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Research Paper

Vaccination coverage among school children in Western Greece from 2016 to 2019

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Pages 4535-4541 | Received 21 May 2021, Accepted 04 Aug 2021, Published online: 02 Sep 2021

ABSTRACT

Vaccine hesitancy has increased, which has an effect on vaccine uptake. The aim of our study was to investigate childhood vaccination coverage in Western Greece and identify factors affecting it. We also aimed to assess trends in childhood vaccination coverage nationwide. A cross-sectional study was conducted (2016–2019) in all the primary schools in Patras, the third largest city in the country. Data collection was undertaken using child vaccination booklets and questionnaires on socio-demographics. Multiple regression analyses were performed to evaluate relevant associations. We also performed a systematic review of published data on childhood vaccination coverage in Greece during the last two decades. Data for 1657 children was collected and 371 questionnaires were returned. High vaccination coverage (>90%) was observed for the majority of the vaccines. For the pneumococcal conjugate vaccine (PCV), coverage with four doses, as recommended at the time of study, was suboptimal (39.2%). For human papillomavirus vaccines and the meningococcal serogroup B vaccine, full vaccination coverage was 2.6% and 6.5%, respectively. No association with socio-demographics was found for vaccines with high coverage. For PCV the number of doses given was related to Greek nationality (β = 0.185, p < .001) and parental employment status (β = −0.115, p = .043). Compared to previous studies (16 eligible), there was a trend toward higher coverage. Public health interventions should focus on increasing vaccine uptake of specific vaccines among populations with particular characteristics. A national network recording vaccine coverage is urgently required in the country to monitor vaccine uptake and assess trends over time.

1. Introduction

According to the World Health Organization (WHO), vaccination prevents up to three million deaths worldwide each year.Citation1 Immunization against infectious diseases represents one of the most cost-effective measures for public health and is recommended by international guidelines. The National Immunization Program (NIP) in Greece is regularly updated by the National Vaccination Committee and was last modified in 2020.Citation2

Vaccine hesitancy has increased during recent years.Citation3–5 The majority of vaccine-hesitant parents question safety and effectiveness of vaccinations. Amongst other concerns is an alleged correlation between autism and the measles, mumps, and rubella (MMR) vaccine.Citation3–5 A recent study on vaccine confidence in 67 countries indicated that Greece was the 8th country in terms of vaccine-safety skepticism.Citation4,Citation5

An extensive study on vaccination coverage was conducted in 2012 by the Greek Center for Disease Control and Prevention in primary school children and found that vaccination coverage in the country is high and has improved compared to a similar study in 2006.Citation6,Citation7 However, some booster doses recommended for the 4-6-year-old age group were not given and MMR coverage with 2 doses by the age of 6 was only 83%.

A more recent study conducted on 432 preschool children in Thessaloniki, the second largest city in Greece, in 2017, showed full coverage (>90%) for the majority of vaccines diphtheria-tetanus-acellular pertussis and the inactivated polio vaccine (DTaP-IPV), Haemophilus influenzae type b (Hib), hepatitis B (HBV), measles-mumps-rubella (MMR), and varicella (VAR)), except for the pneumococcal conjugate vaccine (PCV), meningococcal serogroup C (MCC) and the hepatitis A (HAV) vaccine.Citation8 In addition to the above studies, a cross-sectional study of 2539 preschool children conducted in Athens, the capital of Greece, in 2013, also concluded that there was an overall high coverage, yet delayed vaccination was observed for HBV, PCV and MCC.Citation9

Whilst the above studies provide valuable information concerning vaccination coverage, more data is required to assess the current situation in the country, as well as trends over time. It is of note, that childhood vaccination coverage is not monitored on a regular basis in the country and a national recording system does not exist. The aim of our study was to investigate vaccination coverage in all primary schools in Patras, the third largest city in Greece, and to evaluate factors that might affect it. We also aimed to assess trends of childhood vaccination coverage in the country by summarizing the available data in the field over the last two decades.

2. Materials and methods

2.1. PART 1: literature review on childhood vaccination coverage in Greece

In order to investigate trends in relation to vaccination coverage in Greece, we reviewed all published literature over the last two decades. We identified eligible studies using the electronic database PubMed and the following keywords (abbreviations and full names) and combinations of them: vaccination coverage, Greece, children, students, DTaP, MMR, MCV, PCV, HPV, 4CMenB, meningitis B, immunization, vaccination. Reference lists within included articles which were further reviewed for additional sources. We identified 116 potentially relevant articles and after the removal of duplicates and the exclusion of articles based on title and abstract screening, we further accessed 36 articles for inclusion. We eventually included 16 articles in the systematic review as per PRISMA guidelinesCitation10 .

