Background

The potentially deadly coronavirus disease 2019 (COVID-19), which mostly affects the respiratory system, is caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). COVID-19 exhibits recognized but varying morbidity and mortality patterns [1, 2]. Besides triggering a devastating economic crisis [3], the COVID-19 pandemic affected every aspect of life [4,5,6,7]. On March 11, 2020, the World Health Organization (WHO) declared COVID-19 as a worldwide pandemic [8]. On October 25, 2023, approximately 771.5 million cumulative cases and 6.9 million deaths due to COVID-19 were reported globally. In Egypt, 516,023 cases of COVID-19 and 24,830 deaths have been reported so far [9]. Egypt adopted additional public health and societal measures to combat the pandemic in addition to mass vaccination [10]. Since January 24, 2021, Egypt has distributed 112.6 million doses of COVID-19 vaccines, equaling nearly 110.1 total doses administered per 100 population [9]. In an effort to expand the coverage of vaccination in rural areas, including children over 12 years of age, the Egyptian Ministry of Health and Population (MOHP) has initiated a proactive approach. They have deployed mobile teams to regions with low vaccination rates, bolstered by the support of healthcare workers [11].

Studies have indicated that the viral load in the nasopharynx of children is equivalent to or greater than that in adults, although the symptoms in children are less severe than those of adults [12]. Children may play a crucial role in transmitting the virus since they must go to school and other regular gatherings. Children with malignancies, hematological disorders, neurological conditions, heart diseases, neonates, and other specific medical conditions represent a high-risk group vulnerable to SARS-CoV-2 infection. When developing vaccination strategies for young people, it is crucial to include and prioritize these particular groups [13].

Due to its safety, immunogenicity and effectiveness, vaccination against SARS-CoV-2 has been recognized as a critical approach to prevent and reduce the risk of infection, particularly emerging variants of the virus [14, 15]. However, a notable obstacle to the immunization of children has emerged, namely parental vaccine hesitancy (VH). The phenomenon of VH among parents poses a significant challenge in achieving widespread vaccination coverage, even in the face of effective vaccines [16]. VH is listed among the top 10 threats to global health [17]. It is defined as a “delay in the acceptance or refusal of vaccines despite their availability” [18]. The safety and probable side effects of COVID-19 vaccination are apprehensive of many parents, which could raise their VH [19]. Misinformation and false information concerning COVID-19 can have a harmful influence on individuals' attitudes toward vaccination [18, 20]. The well-known questionnaire "Parent Attitudes about Childhood Vaccines" (PACV) may be effectively used to examine parental COVID-19 VH. The PACV survey has been shown to be useful in detecting anti-vaccination parents and predicting future VH [21, 22]. The PACV has been proven to be externally valid as well [23].

This study hypothesized that a substantial proportion of parents with children with chronic diseases can demonstrate VH towards COVID-19 vaccination. To enhance the effectiveness of policies and healthcare strategies aimed at controlling the pandemic, it is imperative to prioritize an understanding of parents' intentions regarding their children's vaccination and the factors that influence these decisions. By assessing the extent of parental VH and identifying its key determinants, we can take significant steps toward improving vaccine acceptance and strengthening population immunity. Therefore, the objective of this study was to evaluate parental VH among Egyptian parents of children with chronic diseases with respect to the vaccination with COVID-19.

Methods

Study design and settings

This multicenter cross-sectional study was conducted in 3 governorates (Alexandria, Cairo, and Menoufia). Parents were recruited from the outpatient clinics of El-Raml Pediatric Hospital (MOHP), Alexandria, Alexandria Main University Hospital (AMUH) for Maternity and Children (El-Shatby), Al-Galaa Teaching Hospital, General Organization for Teaching Hospitals and Institutes (GOTHI), MOHP, Cairo, and Pediatric Department, Faculty of Medicine, Menoufia University, Menoufia from May 1st till December 15th, 2022.

Target population and eligibility for participation

Parents or guardians of children between the ages of 3 and 12 who have chronic diseases and receive medical services from outpatient clinics in the designated study settings were invited to participate in the study. The recruitment process used the simple random technique, and these parents or guardians were asked to complete the study questionnaire. The study excluded children with terminal diseases or advanced severe comorbid diseases. Furthermore, parents or guardians under 18 years of age and those with mental disabilities or communication difficulties were excluded from the study.

