Measles Status—Barriers to Vaccination and Strategies for Overcoming Them
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Background: The World Health Organization (WHO) set the year 2020 as a target date for the eradication of measles in Europe, yet Germany is still far away from this goal. In this article, we provide an overview of current vaccination gaps and barriers to vaccination among children and adults in Germany, as well as potential strategies for overcoming them.
Methods: This review is based on pertinent publications identified by a selective literature search in PubMed (Medline).
Results: Measles vaccinations are not carried out in the appropriate timely fashion in Germany. Moreover, current vaccination rates among both children and adults are too low to achieve the goal of measles eradication. For example, among children born in 2014, the recommended vaccination rate of more than 95% was only reached when these children were 24 months old. Primary care physicians bear the responsibility for this situation, as they have the greatest influence on the decision to vaccinate. The main causes of vaccination gaps are safety worries and complacency on the patients’ part, and partial skepticism regarding vaccination on the part of the caregivers. We identified promising strategies for overcoming these problems: an instructive talk to provide evidence-based information to patients in an atmosphere of mutual trust, reminder systems, multifactorial interventions, and facilitated access to vaccination, or, as a last resort, the reintroduction of compulsory vaccination.
Conclusion: Primary care physicians play a key role in vaccination. The focus of further strategies should lie above all in improved patient education and in targeted reminders for patients who neglect to vaccinate themselves and/or their children.
Four years ago, the World Health Organization (WHO) had to postpone its objective—to eliminate measles from the European region by 2015—to 2020. It had become obvious that it was not possible to reach this milestone in time (e1, e2). By comparison with Europe, the entire American continent had successfully achieved measles elimination in 2016, with a vaccination rate of >95% (1). In the WHO European Region, measles continues to be endemic in 11 of 53 countries (2). In Germany several measles outbreaks were documented in recent years, in spite of increasing childhood vaccination rates (e3). In 2015, almost 2500 measles cases were reported (incidence 3.1/100 000), which means that Germany had clearly missed WHO’s elimination target (incidence <0.1/100 000 and interrupted transmission for >36 months) (Figure 1) (e3). In 2016, Germany, together with Austria and Switzerland, was able to interrupt endemic transmission for at least 12 months, which constitutes an important step towards measles elimination in Germany as well as in Europe (3). Whether this trend continues remains to be seen; particularly as measles case numbers in 2017 were more than three times those of 2016 (4).
In this article we will discuss why Germany—like Romania, France, Italy, and Georgia, among others—continues to be among the number of European countries where measles is still not eliminated. This is particularly relevant on the background that measles vaccination in Germany continues to have insufficient coverage rates compared with other standard vaccinations (Figure 2). This article provides an overview over existing vaccination gaps in measles, barriers to vaccination in childhood and adulthood, and strategies to overcome these barriers.
We conducted a PubMed search for relevant publications. We used the following search terms: “measles”, “vaccination”, “hesitancy”, “barrier”, “antivaccination attitude”, “compulsory”, “Germany”, “refusal”, “strategy”, “review”. We included German language and English language publications. We complemented our search by searching the internet pages of the Robert Koch Institute (RKI), the WHO European Region group, and the WHO Strategic Advisory Group of Experts (SAGE) on Immunization.
We used relevant abstracts to identify articles about vaccination fatigue and barriers that described intervention strategies. Furthermore, we included articles that showed the current situation (measles vaccination rates) in Germany on the basis of statistical data collections. We also included qualitative studies (focus groups and interviews), editorials, and commentaries, as well as position papers. We also searched the references of all included articles for additional relevant publications.
Vaccination status for measles in Germany
In order to achieve complete protection through immunization, the RKI’s Standing Committee on Vaccination (STIKO) recommends that the first dose of the measles vaccine be given at 11–14 months of age, and the second dose at 15–23 months. No central vaccination registry exists in Germany (5). Since 2001, however, the school entry health examination study has been undertaken in collaboration with the RKI, on the basis of the German Protection against Infection Act (Infektionsschutzgesetz, IfSG). This study collects data from children aged 5–7 years (e4). In 2015, the rate found was >95% at the first vaccination for measles, but in this age group, not all children are optimally protected by a second dose (rate <95%), as shown in Figure 2.
