Vaccine hesitancy among paediatric nurses: Prevalence and associated factors

Objective This study describes the prevalence of vaccine hesitancy associated with the Catalan systematic childhood vaccination calendar and some related psychosocial determinants among paediatric primary care nurses in Barcelona (Spain). Methods Cross-sectional descriptive study. In 2017 we invited the paediatric nurses (N = 165) working in Barcelona public primary health centres with paediatric departments (N = 41) to participate. They answered a questionnaire with sociodemographic and behavioural variables: severity and perceived probability of contracting the diseases of the vaccines in the vaccination schedule; safety and protection offered by each vaccine; and beliefs, social norms, and knowledge about vaccines. Outcome variable was vaccine hesitancy, dichotomized into not hesitant (nurses who would vaccinate their own offspring), and hesitant (including those who would not vaccinate them, those who had doubts and those who would delay the administration of one or more vaccines). We performed bivariate analysis and adjusted logistic regression models. Results 83% of paediatric nurses (N = 137) agreed to participate. 67.9% had the intention to vaccinate their children of all the vaccines in the systematic schedule. 32.1% of nurses experienced vaccine hesitancy, especially about the HPV (21.9%) and varicella (17.5%) vaccines. The multivariate analysis suggests associations between hesitancy and low perception of the severity of whooping cough (aOR: 3.88; 95%CI:1.32–11.4), low perception of safety of the HPV vaccine (aOR:8.5;95%CI:1.24–57.8), the belief that vaccines are administered too early (aOR:6.09;95%CI:1.98–18.8), and not having children (aOR:4.05;95%CI:1.22–13.3). Conclusions Although most paediatric nurses had the intention to vaccinate their own children, almost one-third reported some kind of vaccine hesitancy, mainly related to doubts about HPV and varicella vaccines, as well as some misconceptions. These factors should be addressed to enhance nurses’ fundamental role in promoting vaccination to families.


Background
Vaccination is a demonstrably effective, safe, and cost-effective intervention. (1) However, in several high-income European countries, immunization rates of some immuno-preventable diseases such as measles have declined in recent decades, (2) which has contributed to recent outbreaks of this disease. Vaccine Hesitancy (VH) could in part be responsible for this growing global phenomenon. VH de ned as the reluctance or refusal to vaccinate despite the availability of vaccines and threatens to reverse progress made in tackling vaccine-preventable diseases. In 2019, the World Health Organization (WHO) placed VH among the top 10 threats to global health. (3) VH is complex and speci c for each context and type of vaccine. In Europe, some common reasons against vaccination include the lack of con dence in vaccines, in their administration, in the public health services, and in the pharmaceutical industry. (4) In the last decade, social networks and some digital media have contributed to expanding these doubts and to eroding families' trust in health professionals. (5) (6) In the European Union, around 20% of parents report having doubts about vaccinating their children. (7) In France, 36% of parents question the safety of vaccines (8), and, in Spain, controversies are quite similar to those in other countries: for example, the association between the MMR vaccine and autism is not uncommon, as well as the belief that the pharmaceutical industry in uences the public vaccination schedule (9), or, moreover, 8% of Spanish people think that vaccination carries more risks than bene ts. (10) Healthcare professionals still maintain a positive in uence on family's decisions to vaccinate their children. (11) In Spain, 69% of families reported that pediatricians were their most important source of information. (12) In this country, pediatric primary care teams include medical and nursing healthcare professionals. Primary health nurses can administer vaccines without a medical prescription. (13) All vaccines included in the o cial schedule are recommended, not required, so communication between families and nurses is crucial to maintain high vaccination coverages. Pediatric nurses use an important part of their consultation time to this task, except in complex non-routine cases, which are attended by pediatricians. (14) These functions, together with their accessibility, make nurses a key actor in vaccination.
A recent study among pediatric primary care teams in Barcelona found that 25% of the healthcare professionals involved in vaccination had doubts about some of the vaccines on the systematic vaccination schedule. The study found differences between pediatricians and pediatric nurses for many variables, nurses being more negatively associated with VH, and recommended exploring this phenomenon in greater detail. (15) The aim of the current study was to determine the prevalence of VH and to study its associated factors among pediatric primary care nurses in Barcelona (Spain).

Study design and participants
We conducted a cross-sectional study. The study population included all the pediatric nurses working at the 41 public primary care centers in Barcelona with pediatric service in 2017. We included nurses who performed care work and excluded students, residents, and temporary nurses. The universe was 165 nurses.