Sample size and sampling technique

Based on a previous study conducted in Egypt, the VH among parents of children with cerebral palsy was 70.0% [24], the minimum sample size required to evaluate the VH of parents was 323 assuming the margin of error = 5, power = 80.0% and design effect 1.

Questionnaire of data collection

Parents of children with chronic conditions were interviewed in person by trained physicians. There were four sections in the questionnaire. The age, sex, education level of the parents, the number of children, the relationship with the children, the type of employment (i.e., government, private or jobless), health insurance coverage and income level (i.e., not enough, on a loan and cannot pay back; not enough, on a loan but can pay it back; enough; or enough and saving) were included in the sociodemographic section. The second section included questions about the history of chronic disease, the history of COVID-19 infection, vaccination status (full vaccination, receiving all COVID-19 primary series doses), partial vaccination, not receiving any doses of vaccine, receiving booster dose, receiving booster dose at least two months after primary series doses), reasons for refusal of administration or completion, and sources of information on COVID-19 vaccines. Characteristics of the children were described in the third section (i.e., child age, sex, previous vaccination history and history of chronic diseases). The validated Arabic translation of the PACV survey was included in “Discussion” section [25] (Supplementary file S1). The calculation of the total PACV score was explained elsewhere [21]. Parents who scored 50 or above were categorized as hesitant, while those who scored below 50 were non-hesitant.

Statistical analysis

Statistical Package for Social Sciences (SPSS) software (version 26) was used to handle, display, and perform statistical analyzes. Parental VH toward immunizing their children with COVID-19 vaccination was the primary outcome of the present study. Descriptive statistics were used to present sociodemographic data from parents and their chronically ill children, with measures such as mean and standard deviation for numerical data and frequency distribution presented as number and percentage (percent) for categorical variables. The Mann-Whitney U test (non-parametric test) was used to determine whether there were differences in the distributions of the two groups when the data were not normally distributed, and the assumption of t-test was not met. A ranked-based nonparametric test, the Kruskal–Wallis H test (also known as the "one-way ANOVA on ranks") was used to assess if there are statistically significant differences between three or more groups of an independent variable. A post hoc test was performed to determine which specific groups differ from each other. Independent variables with a p-value of less than 0.20 in the bivariate analysis were retained and incorporated into a multilinear regression analysis to confirm their association with parents' intention to vaccinate their children. We checked for the following assumptions of the model linearity, independence, homoscedasticity, normality of residuals, and no perfect multicollinearity. Findings with a p-value less than 0.05 were considered significant.

Results

In this study, we enrolled 527 caregivers, 55.4% of them were aged 30–39 years, 85.2% were females, 48.0% were from Alexandria, 81.6% were mothers, 85.4 had one child, 77.0% had high school education or less, 68.5% were not employed, 93.5% were non-HCWs, 45.9% self-reported enough monthly income, 38.7% had elders as a family member, and 37.1% had family size of 4 or less (Table 1).

Table 1 Characteristics of parents of children with chronic diseases who were surveyed regarding their hesitancy toward COVID-19 vaccination (N = 527)
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COVID-19 related history

Table 2 shows that 30.0% of the parents had a prior SARS-CoV-2 infection, 47.4% did not report such an infection, and 22.6% were uncertain about their previous infection status. Regarding COVID-19 vaccine status: 11.0% of the respondents had taken all three doses (primary serious and booster dose) of the vaccine, 28.3% did not want to take the vaccine at all, 7.2% expressed their desire to take the vaccine but had not scheduled for it yet, 21.6% had taken the first and second doses and were awaiting the booster dose, while 16.3% had taken the first and second doses but chose not to take the booster dose, 7.8% had taken the first dose and were waiting for the second, and 7.8% took the first dose but refused the second dose.

Table 2 COVID-19-related history and history of chronic diseases among parents and gurdians of children with chronic diseases
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The reasons for not completing the COVID-19 vaccination schedule were as follow: 46.4% indicated it was not applicable (already took the three doses, does not want to take the vaccine, or scheduled for the first dose), 29.4.% were waiting for the next dose, 3.2% mentioned the unavailability of the vaccine, and 21.8% refused to complete the vaccination. A small percentage mentioned that they were pregnant or lactating (0.9%), had autoimmune diseases (as rheumatoid arthritis and systemic lupus) (0.2%), and other reasons (2.7%).

