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Metrics details. Measles elimination in Europe is an urgent public health goal, yet despite the efforts of its member states, vaccination gaps and outbreaks occur. This study explores local vaccination heterogeneity in kindergartens and municipalities of a German county. Children with unknown vaccination status were either removed from the analysis best case or assumed to be unvaccinated worst case.

Vaccination data were translated into expected outbreak probabilities. Physicians and kindergartens with statistically outstanding numbers of under-vaccinated children were identified.

A total of 7. Excluding children without a vaccination certificate best case leads to over-optimistic views: the overall outbreak probability in case of a measles introduction lies between Four paediatricians were identified who accounted for 41 of unvaccinated children and for 47 of incomplete vaccinations; GPs showed significantly higher rates of missing vaccination certificates and unvaccinated or under-vaccinated children than paediatricians.

Missing vaccination certificates pose a severe problem regarding the interpretability of vaccination data. Although the coverage for at least one measles vaccination is higher in the studied county than in most South German counties and higher than the European average, many severe and potentially dangerous vaccination gaps occur locally.

If other federal German states and EU countries show similar vaccination variability, measles elimination may not succeed in Europe. Peer Review reports. Measles is highly contagious and claims many lives every year, particularly among young children. Annually, approximately million cases of measles and 6 million measles-related deaths occurred worldwide before vaccination was introduced in [ 1 ].

Global measles control has been very successful: in countries with routine measles immunization, mass vaccination campaigns, and appropriate case management, measles deaths have dropped dramatically between and , from , to , [ 1 ].

In Germany alone, to cases occurred annually from to 5. The most recent epidemic in Berlin lasted from October to August and led to cases [ 6 ]. In , measles cases were reported in BW [ 7 ]. Key challenges include vaccination hesitancy, complacency, and under-served populations [ 8 ]. Germany ensured its commitment by establishing a national action plan for —20 as well as a national verification commission for the elimination of measles and rubella [ 9 ].

In Germany, measles is a notifiable disease; vaccinations are not mandatory and can only be administered by physicians. Parents can choose whether their children are registered with paediatricians or general practitioners. Due to a shortage of physicians in rural areas, some parents may opt for their children to be registered with general practitioners rather than paediatricians.

Children can be enrolled in schools without proof of vaccination or immunity, but the local public health offices have to survey the vaccination certificates of all 4- to 5-year-old children during the mandatory school enrolment examinations Einschulungsuntersuchungen, ESU [ 11 ].

In comparison, BW had Recent legal amendments aim to improve the vaccination coverage of children: before they can be enrolled in kindergarten, their parents must now consult a physician who has to certify that they were informed about vaccinations.

Their proof of consultation is not documented in the vaccination certificate but on a separate document, which is to be presented to the kindergarten or school upon enrolment, whether the institution is public or private [ 11 ]. There is no standardized vaccination surveillance system in Germany. Thus, the assessment of the vaccination and immunity status of the population has to use random samples or cross sectional surveys. The aim of this study is to assess the local variability of measles vaccination coverage in the German county of Reutlingen BW at a small community level based on the data collected from 4- to 5-year-olds during the ESU in the and school year.

Under-vaccinated pockets will be identified and can then be targeted through tailored vaccination action plans. This study is based on measles vaccination data of 4- to 5-year-old children from and in Reutlingen county that were routinely collected by us. Reutlingen county is located in the south German state of BW and has a population of , inhabitants, who live in 26 municipalities with kindergartens. Therefore, the data that were collected and anonymized by the authors could be used freely for this work and ethical approval was not required.

The dataset includes the age, gender, measles vaccination status, physician, kindergarten, and residence municipality of each child.

The vaccination coverage of children with at least one measles vaccination and with both measles vaccinations were calculated for each municipality and kindergarten in the county of Reutlingen. To examine the presence of a vaccination certificate or the vaccination status, children were classified in different groups: [ 1 ] children who were registered with GPs and [ 2 ] children who were registered with paediatricians.

A third group of children, whose parents were not able to supply the name of a physician, was considered in the multivariate analysis, but not in the group comparisons. In a measles outbreak in a German school, Multiplying the vaccine efficacy VE by the vaccination coverage of a community results in the average immunity level x. Although this probability is valid only for large populations, it can be used as an indicator of how well a group of individuals is protected against the continued spread of measles.

To calculate the percentage that must be vaccinated to prevent epidemics, the immunity level x must reduce R e to a value less than 1, i. To identify physicians and kindergartens with excessively high percentages of unvaccinated children, we performed univariate analyses as follows: for each physician and for each kindergarten , [ 1 ] the number n of all children with vaccination certificates who were registered with the physician or who attended the kindergarten was determined, [ 2 ] the number k of these children who were not vaccinated was determined, [ 3 ] the probability P that children with vaccination certificates were not vaccinated was calculated for all other children who were not registered with the physician or who did not attend the kindergarten.

In these bivariate analyses, we examined the joint influence of physicians and kindergartens. Parameters were estimated by maximum likelihood. The same series of univariate and bivariate analyses was then repeated with children who were vaccinated at least once n and with fully vaccinated children k. The statistical package JMP was used for data evaluation [ 18 ]. In terms of physicians, of the children were registered with 56 paediatricians, while the remaining were registered with 45 general practitioners GPs.