Data Collection
We collected the information using a questionnaire based in literature, (15), translated into Catalan and Spanish and culturally adapted using the cognitive debrie ng method. (16) Cognitive debrie ng is a process where representatives of the target population actively test the translated questionnaires to determine whether respondents would understand the questionnaire as easily as the primary version would be understood. The self-administered questionnaires were made available to nursing staff between March 2016 and February 2017.
The questionnaire gathered sociodemographic information (age, sex years of experience, offspring), and psychosocial determinants based on theoretical models of behaviour: intention to vaccinate their own children, self-e cacy about answering family questions, perception of the severity and probability of contracting the vaccinable diseases, safety and protection conferred by vaccines on the systematic schedule in Catalonia (17), beliefs, social norms, and knowledge about vaccines, as well as myths and doubts posed to nurses by the families. (18) (19) (20) Variables The outcome variable was VH, a dichotomous variable constructed from the variable on the intention to vaccinate their offspring for each of the 14 antigens (Ag) on the vaccination calendar. We used the intention to vaccinate based on the Theory of Reasoned Action which is a theory of planned behavior, and the integrated behavioral mode. (21) The question was: "If you had a child today, would you agree for them to receive the vaccines on the current systematic schedule?" We coded as "vaccine hesitancy" if the answer was "no", "I have doubts" or "I would do it later" for one or more antigens (Ag), and "non-hesitancy" if they responded otherwise.
In line with the Health Belief Model (22) and based on the results of a systematic review, and its recommendations employing this theory among healthcare professionals (23), we collected data on the participants' perception of the severity and probability of contracting each immuno-preventable disease, and the safety and protection conferred for each Ag in the schedule. We collected the answers on a 5-point Likert scale plus a don't know response. Then, we created dichotomous variables, excluding non-responses, as follows: probability of contracting the disease, "probable/very probable" vs other responses; severity of the illness, "serious/very serious" vs other responses; safety of the vaccine, "safe/very safe/totally safe" vs other responses; and protection conferred by the vaccine, "protective/totally protective" vs other responses. The perception of the severity of HPV infection was not included in the severity section because the question referred to 8-year-old girls or boys and it is understood that at childhood they can neither become infected by this virus nor suffer from cervical cancer.
Answers regarding beliefs, social norms, and knowledge were collected in ve categories and dichotomized into "agreement" or "disagreement" with the most favorable option to vaccination, depending on how the question was stated.

Analysis of data
We carried out a descriptive analysis of the data. We studied the relationship between VH and explanatory variables using the chisquare or Fisher's exact tests. After verifying that the data were normally distributed, we analyzed age and years of experience as continuous variables using the T-Student test. We t logistic regression models using the variables statistically signi cant in the bivariate analysis and adjusted for sex, years of experience and offspring. We computed the adjusted odds ratios (aOR) and their 95% con dence intervals (CI). We compared the models based on the likelihood ratio test and chose the model providing the most information with the least variables.
We analyzed "do not know/did not answer" (DK/NR) responses and the missing values together. Missing values accounted for less than 5%. When the percentage exceeded 5%, data were analyzed by including and excluding them as a category. We found that missing values did not affect the results, so we decided to exclude missing values of the analysis. Statistical signi cance was set at α = 0.05. The analysis was conducted using Stata software 13.0.

Results
83% of the 165 nurses participated in the study. 96.4% of them were women, with a mean age 47.7 years, 72.3% had children, and had an average of 23.8 years of professional experience was (Table 1). Nursing professionals who were hesitant to vaccinate had a low perceived risk of infection for 5 of the 14 diseases in the vaccination schedule (diphtheria, whooping cough, polio, measles and HPV), and a low perception of severity for 7 of them (whooping cough, H. in uenzae b, meningococcal disease, hepatitis A, measles, mumps, and varicella) ( Table 2).
More than 90% of vaccine-hesitant nurses perceived these vaccines to be very safe, except for the HPV vaccine, which was considered to be very safe by 76.5% of the vaccine-hesitant nurses, and by 97.7% of the non-hesitant nurses (p < 0.001). Hesitant nurses had a lower perception of the protection offered by the HPV vaccine, varicella vaccine, and whooping cough vaccines than those in the nonhesitant group. The perception of protection offered by the other vaccines was greater than 90% in both groups (Table 2). Beliefs, knowledge and social norms