2.2. PART 2: vaccination coverage in Patras (2016-2019)

2.2.1. Study population

We performed a cross-sectional study on vaccination coverage between 2016 and 2019 among school-aged children attending the 5th and 6th grades of state primary schools (≥10 years old) in the metropolitan area of Patras and its suburbs. All state schools (57) were enrolled in the study with 2331 students eligible for participation, 1305 attending the 5th grade and 1026 attending the 6th grade. Data for 1657 was collected, with 922 of them attending the 5th grade and 735 the 6th grade.

2.2.2. Data collection instruments

The data collection instruments used in our study were i) the school registry, in order to select basic information about the number of classes and pupils, ii) the vaccination record booklet, so as to collect information on the immunization status of each child after parental consent and iii) anonymous voluntarily self-administered questionnaires on socio-demographic characteristics completed by parents. As for the vaccination booklets, parents were asked to bring them to our scheduled school visits for data extraction. Information about gender, date of birth, types and number of vaccines doses, was collected and recorded anonymously in a Microsoft Excel database. Data was collected from September 2016 to December 2019. Parents were also given a short questionnaire written in Greek consisting of eight questions about their demographic characteristics (age, education level, employment status etc.) and the child’s nationality, gender and date of birth.

2.2.3. Definition of complete vaccination coverage

We considered – fully vaccinated children to be those who had received all the recommended doses as per the 2015 NIPCitation11 . More specifically, the recommended doses for each vaccine were i) for diphtheria-tetanus-acellular pertussis (DTaP, TdaP) five doses by the age of 6 years, ii) for inactivated polio vaccine (IPV) four doses by the age of 6 years, iii) for HBV three doses by the age of 18 months, iv) for Hib four doses by the age of 18 months, v) for MMR two doses by the age of 6 years, vi) for HAV two doses by the age of 3 years, vii) for VAR two doses by the age of 6 years, viii) for PCV four doses by the age of 18 months, ix) for MCC one dose by the age of 15 months, x) for Human papillomavirus vaccines bivalent/quadrivalent or nine-valent (HPV) two doses by the age of 12 years, xi) for Bacillus Calmette–Guerin vaccine (BCG) one dose by the age of 6 years. The meningococcal serogroup B vaccine (4CMenB) was, at the time of the study, (as well as at present) only reimbursed for high-risk children (asplenia, complement deficiency, eculizumab therapy). It should be noted that in Greece, if parents wish to vaccinate a non-high-risk child with 4CMenB, they can do so, but have to bear the cost of all the doses themselves.

2.2.4. Statistical analysis

Statistical analysis was performed using IBM SPSS Statistics 25.0 software (IBM Corp, Armonk, NY). Multiple logistic regression models were constructed to identify independent factors in order to assess the impact of parental socio-demographic characteristics on full vaccine coverage. We performed a separate analysis for PCV and 4CMenB vaccine uptake (multiple linear and logistic regression). All tests were 2-tailed and the level of significance was set to 0.05 for all analyses.

2.2.5. Ethical approval

Ethical approval was obtained from the Hellenic Ministry of Education and Religious Affairs, the Regional Steering Committee of the University of Patras and the Regional Directorate of Primary and Secondary Education of Western Greece (decision on the protocol signed and dated 23.09.2016).

