PEDIATRICS Vol. 121 No. 3 March 2008, pp. e428-e434 (doi:10.1542/peds.2007-1415)
ARTICLE |
Vaccination Coverage in 14-Year-Old Adolescents: Documentation, Timeliness, and Sociodemographic Determinants
a Centre for Youth Health Care, Katholieke Universiteit Leuven, Leuven, Belgium
b Center for the Evaluation of Vaccination, Vaccine and Infectious Disease Institute, University of Antwerp, Antwerp, Belgium
c Vrije Universiteit Brussel, Brussels, Belgium
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONREFERENCES |
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OBJECTIVE. The objective of this study was to measure the coverage and influencing determinants of hepatitis B virus, measles-mumps-rubella, and Meningococcus serogroup C vaccination in 14-year-old adolescents in Flanders, Belgium, in 2005.
METHODS. A total of 1500 adolescents who were born in 1991 and were living in Flanders were selected with a 2-stage cluster sampling technique. Home visits to copy vaccination documents and complete a questionnaire on sociodemographic and other related factors were conducted by trained interviewers. Only documented vaccination dates were accepted. Missing data were, when possible, retrieved through medical charts of the School Health System.
RESULTS. For 1344 (89.6%) adolescents, a home visit was performed. Vaccination coverage was 75.7% for the third dose of hepatitis B virus, 80.6% for the first dose and 83.6% for the second dose of measles-mumps-rubella, and 79.8% for Meningococcus serogroup C. Only 74.6% of the adolescents had proof of 2 measles-mumps-rubella vaccines. Although 1006 (74.8%) adolescents had vaccination data available at home at the time of the interview, only 427 (31.8%) were able to show written proof of all studied vaccines. The probably underestimated coverage rates are well below World Health Organization recommendations, but timeliness of vaccinations was respected. Univariate logistic regression showed that unemployment of the father as proxy measure of socioeconomic status was detrimental for vaccination status, in contrast to partial employment of the mother, which was a favorable factor. Previously unreported determinants of lower coverage rates inferred from this study are single divorced parents, larger families (
4 children), lower adolescent educational level, enrollment in special education, and repeating a grade.
CONCLUSIONS. Insufficient documentation is a major barrier in this vaccination coverage study. More attention should go to those with the lowest coverage rates, such as adolescents from large families, with separated parents, and with a lower socioeconomic background.
Key Words: adolescent • immunization • coverage • determinants
Abbreviations: MMR—measles-mumps-rubella • HBV—hepatitis B virus • MenC—Meningococcus[r] serogroup C • CI—confidence interval
Adolescence is an important period for immunization because young people develop the skills for a responsible adult life, including taking care of their own health.1 A high vaccination coverage rate in adolescents is a prerequisite for long-term protection in adult life. It comprises not only booster vaccinations (tetanus, diphtheria, pertussis, and measles-mumps-rubella [MMR]) but also other immunizations recommended only temporarily in this age group in the framework of catch-up programs (eg, hepatitis B virus [HBV] and Meningococcus serogroup C [MenC]). In the near future, immunization in adolescence will become even more important because new vaccines for this age group are in various stages of development (herpes simplex virus) or implementation (human papillomavirus).1
In agreement with the recommendations of the Belgian Superior Health Council, adolescents who live in Flanders (northern region of the Belgian federal state) are offered a second dose of MMR vaccine at 10 years of age (first MMR dose at 12 months of age), 3 doses of HBV vaccine at the age of 12 years, and a tetanus-diphtheria booster dose at the age of 14 years.2 The HBV recommendation is only temporary because guidelines for infant immunization have included HBV since 1999. After introduction of a MenC conjugate vaccine in the infant vaccination schedule at 12 months of age in 2001, a single dose of MenC conjugate vaccine was offered to all individuals between 1 and 19 years of age during a catch-up vaccination campaign from January 2002 until December 2004.3
In Flanders, recommended vaccines are offered free of charge to adolescents in a school-based immunization program, organized by the School Health Services. In accordance with the Flemish school health legislation, the School Health Services have to monitor the vaccination status of all children under supervision, collect immunization data from well-infant clinics or other vaccinators if necessary, inform parents and children about recommended vaccinations, and offer recommended vaccinations, including catch-up vaccinations; however, the school health legislation does not imply mandatory immunization for school entry. Parents are free to accept this offer or to have their child vaccinated by a general practitioner or a pediatrician.