Among those who refused vaccination, the table provides insight into their reasons. Fear of having COVID-19 after vaccination (53.0%), fear of side effects (67.1%), non trust in vaccine efficacy (65.1%), non trust in available vaccination (14.0%), and insufficient information about the vaccines (11.4%) were the main factors mentioned. The data reveals that 46.9% of the respondents reported having a chronic disease such as diabetes mellitus (19.4%), hypertension (32.8%), respiratory diseases (bronchial asthma and chronic obstructive pulmonary disease (COPD)) (34.0%), rheumatic and immunogenic diseases (16.6%), motor disabilities (3.2%), cardiac diseases (8.5%), renal and hepatic diseases (4.4%), while 53.1% did not have any chronic disease.

The survey participants got information on COVID-19 vaccination from a variety of sources. Commonly mentioned sources included television and radio (69.8%), family and friends (23.8%), and social media (35.3%). Some respondents also relied on books and research (2.0%), online websites (11.2%), and family physicians (1.8%) (Fig. 1).

Fig. 1
figure 1

Sources of information of the study participants about COVID-19 vaccination

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Characteristics of studied children

The median age of the children was 6 years, ranging from 3.0 to 12.0 years, 40.0% of the children were females, 6.3% had a confirmed COVID-19 infection, 76.9% did not have COVID-19, and 16.9% were unsure of their COVID-19 status, the most common chronic disease was respiratory disease, affecting 88.6% of the children, and 86.9% of the children received compulsory vaccination as mandated by the MOHP, 22.6% received seasonal flu vaccination (Table 3).

Table 3 Sociodemographic characteristics of studied children
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Regarding child vaccination against COVID-19, 59.6% of the respondents rejected vaccination, while 40.4% accepted it. Respondents who accepted vaccination were further asked about the type of vaccine they preferred. AstraZeneca (1.5%), Pfizer (12.1%), Johnson (12.1%), Sinovac (1.7%), Sinopharm (12.1%), Moderna (0.9%) were the preferred vaccines. Of the participants, 59.6% were unsure of the type of vaccine (Fig. 2).

Fig. 2
figure 2

a Parental attitude about vaccination of children against COVID-19 (b) preferred type of vaccine

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Study participants’ characteristics across intention to vaccinate children variables.

As shown in the bivariate analysis, the site of data collection was significantly associated with PACV score, with AMUH Hospital showing a statistically significant higher PACV score, (median = 43.33) compared to Al-Galaa Hospital or Menoufia Hospital as seen in the pairwise comparative data analysis (Supplementary file S2), p < 0.001. Residence influenced the intention of vaccination, particularly for individuals from Behira (PACV medians = 43.33) compared to those from Cairo, Alexandria and Giza, p < 0.022, p < 0.007, p < 0.015 respectively. Occupational and education were significantly associated with parental attitude towards vaccination. Governmental employees had lower PACV (median = 26.67) compared to those who worked in the private sector and were not employed (median = 36.67, 36.67, p < 0.001). Higher parental education level was associated with a lower PACV score, especially higher education (PACV median = 36.67) compared to university education (PACV median = 33.33, p < 0.036). Participants with governmental health insurance had the lowest PACV (median = 26.67) compared to those with the uncovered category (median = 36.67), this deference was statistically significant (p < 0.001). Distinct vaccination intention was evident between health and non-health sector workers (median PACV was 26.67 vs 36.67 respectively, p = 0.032). Furthermore, income groups also showed varying intentions to vaccinate their children, higher income level was significantly associated with lower PACV (p < 0.001). Previous COVID-19 status was significantly associated with PACV score. Participants who were "not sure" showing distinct intention (PACV median = 40.00) from "yes" (PACV medians = 33.33), p < 0.037. Equally important, various COVID-19 vaccine statuses yielded varying intentions, with those who “Refusal vaccination” (PACV median = 40.00), vs “Took the first and second doses and is awaiting the booster dose” (median = 30.00), “Took the first dose and is awaiting the second” (median PACV = 30.00), and who “Took the three doses” (median PACV = 33.33), p < 0.001. While not statistically significant, there's a subtle variation in intent between participants with female (median PACV = 33.33) and male children (median PACV = 36.67), p = 0.101. Furthermore, although not statistically significant (p = 0.091), slight intention differences appeared among various child history of previous COVID-19 infection. Finally, the presence of respiratory disease in children had a statistically significant association with hesitation to vaccination among parents (PACV median = 36.67 vs 33.33, p = 0.017) (Table 4). The supplementary file (S2) contains the post-hoc analysis of the significant findings.

