.) while 24.6% received information from their general practitioner (GP), pharmacist, or pediatrician ().
Table 3. Univariate (crude OR) and multivariate (adj OR) analysis of factors associated with willingness to receive coadministration of COVID-19 and seasonal influenza vaccines at the vaccination hub of the University Hospital of Palermo, Italy.
The primary reasons for accepting co-administration were trust in official recommendations (41.5%; n.400), reduction in visits to the vaccination center (33.0%; n.318) and concern about the severity of pathologies/enhanced protection against the two viruses (18.7%; n.180) ().
For those unwilling to receive the influenza vaccine, the main reason for refusal was the belief in low circulation of the influenza virus (36.6%; n.30), followed by the perception that the flu is not a severe illness (35.4%; n.29) ().
Those who declined the COVID-19 vaccine primarily cited the assumption that COVID-19 posed no health risk after receiving the booster dose (58.3%; n.21), the belief that the COVID-19’s Omicron variant has no serious and severe effects (19.5%; n.7) and finally, concerns about vaccine effectiveness and safety, respectively, among 13.9% and 8.33% of the respondents ().
As reported in , an increase in subjects that received co-administration of flu and COVID-19 vaccines comparing 2021/22 and 2022/23 season was observed. Indeed, more than half (61.2%; n.737) of the subjects vaccinated received influenza and COVID-19 vaccines in the same session during the 2021/2022 season this finding increased (74.7%; n.944) during 2022/2023 season.
Figure 1. Acceptance and refusal of flu and COVID-19 vaccines coadministration during 2021/2022 and 2022/2023 seasons at the vaccination hub of the University Hospital of Palermo, Italy.
![Figure 1. Acceptance and refusal of flu and COVID-19 vaccines coadministration during 2021/2022 and 2022/2023 seasons at the vaccination hub of the University Hospital of Palermo, Italy.](/cms/asset/facdf493-d2d9-4ef9-8e4d-cb31315fc644/khvi_a_2327229_f0001_oc.jpg)
presents the univariate and multivariate analyses of factors associated with the willingness to receive co-administration of COVID-19 and SIV. The multivariate analysis revealed that factors significantly associated with willingness to receive co-administration of COVID-19 and Seasonal influenza vaccines included being male (Adj-OR = 1.51 (95%CI = 1.27–1.75); p-value <.01); having an age less than or equal to 59 y old (Adj-OR = 2.48 (95%CI = 1.89–3.65); p-value = <.01); being a health-care worker (Adj-OR = 1.66 (95%CI = 1.08–2.57); p-value <.05) and having received both vaccinations in co-administration in the 2021/2022 season (Adj-OR = 41.6 (95%CI = 25.5–67.9); p-value <.05).
Discussion
The main objectives of the present study were to assess the acceptance of co-administering COVID-19 and influenza vaccines, evaluate the knowledge and attitudes surrounding this practice, and understand the reasons for either choosing to receive them together or refusing co-administration of the two vaccines.
In accordance with Italian recommendations and supported by literature data, influenza vaccines do not interfere with the immune response to other inactivated or live-attenuated vaccines. Specifically, co-administering all influenza vaccines with anti-SARS-CoV-2/COVID19 vaccines is feasible.Citation1
The Italian Ministry of Health reiterated the importance of co-administration of the influenza vaccines, including QIVe, QIVcc, QIVa, QIVhd, QIV-LAIV, with other vaccines, including COVID-19 vaccines. In the ‘Prevention and control of influenza: recommendations for the 2022–2023 season’ Annual Circular published the 6th of July 2022.Citation1
A key result of our study was that the majority of individuals who had already received both vaccines in the same vaccination session during the previous season (2021/2022) were willing to repeat the co-administration in the current season. This inclination, derived from patients’ firsthand experiences, appears to align with observations from recent studies suggesting that co-administration of COVID-19 and influenza vaccines preserves the immune response without raising safety concerns, also reducing the need for additional accesses to the vaccination center.Citation13–16
Several studies have previously showed that generally higher vaccination rates were among individuals who consult official websites of Health Authorities, particularly among the younger population.Citation26,Citation27 Our study supports this trend, as most subjects willing to receive coadministration of COVID-19 and influenza vaccines were under the age of 59.Citation28,Citation29
Health-care workers, partly due to their increased perception of disease risk and their inclination to obtain information from official sources, were more likely to undergo COVID-19 and influenza vaccination.Citation30,Citation31
As reported in the fourteenth report on the surveillance of COVID-19 vaccines of the Italian Medicines Agency, susceptibility to COVID-19 infection is equally likely among males and females, but clinical findings reveal that males experience higher severity and mortality from COVID-19 infection.Citation29 Nevertheless, women generally develop more robust innate and acquired humoral and cell-mediated immune responses than men, and this is also reflected in their response to vaccination.Citation29 Women reported more adverse reactions after COVID-19 vaccination, possibly explaining why they were less likely to receive co-administration of COVID-19 and influenza vaccines.Citation29
Some limitations of the present study need to be highlighted. The surveys were primarily conducted during observation period following vaccination at Palermo University Hospital’s vaccination center, and participants were volunteers interested in vaccination, which could introduce potential selection bias.