Since 2004, data have also been collected by the RKI’s health insurance vaccination surveillance, which also includes billing data from adults who are members of statutory health insurance schemes (e5). These observations show for those born in 2014 at the age of 15 months a nationwide increase in the vaccination rate to 89.5% for the initial vaccination (e5). However, in children born in 2014, the rate of >95% for the first dose is achieved too late—namely, at age 24 months (e5). Only 73.9% received the second dose in time, by age 24 months (e5). The timely administration of the two doses seems to continue to be difficult to implement (6). The data published online by the RKI in the “Vacmap” lead to the conclusion that Baden–Württemberg and Saxony did not achieve a vaccination rate >95% for the first dose in children born in 2014, neither at age 15 months nor at age 24 months (7). Furthermore, in Saxony, the Saxon Commission on Vaccinations (SIKO), which was set up in 1991, recommends the second dose for the time around a child’s 4th birthday, in the 46th–48th months of life at the earliest (8). Infants and toddlers in Germany are therefore neither directly protected against measles nor by means of herd immunity (7). Furthermore, maternal passive immunity decreases in societies that have long established measles vaccination programs, because the passive transmission of antibodies from mothers vaccinated against measles to their children is lower than in the prevaccine era (9).
The German Health Interview and Examination Survey for Adults (DESG1) showed for Germany measles vaccination rates in 18–29 year olds in 2008–2011 of overall 79.8% (95% confidence interval [76.3; 82.9]). Of those aged 30–39 years, 46.7% [42.2; 51.2] had been vaccinated, and of those aged 40–49 years, 25.1% [21.8; 28.7] had been vaccinated (e6). In the past, these groups continued to contribute to measles outbreaks. As a result, the STIKO issued a recommendation for booster vaccinations for people born after 1970 who did not have two doses of the measles vaccine as children. Figure 3 shows how the epidemiology of measles developed in the time periods 2001–2003 and 2015–2017. Figure 1 shows hospital admissions between 2006 and 2016.
In the past 10 years, the causes of death statistic posted an average of 1–2 deaths due to measles per year (10). The RKI reports a case fatality rate of 1:1000 persons infected with measles for 2001–2012 (11).
Vaccination barriers in patients and doctors
The German Health Interview and Examination Survey for Children and Adolescents (KiGGS) (12) on the sociodemographic or economic differences in unvaccinated youths and those with incomplete measles vaccination showed that:
- A significant difference between eastern Germany and western Germany existed in adolescents.
- A high socioeconomic status correlates with a lower vaccination rate.
- If parents had general reservations with regard to vaccinations, 54.3% of children aged 2–17 years had not been vaccinated against measles, compared with only 5% who were not vaccinated against tetanus.
- The number of siblings also played a part. Having three and more siblings correlated with a reduced vaccination rate.
- Children who had immigrated to Germany had worse vaccination rates than immigrant children who were born in Germany (13).
- Vaccination skeptics also have a higher educational status (e7).
A further barrier was identified as a result of increasing migration to Europe and Germany. In children who had fled warzones without functioning healthcare systems (78.5% Middle East, 9.6% Africa), a seroprevalence study in 2015 found that measles immunity was insufficient in those younger than 18 (17.3%, [7.7; 26.9]; seropositive: 82.7%) (14).
The reservations about measles vaccination are easy to identify: those opposed to vaccination insist on the assumption that measles is a harmless childhood disease and also attribute it with the task of promoting a child’s development (15). Vaccination skeptics primarily have safety concerns (16–18), especially with regard to possible long-term adverse effects. The worry about exposing a primarily healthy child to the risk of adverse effects of vaccination is understandable and is known in the behavioral sciences as the so-called omission bias (19). Disrespectable websites foment these fears with information that is not always reliable (20).
The argument that has been repeatedly made is that the measles vaccine triggers autism. This is based on a publication in the Lancet (21), which was retracted in 2010 because of serious quality deficiencies and was assessed as fraudulent. For the preservative thimerosal, a systematic review in 2014 additionally disproved any association between measles vaccination and autism (e8). The RKI was able to identify the 20 most commonly held reservations of vaccine skeptics and anti-immunization campaigners and on its website provides extensive answers to how to counter these (e9) (eBox).