Table 4 Participants’ characteristics across intention to vaccinate children variables
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Predictors of PACV score

Multiple linear regression was used to test if the following variables [health care worker, age, governorate, setting, education, working, health insurance, income, elderly presence, previous COVID 19, COVID-19 vaccine status, child vaccination against seasonal influenza, and the number of children in the household] significantly predicted [PACV score]. Overall, regression was statistically significant (R2 = 0.31, p < 0.01). The predictors of the PACV score were governorate, Menoufia (β = 11.30, 95%CI [5.32, 17.27], p < 0.001), study setting, Menoufia University Hospital (β = -20.07, 95%CI [-25.40, -14.75] and El-Raml Hospital (β = -10.74, 95%CI [-14.50, -6.98], p < 0.001), income; not enough loans repaid (β = 3.18, 95%CI [0.54, 5.82], p = 0.018) and not enough loans not repaid (β = 3.57,95%CI [0.08, 7.07], p = 0.045). The variable "COVID-19 vaccination status" indicates that various categories had significant effects on the outcome. For example, taking the "first and second doses and awaiting the booster dose" (β = -9.54, p < 0.001) and "three doses" (β = -8.31, p < 0.001) had significant negative impacts on the PACV compared to the reference category (Table 5).

Table 5 Multivariate analysis of the predictors of PACV score
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Discussion

With few therapeutic options for COVID-19, vaccine development has been accelerated around the world. COVID-19 vaccines are a major public healthcare achievement of the twenty-first century, and vaccines have apparently decreased the disease’s severity and progression. However, the success of COVID-19 vaccines is dependent on herd immunity. VH has been identified as a major impediment to achieving herd immunity. This study examined parents' intentions to vaccinate their children with chronic diseases aged 3.0 to 12.0 years old, as well as the contributing sociodemographic, health-related, and behavioral factors.

Main study findings

A survey revealed that 59.6% of the respondents refused COVID-19 vaccination for their child, while 40.4% accepted it. The preferred vaccines were AstraZeneca, Pfizer, Johnson, Sinovac, Sinopharm, and Moderna. Information on COVID-19 vaccination was obtained from various sources, including family, friends, social networks, television, radio, books, online websites, and family physicians. Multilinear regression model showed that factors such as study location, governorate, income, parental COVID-19 vaccine status significantly influenced the PACV score.

Interpretation of the main study findings

We found that almost two-thirds of parents (59.6%) refused to vaccinate their children despite 11.0% of the parents surveyed having completed their vaccination schedule (received the primary series and booster vaccine). In a similar vein, numerous studies conducted in Egypt have reported low COVID-19 vaccination rates among children [24, 26]. Reports from Egypt revealed that vaccination coverage among individuals aged over 5 years was comparatively low, with only 14.0% of the population receiving booster doses. This percentage was significantly lower than the global vaccination coverage, which is reported at 31.4% [27]. A study conducted at the National Liver Institute in Egypt found that 81.5% of parents of children with chronic liver disease hesitated to vaccinate their children [26]. Another study conducted in Egypt found that 70.0% of parents of children with cerebral palsy were hesitant to administer the COVID-19 vaccine [24]. On the other hand, Drouin et al. [28] reported a higher intention of parents (64.0%) to vaccinate asthmatic children in Saudi Arabia. The low coverage of COVID-19 vaccination in Egypt may be attributed to uncertainty about vaccine effectiveness, lack of trust in vaccine due to rapid vaccine production, lack of information, and concern about vaccine side effects [29, 30]. An additional explanation from a psychological perspective, particularly involving beliefs in conspiracy theories, points to a fear of infertility as one of the side effects of vaccination among the population residing in the Middle East region [31, 32]. Despite some parents' hesitancy, it is promising to see that the majority of parental concerns focused on the vaccine's safety and efficacy. These concerns can be addressed to some extent by time and announcing the pharmacovigilance reports concerning the vaccination of children, which are expected to show high safety and efficacy in children.