Additionally, a social desirability bias should be considered since vaccine acceptance was self-reported. This may lead to participants reporting responses influenced by social expectation rather than their true beliefs, potentially overestimating the acceptance of vaccination in general and, in this case, the coadministration of the COVID-19 and influenza vaccines.
In addition, a partial generalizability bias to the general population should be taken into account, due to a high percentage (40%) of respondents that were health-care professionals (HCPs). This could be explained because the vaccination hub belongs to the main University Hospital of Sicilian Region and HCPs represented one of the categories for which seasonal flu and covid vaccination were strongly recommended. At the same time, more than 750 subjects belonging to the general population were enrolled in the study and in the multivariable analysis the adjusted impact of being HCPs in administration acceptance was evaluated by the AAs.
Finally, recall bias may affect the accuracy of reported factors associated with vaccination-related decisions. The clinic-based nature of our sample warrants consideration. While strategically chosen for its relevance to vaccination decisions, it inherently limits the external validity of our findings. The insights garnered may be more applicable to individuals actively seeking health-care services, potentially excluding those less engaged with health-care facilities.
While our study aimed to capture the dynamics and perceptions within a specific vaccination hub’s real-world setting, we recognize the absence of a comparative arm for individuals who did not undergo co-administration. This limitation restricts our ability to draw causal inferences and generalize our findings to the broader population.
Despite these limitations, we believe that our study contributes meaningfully to the existing literature by shedding light on the practical aspects of vaccine co-administration. The observed acceptance rates, attitudes, and experiences provide valuable insights for health-care practitioners and policymakers. Future studies employing a controlled design could further explore the factors influencing vaccine choice and refusal.
Conclusions
The present study demonstrated that, among subjects that usually go to vaccination center in order to receive influenza or COVID-19 seasonal vaccines, a significant majority are willing to receive both the vaccines in the same vaccination session. This inclination was primarily observed in those subjects who had already received both vaccines in co-administration during the 2021–2022 season.
The decision to opt for co-administration during the following season could be likely influenced from the relatively few side effects experienced after administration, which are no more severe than those associated with the single vaccine (influenza or COVID-19) administration.
Furthermore, co-administration reduces the need for multiple visits to the vaccine center, proving especially important during the pandemic period when it was crucial to minimize gatherings and interactions.
Co-administration should become a standard procedure in public healthcare. Already implemented during 2022/2023 season in Italy and in other European countries as a standard recommended procedure, it should further become increasingly common in the upcoming seasons, as COVID-19, similarly to influenza, would become seasonal in its circulation.
Draft Questionnaire.pdf
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Supported in part by an independent research grant from Novavax Inc. The opinions expressed in this paper are those of the authors and do not necessarily represent those of Novavax Inc.
Data availability statement
The data that support the findings of this study are available from the corresponding author, CC, upon reasonable request.
Supplementary material
Supplemental data for this article can be accessed on the publisher’s website at https://doi.org/10.1080/21645515.2024.2327229
Additional information
Funding
References
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