Few large studies on vaccination coverage in adolescents have been conducted, because, in comparison with younger age groups, it is harder to reach them and to obtain reliable data.4–6 Timeliness of vaccination and determinants of nonimmunization or partial immunization are even less investigated in this age group. Assessments of indirect socioeconomic factors (eg, use of free or reduced-price lunches, living in medium to high deprivation areas) that influence adolescent immunization negatively have been reported,7–9 but the influence of more direct sociodemographic factors such as family related determinants (eg, civil status, family size, rank of child) have not, to our knowledge, been studied in this age group. This article reports the documented vaccination coverage, timeliness of recommended vaccinations, and sociodemographic factors that were associated with nonimmunization or partial immunization against HBV, MMR, and conjugate MenC for adolescents in Flanders.
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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Population and Sampling Procedure
Of all adolescents who were born in 1991 and living in Flanders, a cluster random sample of 1500 individuals was selected using a World Health Organization/Expanded Program on Immunization 2-stage cluster sampling design.10 A sample size of 1500 individuals was chosen to obtain a confidence interval (CI) of ±2.5% for a coverage rate of 90% and a cluster design effect of 2. The individuals were divided over 125 clusters of 12 individuals each, proportionally divided over the 5 geographic regions (provinces) of Flanders. These 125 clusters were selected from all municipalities in a proportionate random way, which allowed larger municipalities to be drawn more than once. The selection resulted in 107 municipalities, for which the Belgian National Registry randomly selected 18 adolescents who were born in 1991 per cluster (12 primary and 6 replacements). The register contains only individuals who are officially registered as residents in Belgium, which includes all individuals who are of Belgian nationality and were born and/or are living in Belgium or abroad. Refugees who applied for the Belgian nationality and who are awaiting a decision are enrolled in the register. Individuals who reside illegally in Belgium and foreigners who work in Belgium are not included in this register.
Survey Procedures
The questionnaire was based on a questionnaire used in the 1999 Flemish coverage study of children of 18 to 24 months of age but adjusted for the current vaccination program and age group.11 A letter with information on the study and announcing the visit of an interviewer was sent to all selected families in May 2005. Trained interviewers visited the selected families between May and July 2005. Interviewers were instructed on the questionnaire and transcription of immunization documents by the researchers.
Adolescents were substituted with a replacement from the same municipality when (1) the interviewer was not able to contact the family after 3 attempts, including at least 1 visit during the evening; (2) the interviewee was not able to understand the questions (mainly French-speaking individuals) because only a Dutch version of the questionnaire was available; or (3) the selected adolescent did not attend the first year of secondary education during the school year 2003–2004, because HBV vaccination is offered during this first year. An exception was made for pupils who attended special education, because they are immunized at calendar age of 12 years instead of in a particular school year.
After having obtained written informed consent from a parent or legal guardian, the interviewer copied all data from vaccination documents and completed the questionnaire with a parent or caregiver. All parents were asked for their written consent to retrieve the immunization data from the medical chart of the School Health Service. For all adolescents with consent, data were requested from the respective school health services, but only for adolescents with lacking data were the vaccination dates from the school health service taken into account.
The questionnaire covered several demographic indicators related to the adolescent (date of birth and gender, school year, and study discipline), the family (civil status of parents, family size, rank of child, and family income), and the parents (ethnicity of parents and grandparents and education and employment of mother and father). Reasons for nonimmunization or partial immunization were asked when appropriate. Parents who refused to participate were asked for the reason but were not replaced, so as to minimize selection bias of replacing individuals who were opposed to vaccines with parents who favored vaccination.
Definitions
According to the Belgian national recommendations on catch-up immunization, valid immunization for MMR was defined as 2 doses of MMR, the first of which was given after the age of 12 months and the second at least 4 weeks later. For HBV, a valid schedule implied at least 3 doses of HBV at any age from birth on. The first and the second HBV doses needed to be at least 4 weeks apart, and the third dose had to be at the age of 6 months or later and at least 16 weeks after the first and 8 weeks after the second dose. For MenC, each dose given after January 5, 2001, was considered valid, because the conjugated vaccine became available on that date.
Civil status of parents was defined as (1) 2 parents present, (2) single separated parent, or (3) single unmarried parent or widow(er).
The ethnic background of children was based on the country of birth of parents and grandparents. Children were classified as Belgian when all parents and grandparents were born in Belgium, European when 1 parents or grandparents were born in a country that belongs to the European Union (25 countries), or non-European when 1 parents or grandparents were born in a country that is not part of the European Union. Adolescent with mixed ethnic background (European/non-European) were categorized as non-European.