It doesn’t seem to be rare even for primary care professionals to be vaccine skeptics (22), and they do not always act in an evidence-based manner (23). Increased personal contributions in those with private health insurance may in future contribute to these patients deciding against vaccinations, for financial reasons (e10).
Historically, measles vaccination in Germany—by contrast to the German Democratic Republic and the USA)—was not applied in an evidence-based manner, especially in the 1960s. The inactivated split vaccine remained the vaccine of choice, and Germany’s Federal Ministry of Health (BMG) recommended only individual prophylaxis for children at risk. This did not bring about greater acceptance (24). Further important barriers are complacency or indifference, as described by WHO in its definition of vaccine skepticism. These affect primarily countries where vaccine preventable diseases are rare and other decisions about health may consequently seem more important. An additional factor is the laziness of patients, who—in Germany, for example—have to make a special appointment (25).
Strategies for overcoming barriers
Total vaccine objectors/antivaccinationists generally or who deny the pathogenicity of viruses are hard to convince with arguments alone (26). For this reason, the particular focus should be on ambivalent vaccine skeptics (27, 28). WHO’s Tailored Immunization Programmes (TIP) target the inhomogenous group of vaccine skeptics with evidence-based information. They initially identify regional gaps in vaccination coverage as well as populations that are particularly affected, and they seem to effect behavior changes successfully (e11). The SAGE found in a systematic review that dialogue-based interventions and multimodal approaches (for example, flyer plus dialogue) are most effective (Box) (29).
By contrast, a Cochrane review that included six randomized controlled trials (RCTs) and a cluster RCT with a total of 2978 participants found only a slight effect or no effect at all from personal consultations with parents on the acceptance of recommended standard vaccinations in their children. The Cochrane Collaboration therefore recommends conveying the relevant communication not in a separate appointment but in the normal practice encounter between doctor and patient (30). The May 2018 update of the review (seven RCTs, three cluster RCTs with 4572 participants) reaches a similar conclusion: “The effect of the intervention in a population where concerns about vaccines or vaccine hesitancy is the primary barrier is less clear.” (e12).
In the context of a further Cochrane meta-analysis, two studies from India and Pakistan investigated the effect of intensive information/education campaigns at community level regarding the benefit of childhood vaccination. They found a positive effect in populations with known low vaccination rates, but it took disproportionately much effort for a comparatively small success (31).
A meta-analysis of 38 studies (focused on high-income countries, partly relating to measles–mumps–rubella [MMR]) uncovered deficiencies—as described by parents—in the communication about standard vaccinations: the parents were missing more and balanced—as well as individualized—information about the risks and benefits of defined vaccinations. Healthcare professionals were the most credible source, but parents also wanted information sources outside the healthcare system. They themselves found it difficult to decide which sources were trustworthy and unprejudiced. More skeptical parents wanted more detailed information (32).
Table 1 shows the results of a further systematic research study into overcoming barriers to vaccination. This overview shows that primary care providers have a key role in dismantling barriers to vaccination. According to WHO and WONCA (World Organization of National Colleges, Academies and Academic Associations of General Practitioners/Family Physicians), primary prevention is the task of responsible physicians (33, 34). Patients’ decisions in favor or against vaccination are vastly influenced by how important their doctor deems the vaccinations (35). The strategy of last resort could be to re-introduce compulsory vaccination (36). As an initial alternative, a subsidiary and unified nationwide program could be implemented that uses the already existing structures of the public health service (ÖGD). Vaccination clinics in pharmacies and supermarkets as an easy-access service are another option, following the North American example.
Familiy physicians and pediatricians are particularly tasked with closing gaps in vaccination coverage in the German population, as they have an important influence on the decision in favor of or against vaccination (e13). Measles vaccination coverage in children and especially in adults in Germany has substantial gaps. As a result, repeated local outbreaks have occurred, and in the past 10 years, 15–50% of infected patients had to be admitted as hospital inpatients. This is largely due to not only vaccine skeptic patients, but also vaccine skeptic doctors, who have forged effective communications networks via modern social media (37).
Vaccine skeptic primary care professionals prioritize the individual decision regarding vaccination, and they thus ignore the responsibility for the whole of society—as defined by the infection law—which is to prevent infections (37). A vaccine skeptic pediatric practice with 1100 patient contacts every quarter (38) therefore bears the risk of jointly causing and contributing to regional outbreaks.