Vaccination coverage values for at least one measles vaccination in County Reutlingen, its municipalities and kindergartens are visualized in Fig. Some of the kindergartens and municipalities are highly under-vaccinated, making them vulnerable to measles introduction Figs. Vaccination coverage with at least one measles vaccination, County Reutlingen worst case and best case.

Illustration of the vaccination coverage for at least one vaccination on different community levels. The figures display the best-case scenario, where all children without vaccination certificates were omitted from analysis left , and the worst-case scenario right , where these children were regarded as unvaccinated. The local vaccination coverage was colour-coded see inlet. The areas of the kindergartens are proportional to the number of children for whom data were available see inlet.

To ensure the anonymity of kindergartens, the dots do not represent real geographic locations. Measles epidemic probabilities in municipalities and kindergartens.

Significantly higher percentages of children who were registered with a GP had no vaccination certificate In our first univariate analyses, two kindergartens out of and four paediatricians out of 56 with exceptionally high fractions of unvaccinated children were identified see Online Additional file 1 for details.

As some children who attended one of these two kindergartens were also registered with one of the four paediatricians, we added a bivariate analysis, which allowed for competing risks. In a second univariate analysis, eight kindergartens and three paediatricians with exceptionally high fractions of incompletely vaccinated children were identified. Interestingly, these three paediatricians are a subgroup of the four paediatricians who were identified in the first analyses concerning children who were unvaccinated.

The fourth paediatrician may only have dropped out of the second analysis concerning complete vaccination because too few children with at least one vaccination were left. Altogether, With It can be seen that — although Reutlingen county has an overall coverage of If we assume that other federal German states or EU countries show similar vaccination variability at community and kindergarten levels cf. This variability would also explain why apparently well-vaccinated populations still experience measles outbreaks.

A more recent study from the Netherlands reported measles cases in This shows that high national or regional vaccination coverage cannot guarantee the prevention of outbreaks. All of these outbreaks were linked to communities that had low vaccination coverage. Many of the affected people were not vaccinated.

Reaching under-vaccinated groups in schools and improving their vaccination uptake would greatly decrease the chance of outbreaks [ 23 ]. Frequency of communities grouped by measles vaccination coverage best-case scenario; at least one vaccination; — Level 3: comparison of County Reutlingen to the other counties of BW [ 31 ].

In our search for vaccination gaps, we have identified four paediatricians out of 56 and six out of kindergartens with extremely low vaccination rates. As parents are free to choose paediatricians of their own liking, families with reservations against vaccination may cluster with some paediatricians and avoid others.

GPs provide medical treatments to all age groups and are less specialized for treating children. Therefore, they may be less informed on current vaccination schedules for children and may have a shortage of the vaccines needed for children. These factors could explain why children seeing GPs have a lower vaccination status than those seeing paediatricians. The outcomes of this work have stimulated discussions on the current situation and on targeted solutions.

Although physicians themselves may not always be the cause of under-vaccination, they could still be pivotal points of intervention campaigns. All paediatricians of County Reutlingen have been informed of their vaccination results and their ranking among their peers. Vaccination coverage could be largely increased by improving the vaccination uptake of the children who were registered with the four identified paediatricians.

Even if the vaccination status of only these children reached the level of the others, Children registered with GPs generally had lower vaccination rates than those registered with paediatricians. Unlike paediatricians, GPs could not be analysed individually because of the small number of children per GP most of them observed less than 5 children.

The issue of the low vaccination coverage of children who were registered with GPs should also be discussed in the German GP Associations. They further demand that children may only enrol in private or public kindergartens and schools if they have received all vaccinations unless a contraindication exists that are recommended in the German vaccination calendar by STIKO [ 25 ].

Given the compulsory school attendance in Germany, this would imply obligatory vaccination, as was recently demanded by the president of the German National Medical Chamber [ 26 ]; yet, so far, compulsory vaccination has been declined in Germany.

A major problem that became apparent during this study was the huge gap between the best- and worst-case scenarios, which was caused by participants without vaccination certificates. It would be helpful if the existing legal obligation of providing a vaccination certificate at ESU was actually enforced. At the moment, it is common practice in Germany to calculate the vaccination coverage only from data on children who present a vaccination certificate [ 27 , 28 ,, 28 ], which may easily lead to over-optimistic views.

Currently, the measles vaccination coverage of Germany seems to be exactly as high as in Sweden, yet this result may be misleading: the Swedish dataset is registry based, whereas the German data are based on a best-case scenario. The establishment of a vaccination register, per se, would not improve vaccination coverage, but it would help shed light on the vaccination status of the population and identify under-vaccinated pockets and sources of low coverage.

Over the last sixteen years, vaccination coverage has gradually increased, and it has reached a plateau in Reutlingen country. This also implies that older children and juveniles may have an even lower vaccination coverage than the children in this study.

Another limiting factor is that only one German county was analysed in this study.


Local measles vaccination gaps in Germany and the role of vaccination providers

Metrics details. Measles elimination in Europe is an urgent public health goal, yet despite the efforts of its member states, vaccination gaps and outbreaks occur. This study explores local vaccination heterogeneity in kindergartens and municipalities of a German county. Children with unknown vaccination status were either removed from the analysis best case or assumed to be unvaccinated worst case. Vaccination data were translated into expected outbreak probabilities.


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