Family income was determined as the total amount of money available monthly that could be spent, including wages, alimony, and social security allowance.
Ethical Approval
The study protocol, questionnaire, and informed consent were approved by the ethics committee of the University Hospital of Antwerp and by the privacy commission of the Belgian Government.
Statistical Analysis
Coverage estimates are presented with a 95% CI. Statistical significance of the effect of determinants on coverage rates was tested for each vaccine independently by univariate and multiple logistic regression. Final models were selected with backward selection. Only ethnic background and educational level of the mother were included because these determinants were highly correlated between both parents. A test probability of 5% was considered significant. All CIs and statistical tests were calculated taking into account the cluster design of the sample, using the Survey Package 3.3 for R 2.2.1 (R Foundation for Statistical Computing, Vienna, Austria).
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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Response
Of the original sample of 1500 adolescents, 1495 (99.7%) were actually visited. The parents of 137 (9.1%) youth refused to participate, mainly because of lack of interest and/or time. Opposition to vaccines was no reason for refusal of parents to participate in the study. There was a significant difference in refusal rates according to geographic region (range: 3.6%–12.9%; P < .001). In total, 14 (0.9%) files were lost between intake and analysis. Finally, 1344 questionnaires (89.6% of the target sample) were available for analysis, including 210 (16.6%) replacements.
Population
The mean age of adolescents at the time of inclusion was 13.9 ± 0.27 years (range: 13.4–14.4 years). The gender ratio (51.9% boys) was comparable to that found in Flanders' first grade of secondary school. All other demographic findings (civil status of parents, ethnicity, education and employment of parents, school attendance, and family income) were in line with national census estimates for this age group.
Vaccination Coverage
For 1006 adolescents (74.8% of the questionnaires), complete or partial vaccination data were available at home, but only 427 (31.8%) were able to show written proof of all recommended vaccines. Between 19.1% and 27.3% of the records were updated with immunization dates retrieved from School Health Services for the respective vaccinations. Thereafter, 96 (7.1%) adolescents still had no written proof for any of the studied vaccines. The overall rate of adolescents who were up-to-date for all 3 vaccines was 58.1% (n = 781). The coverage rates reported here are based on the total number of adolescents who were included in the analysis (n = 1344; Table 1).
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Vaccination coverage per dose for HBV, MMR, and MenC vaccines ranged between 75.7% for the third HBV dose and 83.6% for the second MMR dose (Table 1). Only 74.6% (95% CI: 72.0%–77.1%) of the adolescents had proof of both MMR vaccine doses. There were no significant differences according to geographic region, and no relation existed between the proportion of refusals to participate in the study and coverage rates per geographic region.
Coverage rates dropped slightly when criteria for validity of vaccinations, as recommended by the Belgian Superior Health Council, were applied. Only 14 adolescents received the first dose of MMR before 12 months of age, which reduces the coverage for valid vaccination to 79.4%. For MenC, 8 adolescents were withdrawn because the date of vaccination referred to the time before the introduction of the vaccine on the Belgian market, resulting in a MenC coverage of 79.5%. The impact of the recommendations for valid HBV vaccination was more important, reducing the coverage rates to 82.9% (95% CI: 80.6%–85.1%), 76.4% (95% CI: 73.7%–79.1%), and 72.6% (95% CI: 70.0%–75.2%) for the first, second, and third HBV doses, respectively. For 77 adolescents, the minimum interval between 1 HBV doses was not respected. Most cases (n = 48) concerned an interval between the first and second dose being only 2 to 3 days shorter than the minimum.
Reasons for missing data were available for 326 adolescents. For the majority of these youth (60.1%; n = 196), parents claimed that all necessary immunizations had been given, and 27.6% (n = 90) mentioned that documents were missing without reference to the completeness of the vaccination schedule. Other reasons for nonimmunization were forgetfulness (4.9%; n = 16), medical contraindication to vaccination for the child or sibling (3.1%; n = 10), or residency abroad (2.4%; n = 8). Parents of 18 (1.3%) adolescents opposed some or all vaccinations. Fifteen of these youth were partially immunized.
Vaccinator
The school doctor is the main vaccinator in this age group. A total of 72.8% of the adolescents received the second dose of MMR, 70.6% the third dose of HBV, and 56.1% the MenC vaccine from the school doctor. The lower proportion for MenC vaccine is probably attributable to this vaccine's being available from private practitioners before it was offered free of charge through the school immunization program.
Determinants of Vaccination Status
The results of univariate analysis of the most important determinants are presented in Table 2. For parent-related determinants (ethnicity and education), only those of the mother are shown. The father's ethnicity and education showed similar results compared with the mother.