Determinants of vaccination hesitancy

Sociodemographic factors

In our study, we found that several socioeconomic variables, including parents’ residence, level of education, working sector, and a previous history of infection with COVID-19; had a significant impact on parents' willingness to vaccinate their children. However, factors like gender of the respondents and age were not significant in bivariate or multivariate analysis. These significant factors could be explained by a spike in anxiety, depression, and stress during the pandemic [33]. Furthermore, in bivariate analysis, parents who had elderly family members living with them at home were more likely to express hesitancy. Interestingly, this variable was not significant in multivariate analysis. This hesitancy may be due to their concerns about their elders' well-being and their heightened vulnerability to infections resulting from age-related changes in the immune response [34].

Several studies have shown that parental VH is influenced by their monthly income [20, 35, 36]. In the current study, income level was significantly associated with PACV score in bivariate and multivariate analysis. Parents in our study whose income was not enough and who tend to get unrepaid loans had 3.57 times higher PACV score compared to those who had enough income. In research conducted among parents of children aged 5 to 11 years in Saudi Arabia, those with a monthly household income of more than 10,000 Riyal were significantly more likely to vaccinate their children against COVID-19 [37]. Other studies in the United States, England, and Bangladesh supported this finding [20, 35, 36].

Parents’ vaccination status

In the current work we found that vaccination of parents against COVID-19 significantly decreased the PACV score, almost 10 times more than those who were not vaccinated. Likewise, Choi et al. [38] indicated that the Chinese population who completed their vaccination program had a higher intention to vaccinate their children. Elkhadry et al. [26] reported that parents’ trust had a direct negative association with their reluctance to vaccine children. Furthermore, Durmaz et al. [39] found that Parents who are VH, as determined by the PACV scale, have a less positive attitude toward the COVID-19 vaccine.

These theories met the debates about the safety margin of specific types of vaccination, such as mRNA vaccines [40]. Plenty of adverse events following immunization (AEFI) have developed. The Uppsala Monitoring Centre for pharmacovigilance recorded 2.9 million reports during 2021 and an additional 1.7 million reports in 2022 [41]. Despite evidence argue the safety of mRNA vaccine on the human fertility and maternal health [40, 42, 43]. In the last two years, Mansour et al. [44] reported menstrual irregularities in women subsequent COVID-19 vaccination with poorly understood mechanisms. Eslait-Olaciregui et al. [45] indicated that COVID-19 vaccinations has an epidemiological linkage to neurological disorders such as cerebral venous sinus thrombosis, stroke, convulsions, Guillain-Barré syndrome, facial nerve palsy, and other neurological diseases. Khalid et al. [46] reported high rates of anaphylaxis to the mRNA vaccines in young to middle-aged females. COVID-19 vaccination was also associated with higher risks of multisystemic inflammatory syndrome in children (MIS-C), myocarditis, and pericarditis in adults and children [47,48,49,50]. As a result, health authorities should proactively develop intervention programs aimed at delivering health messages through widely used communication channels to reassure parents about the safety and effectiveness of COVID-19 vaccination. Decision-makers need to actively combat rumors and address infodemics that could potentially influence parents' attitudes toward vaccination.

Strengths and limitations

This study offers numerous strengths that contribute to its quality and reliability. First, to our knowledge, this is the first study to assess VH in children with different chronic diseases in Egypt. Second, conducting the study multicentrally and at different socioeconomic levels supports its external validity. Finally, using valid questionnaire and random sampling method allows the generalization of the findings and provides robust evidence. However, there are a few limitations to consider in our study. First, the cross-sectional design of the study made it not accessible to measure causality between the variables studied, more cohort studies are required to detect changes in VH over time. Second, recall bias among respondents when remembering the vaccination history of their children may be present.

Conclusion

In conclusion, almost two-thirds of our sample were hesitant to vaccinate their children. Parents' willingness to vaccinate their children was significantly influenced by socioeconomic factors such as their parents' residence, level of education, working sector, and history of COVID-19 infection. That requires more attention from the decision-makers to pay attention to the causes of VH and point out the significance of awareness programs for parents and caregivers on the importance of vaccination campaigns to minimize the complications of SARS-CoV-2 disease in children with chronic diseases. In future research, the emphasis should be placed on community engagement initiatives that incorporate local leaders and family physicians to promote open discussion and build trust. In addition, interventions should be designed with income considerations, ensuring affordability and accessibility across all socioeconomic groups. Tailoring strategies to specific governorates are crucial for addressing region-specific concerns. Encouraging parental participation and using family networks can play a crucial role in increasing confidence in the vaccination process, thus contributing to increased rates of COVID-19 vaccination among children and fortifying broader public health efforts.