3. Results

3.1. PART 1: literature review on childhood vaccination coverage in Greece

The 16 studies that were included in our systematic review are listed in two Tables (available as supplemental material Tables S1 and S2). Twelve out of the sixteen studies described vaccination coverage for all recommended vaccines and found overall increasing vaccination uptake during the last two decades in the country. In particular, a study conducted in 2001–2002 including 493 students between 6 and 16 years concluded that only 54% of them were fully vaccinated for DTP, IPV, MMR, BCG and HBV.Citation12 In another study, conducted in 2004–2005 including 3878 pupils (mean age: 6.76 years), 63.9% had received all the recommended doses and vaccines but only 52.1% had an age-appropriate vaccination status.Citation13 According to the latest national study in 2012 on 1046 school children (mean age: 6 years), more than 90% of them have received all the suggested doses for DTaP-IPV, 83% for MMR and 82% for HAV.Citation6 Moreover, while approximately 80% of the children had received 4 doses the Hib vaccine and 74% 2 doses of VAR, only 36% had received all three doses of the HBV vaccine and only 15% all three doses of MCC up to the age of two. A more recent study conducted in Athens, between 2010–2011 including 731 preschool children, showed a satisfactory immunization coverage for DTaP-IPV, Hib, HBV and first MMR dose coverage exceeding 90%.Citation14 Similarly, another study conducted in Athens between 2009 and 2011 including 1667 infants indicated an optimal vaccination coverage for the majority of vaccines.Citation15 Οn the other hand, during the same period, in a study of 1005 adolescents aged between 11 and 19 years, only 22.7% of them were completely vaccinated for Td/Tdap, MMR, HBV, OPV/IPV, MenC and HAV.Citation16

It is of note that one study reported on PCV vaccination coverage (15,9% fully vaccinated by 20 months of age),Citation17 one study focused on 4CMenB (28,9% fully vaccinated)Citation18 and two studies provided data on about the vaccination coverage of HPV (8,9% and 25,8% fully vaccinated respectively).Citation19,Citation20 Supplemental Table S1 lists the studies that report on vaccination coverage based on data collected during childhood, whereas those in which childhood data were extrapolated from adult studies are presented in supplemental Table S2.

3.2. PART 2: vaccination coverage in Patras (2016-2019)

Out of 2331 eligible children, 1657 children were enrolled (participation rate 71.09%) with a median age of 11.44 years (range 10–14 years). presents the socio-demographic characteristics of the population studied. The vaccination coverage for each vaccine is shown in , whereas provides the results of stratified analysis per year. The highest full coverage was observed in DTaP-IPV, MMR, MCC (>98%) and HepB (>97%). However, we also observed a high variability of PCV doses given. Although the NIP at the time of the study recommended vaccination with three doses in the first year of life and a fourth dose after the first year (i.e., a total of four PCV doses), only 39.2% (649) of the children in our cohort were completely vaccinated with four doses. As far as the rest of the children were concerned, 7.1% (117) of them have not had any dose of the PCV vaccine, 18.5% (306) have received only one dose, 14.7% (244) two doses and 20.6% (341) three doses. Moreover, 83% (668) of the girls have not received the first dose of the HPV vaccine, 14.4% (116) of them had received one dose of HPV, while only 2.6% (21) were fully vaccinated.

Table 1. Sociodemographic characteristics of children in our cohort (n = 1657) and of parents that returned the questionnaire (n = 371)

Table 2. Vaccination coverage expressed as percentages with correspondent number of children in parentheses {% (n)} for all vaccines

Table 3. Trends in full vaccination coverage from 2016 to 2019 expressed as percentages with corresponding number of children in parentheses {% (n)}

3.3. Associations of vaccination coverage with socio-demographics

Out of 1657 children, 371 questionnaires were completed by their parents (response rate 22.4%). The analysis of vaccination coverage showed no differences between the coverage of those children whose parents had returned the questionnaire and those whose parents had not (data not shown). Multiple logistic regression analysis did not reveal any association between socio-demographic characteristics and complete vaccination coverage for the vaccines with a high uptake. For PCV, for which vaccination coverage with the recommended four doses was low, further analysis was performed. In a multiple logistic regression analysis, we found that both parents being employed (adj. OR = 1.65 (1.02–2.69)) and of Greek nationality (adj. OR = 7.75 (1.00–59.9)) were factors that were associated with PCV vaccination uptake with four doses. In a multiple linear regression analysis, we found that Greek nationality (β = 0.0185, p < .043) and unemployment (β = – 0.115, p = .043) were factors associated with the total number of PCV doses given (). shows a boxplot describing the number of PCV doses stratified per parental unemployment. The same analysis was performed for 4CMenB, for which the immunization uptake was also low. In a multiple logistic regression analysis, we found that nationality (adj OR = infinite; all with non-Greek nationality have incomplete 4CMenB coverage) and paternal age (adj OR = 0.91 (0.84–0.99)) were factors influencing 4CMenB immunization coverage. In a multiple linear regression model () we found that Greek nationality was positively correlated with the number of doses for 4CMenB vaccine (β = 0.102, p = .054).

Table 4. Factors that determine the number of PCV and 4CMENB doses

Figure 1. Number of PCV dosed stratified per parental unemployment.