Communicating with vaccine skeptics and anti-vaccinationists in clinical practice can be emotionally fraught. Strategies for a positive dialogue—which has been found to be a vital factor of influence—are therefore crucial. It is important to direct the focus on those vaccine skeptics who are more open to reasoning (27). A truthful/trustful dialogue with reliable primary care professionals who are participating in continuing professional development/continuing medical education (35), who follow the recommendations of the STIKO, and who act in an evidence-based and rational manner, is also promising. As a supporting measure, reminder mechanisms could be implemented—such as the electronic vaccination passport in Switzerland—in order to reach inattentive persons (e14).
As the original target for measles elimination has to be postponed and its implementation by 2020 seems unlikely, re-introducing compulsory vaccination as a strategy of last resort is currently under discussion. Since 25 July 2017, those in charge of nurseries/children’s day-care centers have been legally obliged (according to the German law on the modernization of epidemiological surveillance of communicable diseases and the IfSG) to report unvaccinated or incompletely vaccinated children to the public health authorities. The plan is to then invite parents for a consultation whose outcome is not predefined.
It should be borne in mind that compulsory vaccination for measles only may well have the opposite effect of what is intended. Vaccine skeptics may then refuse all other vaccinations, even some of those that are not compulsory (e15). In order to counteract this, in 2017 Italy and France, for example, extended existing compulsory vaccination schedules or newly introduced such schedules. In these countries, the right to protection via herd immunity of the human being who cannot (yet) be vaccinated (infants, persons with immunosuppression) supersedes the vaccine skeptic’s right to physical integrity.
When compulsory vaccination for smallpox was abolished in Germany in 1961, the responsibilities for vaccination and cost absorption transferred from the public health authorities to the primary care providers (e16). The question of whether newly introduced compulsory vaccination might have a positive effect on measles vaccination rates is not easily answered. First of all, it would need to be clarified unequivocally how compulsory vaccination should be enforced. Exclusion from school—such as is practiced in the USA, for example—is not possible in Germany because school is compulsory. Vaccination was formally compulsory in the German Democratic Republic, and even in 2000, the incidence of measles in the new German states was below 0.9/100 000 (old German states 46.8/100 000) (36).
Several strategies in Germany are conceivable in order to achieve the objective of measles elimination by 2020. Above all others ranks the trustful/truthful dialogue between responsible physicians and vaccine skeptic patients on the basis of evidence-based information. Other means could support this, such as reminder mechanisms for neglectful patients.
The effects of compulsory vaccinations are unpredictable. They may achieve the objective more quickly. But it will need to be legally clarified how enforcement would work. We think that initially, a subsidiary, non-compulsory, nationwide program might be introduced at community level, organized by the public health authorities or a school physician system. This could support primary care professionals and facilitate access for lazy or neglectful patients. Vaccinations constitute a prevention measure at societal level, and therefore should—in the sense of the public’s health—be undertaken consistently nationwide.
Conflict of interest statement
Prof. Heininger received consultancy fees from Takeda.
Dr. Sanftenberg received reimbursement of conference delegate fees and travel expenses from Pfizer. She has received author/co-author fees from Thieme Publishers, in the context of a publication whose subject matter is relevant to this article.
Prof. Schelling received consultancy fees from Pfizer, MSD, and GSK.
The remaining authors declare that no conflict of interest exists.
Manuscript received on 23 June 2017, revised version accepted on
9 July 2018.
Translated from the original German by Birte Twisselmann, PhD.
Dr. med. Constanze Storr
Institut für Allgemeinmedizin der Technischen Universität München
Orleansstr. 47, 81667 München, Germany
For eReferences please refer to:
blicationFile (last accessed on 24 June 2018).
Institute of General Practice, Ludwig-Maximilians-Universität München: Dr. rer. nat. Linda Sanftenberg, Prof. Dr. med. Joerg Schelling
Department of Pediatric Infectiology and Vaccinology, Universitäts-Kinderspital beider Basel (UKBB):
Prof. Dr. med. Ulrich Heininger
Institute of General Practice, Technische Universität München: Prof. Dr. med. Antonius Schneider
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