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The documented coverage for both MMR vaccines and MenC vaccine was significantly lower in families with single, divorced parent. Children in the middle position and children from larger families (at least 4 children) were significantly less well immunized for the second dose of MMR vaccine, compared with children without siblings (P < .01 and P < .05, respectively; data not shown).
Adolescents of non-European origin were significantly less well immunized than their Belgian peers. When we explored ethnicity in detail, children with a Turkish background showed the lowest coverage rates for all 3 vaccines, with a rate as low as 36.4% for the second dose of MMR (data not shown).
Better coverage rates were noted when parents had a higher educational degree, except for parents with a university degree (Table 2). Part-time employment of the mother was related to higher coverage rates for all vaccines compared with adolescents from full-time working mothers (Table 2). In contrast, part-time employment or unemployment of the father resulted in lower coverage rates for all vaccines compared with youth from full-time working fathers (P < .01). Higher coverage rates for the second dose of MMR and the third dose of HBV were observed when family income increased (Table 2). Influence of academic performance of the adolescent is shown in Table 2.
When all possible determinants were combined in a multiple logistic regression model, attendance in special education and having a mother with a non-European background were the strongest negative predictive factors and part-time employment of the mother the most significant positive predictive factor for adolescent vaccination coverage (Table 3).
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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In this study, we showed that coverage rates in 14-year-old adolescents in Flanders ranged from 75.7% to 83.9% for HBV, MMR, and MenC vaccines; however, a substantial number of youth partially or completely lacked immunization data, even after data were supplemented from medical charts available at School Health Services. Therefore, the coverage rates presented here should be considered minimum estimates.
Documentation of Immunization
In this study, only 31.8% of the adolescents had documentation for all studied vaccines at home. Even after inclusion of data from School Health Services, the proportion of adolescents with full proof of immunization was relatively low (58.1%). Keeping track of immunization data, however, is one of the cornerstones for the evaluation, improvement, and sustaining of vaccination coverage.12 The Belgian school-based immunization program combines both client-held vaccination cards and provider reminder strategies. At each medical contact at school, the immunization status is checked and a reminder is sent to the parents when immunizations are missing; however, correct and complete documentation of vaccinations in adolescents is often problematic because, over the years, immunization is scattered over several providers (eg, well-infant clinics, School Health Services, private physician). Multiple vaccine providers enhance the risk for losing immunization records.12 In addition, before and during the study period, no general computerized database was in place for this age group; therefore, the registration of administered vaccines tended to be incomplete. The combination of a school-based immunization program and mandatory registration of recommended vaccines in a centralized immunization database could probably offer more complete and reliable data on immunization in adolescents. School-based immunization programs provide 4 major advantages to immunization by private practitioners: (1) for generally healthy youth, school attendance is much higher compared with primary care attendance (immunize them where they are); (2) adolescents can be vaccinated before they engage in high-risk behavior; (3) compliance in multidose vaccination programs is enhanced through peer pressure at school; and (4) these programs are more cost-effective.9,13 A practical issue of a school-based immunization program is obtaining parental consent. Legal constraints of parental consent and adolescent assent could hinder vaccination programs in reaching high coverage rates in some countries.
Insufficient documentation was a major barrier in this vaccination coverage study. The implementation of a central vaccination register may facilitate future assessments. A centralized vaccine database, Vaccinnet (www.vaccinnet.be), was recently developed for the Flemish Ministry of Health. All public (well-infant clinics and school health centers) and private (family physicians and pediatricians) vaccinators have been progressively receiving access since 2005 and are requested to register all administered vaccines. The use of this centralized vaccination database improves documentation of immunization and should result in more reliable estimates of vaccination coverage in the future.
Although this study proved that documenting immunization is difficult in this age group, measuring the adolescent vaccination coverage with an Expanded Program on Immunization survey was a useful strategy because of the higher participation rate (89.6%), compared with telephone or written surveys.14 In addition, telephone and written surveys tend to overrate the actual vaccination coverage because the data retrieved are usually based on parental recall, not on written proof of immunization.14,15 In contrast, this survey may underrate the coverage, because documents on immunization were often not available at home. The interviewers were explicitly instructed to rely only on written documents and not on parental recall.