(Comparisons were performed using Kruskal-Wallis with Dunn’s post-hoc test).
Figure 1. Number of PCV dosed stratified per parental unemployment.

4. Discussion

In this study, one of the largest conducted in Greece in the last decade, we assessed vaccination coverage among 1657 school-aged children living in Patras, the third largest city in Greece.

4.1. Vaccination coverage

Overall, we found adequate vaccination coverage for the majority of recommended vaccines (DTaP-IPV, HBV, MMR, Hib, HAV, MCC and VAR). Compared to previous studies in the country, our population was older and coverage for all vaccines was higher, which indicates an increasing compliance with the NIP, but there is certainly space for further improvement, especially regarding certain vaccines.Citation6,Citation8,Citation9,Citation13,Citation14 It is also worth mentioning at this point that previous studies have demonstrated that, despite good overall coverage in the first years of life, low booster uptake was observed in adolescence.Citation16 The latter might indicate that infants and toddlers may have better vaccine coverage as parents are more worried about their general health and consult their pediatrician more often. As the child grows older, these visits become less frequent and booster doses in adolescence might be missed, as there is no central vaccine reminder system in the country. In our study, though, we observed better overall vaccine coverage with regards to boosters, which could be the result of continuous public health efforts in the field over the years.

Nonetheless, we found suboptimal coverage for the PCV, BCG and HPV vaccines. Regarding BCG, the low coverage could be explained by concern about suboptimal vaccine effectiveness when given in childhood, which has probably led to weak recommendations on the part healthcare providers, despite the NIP recommendation. It should be noted that, since 2017, due to the low incidence of the disease in Greece, the BCG vaccine is only recommended for high-risk groups and, more specifically, for neonates and children belonging to certain ethnic backgrounds with a high incidence of tuberculosis.

4.2. Pneumococcal vaccine

As for the pneumococcal vaccine, the high dosing variability that we observed in our studied population is significant. In a national study in 2012, 94% of the children were given one dose against PCV, whilst only 4% of the children had received all four recommended doses by the age of two.Citation6 Compared to this study, we found a higher PCV coverage, but obviously there is room for further improvement. It is worth mentioning at this point that the current NIP, updated in 2020, recommends three doses for PCV (two doses in the first year of life and the third in the second year).Citation2

4.3. HPV vaccine

The HPV vaccine was introduced in the Greek NIP in 2008. As shown in our study, the immunization coverage of girls by the age of eleven is very low (2.6%), which could be related to several factors, for example, lack of trust in this vaccine, decrease in vaccination uptake during adolescence, and delay in the administration of the vaccine by healthcare professionals. It could well be, though, that the vaccine might eventually be given later on in adolescence. Hence, we may not conclude suboptimal HPV vaccine coverage at this stage. Nevertheless, this low vaccine uptake is noteworthy. Few studies have investigated the coverage for HPV in the young Greek female population. According to a cross-sectional survey in Greece between 2008 and 2014 in 632 female adolescents (aged 11–16 years), only 8.9% had been vaccinated with all the recommended doses of the HPV vaccine.Citation19 Moreover, the study indicates that the vaccination uptake rate increased gradually from 3.2% in 2008 to 17.1% in 2011. However, it abruptly decreased to 2.1% in 2012 and increased again to 9.2% in 2013 and 11.5% in 2014. The participants reported that one of the main factors which prevented them from getting vaccinated against HPV was a fear of side effects. Another similar study with 3153 female higher education students conducted in Greece between 2010 and 2011 showed that only 25.8% of the students were fully vaccinated against HPV and 52.8% of them were vaccinated between 17 and 18 years old.Citation20 Overall, the HPV vaccination coverage in the country is an area that requires further improvement.

4.3.1. CMenB vaccine

In Greece, only 6.5% (108) of our participants had received two doses of the 4CMenB vaccine, whereas 6.9% (114) children had been vaccinated with one dose. It is worth mentioning that, at present, we do not have any national coverage data for this new vaccine. Furthermore, in a study conducted in Greece in May 2016, 1003 parents were interviewed by phone about their perceptions and attitudes toward 4CMenB.Citation18 The study reported that 28.9% of the parents had their children vaccinated against meningitis B, but no data on the children’s age was given and, moreover, study data was not based on the children’s vaccination booklets in order to capture vaccine uptake accurately.

