DÄ internationalArchive21/2020Vaccine-Preventable Infections in Childcare Workers

Original article

Vaccine-Preventable Infections in Childcare Workers

A Systematic Review and Analysis of the DEGS1 Study and of Notifiable Disease Surveillance Data

Dtsch Arztebl Int 2020; 117: 365-72. DOI: 10.3238/arztebl.2020.0365

Kofahl, M; Starke, K R; Hellenbrand, W; Freiberg, A; Schubert, M; Schmauder, S; Groß, M L; Hegewald, J; Kämpf, D; Stranzinger, J; Nienhaus, A; Seidler, A

Background: Adequate immunity to so-called childhood diseases can lower the occupational risk of vaccine-preventable infectious diseases in persons who work in day-care centers for children.

Methods: A systematic literature survey was carried out in PubMed and Embase for the period January 2000 to February 2019. Studies on immune status and vaccination status were included. In addition, data from the first wave of the German Health Interview and Examination Survey for Adults (Studie zur Gesundheit Erwachsener in Deutschland, DEGS1) and surveillance data on notifiable infections in Germany were evaluated.

Results: Six studies and the DEGS1 analysis of vaccination or immune status for varicella zoster, rubella, hepatitis A (HAV), pertussis, measles, and mumps in persons caring for children in day-care centers, most of whom are women, were included in this review. According to DEGS1, childcare workers are more commonly vaccinated against HAV and pertussis than the general female population (prevalence ratios [PR]: 1.46 [1.12; 1.90] and 1.57 [1.05; 2.36]), yet 57% had not been vaccinated against HAV and 77% had not been vaccinated against pertussis. Childcare workers were found to be less commonly vaccinated against rubella than the general female population, although the difference was not statistically significant (PR: 0.87 [0.71; 1.07]). In a Canadian study, positive HAV serology was found to be correlated with the duration of activity as a childcare worker. In the DEGS1 study, large proportions of the younger childcare workers in particular were seronegative against measles (16%), mumps (19%), and HAV (37%). Notifiable disease statistics show that those working in community facilities had a markedly higher risk of mumps, pertussis, and varicella (relative risk [RR]: 1.8–2.6) and a somewhat higher risk of rubella and HAV (RR: 1.47 and 1.21, respectively).

Conclusion: Childcare workers have a higher occupational risk of infection but do not always receive the appropriate vaccinations. In particular, women of child-bearing age working in day-care centers should be made more aware of the need for vaccination.

LNSLNS

The question of adequate immunoprotection against the so-called childhood diseases now no longer relates only to children. In Germany 73% (1) and in Europe 62% of patients with notified pertussis are older than 14 years (2), and 35% of notified cases of measles are in persons older than 20 (3). Some of these infections cause more complications in adults than in children and also last longer (4). In addition to a lack of booster vaccinations for tetanus, diphtheria, and pertussis, which are recommended by most European countries (5), decreasing effectiveness of measles vaccine with increasing age has also been observed (6).

Seronegative pregnant women are among the groups at high risk. Measles infection can cause pregnancy complications, premature birth, and miscarriage, and connatal varicella zoster or rubella can result in irreversible damage to the child (4, 7, 8). Since the spread of infection is already wide in childhood, primary infections in pregnancy and thus fetal varicella syndrome are rare (9). However, rubella is still endemic in seven EU countries (Belgium, Denmark, Germany, France, Italy, Poland, and Romania) (10), so the risk for connatal rubella infection remains high.

Childcare workers in day-care centers are in constant close contact with children, and droplet infection or smear infection can readily occur. As long as vaccination coverage is anything less than almost complete, such childcare workers have an increased risk for occupational infection with vaccine-preventable pathogens.

With the aim of estimating the infection risk, we undertook a systematic review, analyzed data from the first wave of the German Health Interview and Examination Survey for Adults (DEGS1), and documented the incidence of notifiable communicable diseases in Germany.

Methods

Systematic review

The study protocol was drawn up a priori (PROSPERO registry no. CRD42018083646). This study is part of an overarching systematic review and focuses on vaccine-preventable diseases. Two studies of non-vaccine-preventable diseases have already been published elsewhere (11, 12).

The research question was operationalized by using inclusion and exclusion criteria for population, exposure, comparator groups, and outcomes (Table 1). Our primary outcome was the relative risk of infection, which ideally is measured longitudinally by the seroconversion rate of childcare workers compared with the general population. In order to determine the secondary outcomes, we included studies that used a cross-sectional design to determine vaccination rates or antibody seroprevalence rates (“seropositivity”) in childcare workers. We restricted ourselves to studies published from the year 2000 onwards, in order to obtain recent results that were not biased by any cohort effects. Earlier studies were included in the review by Elsner et al (2009) (13).

Inclusion and exclusion criteria for systematic review
Table 1
Inclusion and exclusion criteria for systematic review

We conducted our systematic literature search in the databases PubMed and Embase (eTable 1) on 12 February 2019. Further information on the method, hand search, data extraction, and quality evaluation can be found in eBox 1 and eTable 2.

Instrument for evaluating the quality of studies included in the systematic review
eTable 2a
Instrument for evaluating the quality of studies included in the systematic review
eTable 2 a continued
eTable 2b
eTable 2 a continued
Assessing the quality of the included studies
Table 2
Assessing the quality of the included studies
Additional information about the systematic literature search
eBox 1
Additional information about the systematic literature search
Search algorithm of the systematic database interrogation
eTable 1
Search algorithm of the systematic database interrogation

The German Health Interview and Examination Survey for Adults and the surveillance of notifiable communicable diseases

In addition to the systematic search, we evaluated data from DEGS1 (14) and from the surveillance of notifiable communicable diseases according to Germany’s Infection Protection Act (Infektionsschutzgesetz, IfSG). Information on study design and data analysis can be found in eBox 2 and eBox 3.