Discussion
In our study, one in three pediatric nurses questioned the administration of at least one of the routine vaccines in Catalonia. The vaccines that generated most doubts were those against HPV, varicella, pneumococcus and hepatitis A. VH nurses had a lower perception of the risk of vaccines for some diseases, a lower perception of the bene t of the varicella and HPV vaccines, and generally more unfavorable beliefs about vaccination (e.g. the time of administration or the number of vaccines) than non-hesitant nurses.
Compared with other healthcare professionals in European countries, Barcelona pediatric nurses appear to be less likely to have the intention to vaccinate their offspring on the standard vaccination schedule than professionals in countries like Switzerland (24), where 95% of pediatricians would do so. On the other hand, it has been seen that general practitioners in France are less likely to recommend vaccines to their patients than to their offspring (25). If Barcelona's pediatric nurses would have a similar behaviour, more than 30% of nurses would not recommend vaccines in practice. The vaccines that generate most doubts are those that have been added in the systematic schedule most recently: HPV, introduced in 2008; varicella, in 2016 for infants; and pneumococcus, in 2016.
(26) These changes, and the fact that some vaccines are only recommended in Catalonia, such as that against hepatitis A, can generate suspicion if the reasons for these differences are not well communicated. (4) Despite having been introduced into the calendar in 2008, the vaccine against HPV generates most controversy and misconceptions, as shown by our results on the perception of its protection and safety. Several studies have reported a low perception of the protection offered by the HPV vaccine by parents (20), healthcare professionals (21) and girls (22). This can be related to the perceived scarcity of e cacy studies or a lack of clear information about the infection and the vaccine. (27) The low perception of the safety of HPV vaccine, among vaccine hesitant nurses is consistent with a study that found that primary healthcare professionals had been receiving contradictory information about the effectiveness and e cacy of this vaccine. (28) Another differential factor between hesitant and non-hesitant was the low perception of the severity of immuno-preventable diseases.
This could be related to the fact that primary care nurses do not directly treat these diseases as they are attended by pediatricians and serious cases are referred to the hospital, or, importantly, because these diseases are generally rare. This lack of contact may lead to false beliefs that trivialize vaccination and question the need to vaccinate. Similarly, since 2010, there has been an increase in mild cases of whooping cough, including among children who had been correctly vaccinated. (29) Thus, this could have eroded the perception of effectiveness in vaccines in some nurses.
Many of the beliefs held by vaccine-hesitant nurses highlight mistrust in the vaccination calendar (too many vaccines and administered too early). This aspect suggests limited knowledge about the reasons and timing of vaccination. Moreover, we have found an association between the distrust in pharmaceutical industry, although not with government health authorities, and the nurses' perception about vaccine administration timing. Another study observed that the perceived lack of transparency of administrations could lead to mistrust about changes in the vaccination calendar. (10) Contrary to our assumptions, we observed no differences in knowledge between hesitant and non-hesitant professionals, perhaps because both groups had a high percentage of missing values, especially concerning adjuvants and vaccine preservatives. Some European studies highlight the importance of professionals' lack of knowledge about the components of vaccines and the possible consequences of this unawareness.(30)(31) The composition of vaccines is one of the questions most frequently raised by families, (19) and it is therefore crucial for pediatric nurses to be familiar with these issues, considering their autonomous-role(32) in aspects of vaccination and their close and accessible role for families in primary care pediatrics. Although, in Spain and Catalonia it is compulsory to have a nurse degree to work as a pediatric nurse in primary care, it seems that training in vaccination during the degree is quite basic, as we found that less than a half of nurses reported having enough information about vaccination. Besides, the continuous training of nurses in Spain is optional.
Another factor associated with VH, but in this case as a protective factor, was not having children, which could be because these individuals have not yet had to consider the decision to vaccinate, and may thus assess the risk of these diseases only from a hypothetical standpoint, which is reassessed with better information when having children.It would be interesting to study in more depth the relationship between parenthood and a more favorable attitude to vaccination.
This study has some limitations. Participation was voluntary, which could lead to a selection bias although the percentage of participants was high (> 80%). Individuals who did not participate would likely be even more VH, such that our results could underestimate the magnitude of the problem. The partial face-to-face administration of the questionnaires could introduce a complacency bias in the responses. A further limitation is that data were collected for a speci c period, 2016-2017, so our results on VH, which is known to vary according to place, time, and context, (33) may not re ect behaviors before or after that period. Therefore, the results and conclusions of this study may not necessarily apply to other countries or even to other territories in Spain. Even though, some strengths arise, this study accessed to all the pediatric nurses of CAP in Barcelona and allowed to assess the status of a complex multifactorial phenomenon and collected information on the poorly understood issue of VH in pediatric nursing. (13) Our results highlight four factors associated with VH that could be used to compare our context with other populations, and that should be addressed.

Conclusions
Although most pediatric nurses would vaccinate their own children, almost one third display some kind of vaccine hesitancy, mainly related with doubts about HPV and varicella vaccines, as well as some misconceptions. These factors should be addressed to enhance their fundamental role in promoting vaccination among families.
Abbreviations VH Vaccine Hesitancy

Declarations
Ethics approval and consent to participate The study 2018/7790/I was approved by the ethics committee of the CEIm-Parc de Salut MAR of Barcelona. The study was conducted in accordance with the principles of the Declaration of Helsinki. All participants in the survey provided signed informed consent.