In our country, this vaccine is recommended by the NIP only for groups of children who are high risk for meningococcal disease, such as children with asplenia or complement deficiency. The reasons behind this recommendation are mainly the low disease incidence and the high cost of the vaccine. In 2015 the UK was the first country to implement the 4CMenB vaccine in the immunization program.Citation21 Following the UK, other countries, such as Ireland and Italy, have adopted the same policy.Citation22 The main reason underlying this policy was the higher disease incidence in these countries.Citation22

4.4. Associations between vaccination coverage and socio-demographics

As far as the vaccines with adequate vaccination coverage were concerned (DTaP-IPV, HBV, MMR, Hib, HAV, MCC and VAR), our study showed no association with socio-demographics. For PCV, though, we found that Greek nationality and one of the two parents being employed positively affect the number of doses of PCV (). Previous studies in Greece have also reported that nationality and occupational status are factors that affect the vaccination coverage of children.Citation13–16 Financial and other practical constraints associated with unemployment could account for the associations found. Regarding nationality, the majority of our participants were of Greek origin whereas the number of parents with non-Greek origin (immigrants, belonging to the Roma ethnic group) was very small (). Non-Greek nationality could be a reason for low response rates in this subgroup, as the majority of the Roma population is illiterate. This could also be explained by a lack of willingness to participate in the study. Nonetheless, we know, for instance, that, in general, parents with non-Greek origin do not vaccinate their children at the same rate as Greeks, due to difficulties in accessing healthcare services or due to cultural beliefs.Citation14 With regards to how immunization is delivered in the country, it is important to note that the majority of Greeks vaccinate their children by visiting private primary care pediatricians. Although the vaccines are free of charge, the pediatric consultation is not free. Thus, parents with non-Greek origin might perhaps not adhere to the routine vaccination follow up visits for financial reasons?

4.5. Limitations

We acknowledge that our study has limitations. One limitation is that it is geographically restricted to one large metropolitan area and not the whole of Greece. Nonetheless, our results could be representative of the whole country, because there are no major differences concerning the socio-demographic characteristics of the population in other Greek urban centers (which accounts for nearly 80% of the total country population).Citation23 In addition, it is one of the largest studies assessing vaccination coverage conducted in Greece the last decade. A second limitation is the low participation rate in questionnaires, which could have been improved if we had repeatedly distributed the questionnaires. A third limitation is that, concerning vaccines in adolescence, we cannot ascertain whether there is a full vaccination uptake or not, because these vaccines are recommended for children above 11 years old. Therefore, we do not know if the vaccines would be eventually be given in the near future.Citation24–26

5. Conclusions

In conclusion, the findings of this study, one of the largest conducted in Greece, demonstrate that for vaccines included in the national vaccination program before 1990 (DTaP, IPV, MMR), high vaccination coverage is achieved for the recommended doses. Moreover, we observed an overall trend of higher vaccination coverage rates compared to previous studies in the country. Nevertheless, it is still of paramount importance to monitor vaccination coverage for specific vaccines such as PCV, especially given the recent dose reduction recommended in infancy. Particular attention should also be paid to certain parental characteristics such as non-Greek origin and unemployment, which were associated with suboptimal vaccination coverage, in order to guide further development of public health interventions. In addition, adequate training of pediatricians is of paramount importance to provide sufficient information about vaccinations, as well as to clarify any misperceptions, especially in those groups of parents with particular characteristics that may make them prone to suboptimal vaccination. Finally, a national network recording vaccine coverage data is urgently required in the country to monitor vaccine uptake and assess trends over the years.

Abbreviations

diphtheria-tetanus-acellular pertussis and inactivated polio vaccine (DTaP-IPV), diphtheria-tetanus-acellular pertussis (DTaP, TdaP), inactivated polio vaccine (IPV), Haemophilus influenzae type b (Hib), hepatitis B (HBV), measles-mumps-rubella (MMR), and varicella (VAR), hepatitis A (HAV), pneumococcal conjugate vaccine (PCV), meningococcal conjugated serogroup C (MCC), Human papillomavirus vaccines bivalent/quadrivalent or nine-valent (HPV), Bacillus Calmette–Guerin vaccine (BCG),meningococcal serogroup B vaccine (4CMenB).

Disclosure of potential conflicts of interest

No potential conflicts of interest were disclosed.

Acknowledgments

We would like to thank all of the parents who consented to participate in the study as well as the school teachers for their time in helping us to accomplish this study.

Data availability statement

Data available on request from the authors.

Additional information

Funding

The publication of this article has been financed by the Research Committee of the University of Patras.

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