Timeliness of Immunization
Protection that is generated by vaccines depends not only on their immunogenicity but also on the age at which immunizations are given and the correct interval between subsequent doses. Most studies on timeliness of vaccination focus on the delay between subsequent doses and reflect on the period children remain unprotected16; however, if a vaccine is given too early (eg, MMR before 12 months of age) or doses are given with a shorter interval than recommended, then a suboptimal immune response may be generated. These invalid doses can lead to a false sense of protection.17 In our study, only minimum ages and minimum intervals were taken into account to measure the coverage of valid doses, because these are most influential on the protection that is induced by vaccinations. Because only minor deviations from a valid vaccination scheme were noted, we conclude that most adolescents were correctly immunized. Although timeliness of vaccination is favorable, the need to maintain recommended intervals and respect for minimum age of vaccination should be stressed, because sloppiness can lead to less-than-optimal protection.17
Sociodemographic Determinants of Adolescent Immunization
Although the vaccination coverage was influenced by the completeness and quality of documentation, several sociodemographic indicators showed a relation with adolescent coverage rates. Whether these determinants are correlated with the ability of parents to produce vaccination documents or with the coverage itself remains largely unknown. Probably, both are affected, because most parents (87.7%) who gave a reason for nonimmunization or partial immunization believed their child to be fully immunized.
One of the most important determinants of a lower immunization coverage in the univariate analysis was unemployment or part-time employment of the father. Employment of parents, however, is largely correlated with other indicators of the socioeconomic status, such as educational level of parents and children, family income, and ethnicity. For instance, in our population, 25.3% of the non-European fathers were unemployed compared with 5.5% of the European fathers and 2.1% of the Belgian fathers. Although in Flanders immunizations are available free of charge (including the cost of the immunization consult), youth with a less favorable socioeconomic background had less proof of recommended immunizations. Similar results were reported for HBV, MMR, and tetanus-diphtheria vaccines in the United States and the United Kingdom.7–9 These lower immunization rates are likely related to a combination of factors: (1) the knowledge or (2) language skills of parents and adolescents may not be sufficient for full understanding of the information on vaccinations that are provided by the school health service, or (3) the time needed to review this information is simply missing.9
Family- and school-related factors have not been investigated by other authors in this age group. According to our study, youth in 2-parent households tended to have better proof of immunization for MMR and MenC. That the organization of a household can be shared between 2 people can also contribute to a higher coverage in these families. During a divorce, loss of documents will occur more easily as a result of division of goods and possibility of moving houses. The size of the family and rank of the child in the family also interfered with MMR vaccination status. The effect of family size was also noted in a French study of 3-year-old children, in which children from larger families were less well immunized.18 In our study, factors related to academic performance also had an impact on adolescents' immunization coverage. Adolescents who repeated the first year of secondary school and pupils who attended special education were particular risk groups for nonimmunization. Despite that these adolescents should have received the same offer of immunization through the school-based system, they were less well immunized. From the results of this study could be inferred that some families have more urgent priorities (financial, relational, and educational) to resolve than the immunization status of their children. Additional support for these particular families to improve the immunization of their children should be encouraged. Family- and school-related indicators can be easily incorporated in a school-based immunization program, and a strict follow-up of children at risk may lead to better overall immunization coverage.
Unvaccinated adolescents have a greater risk for contracting vaccine-preventable diseases and could transmit disease to infants who are not (yet) fully immunized, to individuals with medical contraindications for immunization, and to immunized individuals who did not respond to the vaccine (vaccine failure).18 Because adolescence is the last opportunity for large-scale immunization programs through school, every opportunity to assess and update the vaccination status should be used to maximize the vaccination coverage. This study showed that it is possible to identify children who are at risk for a suboptimal vaccination status. Specific actions aimed at risk groups could improve the overall vaccination coverage and protection against vaccine-preventable diseases.
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ACKNOWLEDGMENTS |
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This study was funded by the Flemish Ministry of Welfare, Health and Family, Belgium.
We thank all of the families who participated in this study. We also thank the School Health Services, who willingly provided us with many missing vaccination data, and Sara Daman and Katrien Hofkens for help with data input.
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FOOTNOTES |
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Accepted Jul 21, 2007.
Address correspondence to Corinne Vandermeulen, MD, Center for Youth Health Care, Katholieke Universiteit Leuven, Kapucijnenvoer 35, B-3000 Leuven, Belgium. E-mail: corinne.vandermeulen{at}med.kuleuven.be
Financial Disclosure: Drs Hoppenbrouwers and Van Damme have been principal investigators of several vaccine trials for which the respective universities received research grants. All other authors have indicated they have no financial relationships relevant to this article to disclose.
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PEDIATRICS (ISSN 1098-4275). ©2008 by the American Academy of Pediatrics
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