Data analysis of the German Health Interview and Examination Survey for Adults (DEGS1)
eBox 2
Data analysis of the German Health Interview and Examination Survey for Adults (DEGS1)
Evaluation of data from the surveillance of notifiable communicable diseases
eBox 3
Evaluation of data from the surveillance of notifiable communicable diseases

Results

Study selection and characteristics of the systematic search

The flow chart in the eFigure shows the selection process for the 8130 publications identified during the search. Six studies met the inclusion criteria. Three of these were on varicella zoster virus (15, 16, 17), two on rubella virus (15, 18), and one each on hepatitis A virus (HAV) (19) and Bordetella pertussis (20). All included studies had a cross-sectional design and simultaneously collected data on immune status and/or vaccination status. We therefore did not investigate infection rates or infection risks. The study characteristics and quality evaluations are listed in Table 2 and eTable 3, and the study descriptions can be found in eBox 4.

Results of the systematic review and the German Health Interview and Examination Survey for Adults (DEGS1)
Table 3
Results of the systematic review and the German Health Interview and Examination Survey for Adults (DEGS1)
Description of the studies in the systematic review
eBox 4
Description of the studies in the systematic review
Selection process for publications
eFigure
Selection process for publications
Characteristics of the included studies
eTable 3
Characteristics of the included studies

The German Health Interview and Examination Survey for Adults

The characteristics of the study population are summarized in eTable 4. One hundred twenty-six female participants (3.4%) reported that they were childcare workers. High seroprevalence rates were found for measles, mumps, rubella (MMR), with no differences between the exposure group and the reference group (Table 3, eTable 5, eTable 6). Of childcare workers under the age of 30 years, 15.7% were seronegative with regard to measles and 18.9% with regard to mumps, and therefore at risk of infection. More childcare workers up to the age of 29 years were seropositive with regard to HAV than in the reference group (62.9% versus 36.0), and their vaccination rates were higher (66.0% versus 38.9%). Just under 80% of childcare workers had not received the pertussis vaccine in the preceding 10 years.

Relative risk in community facilities caring for minors versus general population, 2016–2019
Table 4
Relative risk in community facilities caring for minors versus general population, 2016–2019
Characteristics of the DEGS1 population
eTable 4
Characteristics of the DEGS1 population
Results of the included studies and DEGS1
eTable 5
Results of the included studies and DEGS1
Expanded table of DEGS1 results
eTable 6
Expanded table of DEGS1 results

The results of the systematic search and the DEGS1 data analysis are summarized in Table 3 and eTable 5.

The surveillance of notifiable diseases in accordance with Germany’s Infection Protection Act (IfSG)

Mumps, pertussis, and varicella were more common among workers in community facilities caring for minors, covered by § 33 of the IfSG, than in the general population between the ages of 15 and 65 years (Table 4). There are indications that HAV and rubella are also more common in such workers, but the effect did not reach significance. No effect was observed for measles (Table 4). In a conservative approach to the data analysis, we included persons for whom no data on a possible job in community facilities caring for minors were available. Here, except for rubella, the risk increases persisted for those employed in community facilities caring for minors (eTable 7). Sex-specific evaluation (eTable 8) showed tendentially higher risks for male employees in community facilities than for their female counterparts.

Risk for workers in German community facilities caring for minors (2016–2019)
eTable 7
Risk for workers in German community facilities caring for minors (2016–2019)
Relative risk for certain infectious diseases in workers of community facilities caring for minors versus the general population in Germany (men and women, 2016–2019)
eTable 8
Relative risk for certain infectious diseases in workers of community facilities caring for minors versus the general population in Germany (men and women, 2016–2019)

Discussion

This systematic review with linked DEGS1 data analysis showed no difference in seroprevalence for mumps, measles, and rubella between childcare workers and the general population. Of the three studies of varicella zoster, one (methodologically limited) analysis showed a significantly higher proportion of female childcare workers who tested seropositive. In a methodologically sound study, positive HAV serology was associated with the length of employment as a childcare worker (odds ratio for every 5 years 1.3; 95% confidence interval [1.0; 1.8]).

According to DEGS1, the vaccination status for HAV and pertussis was higher in female childcare workers than in the female general population (prevalence ratio 1.46 [1.12; 1.90] and 1.57 [1.05; 2.36]); however, 57% of the childcare workers had not been vaccinated against HAV and 77% had not been vaccinated against pertussis.

A substantial proportion of childcare workers were seronegative for HAV (37% of 18–29 year old) and for measles/mumps (16% and 19% of 18–29 year olds, respectively) and therefore at risk of infection.

For childcare workers in community facilities, a consistently raised risk of infection was found for HAV, mumps, rubella, pertussis, and varicella. The risks were tendentially higher for male than for female workers in community facilities. This might indicate greater awareness of the infection risk among female employees.

Regional and disease-specific features

Varicella zoster

The two French studies did not find any differences in seroprevalence, but the Dutch study reported by van Rijckevorsel et al. (17) showed a higher proportion of seropositivity for childcare workers in day-care centers than for women in the general population. Varicella vaccination was not provided for childcare workers at the time we conducted our study. The difference in the seroprevalence rates could therefore be explained by occupational exposure. For Germany, the evaluation of surveillance data for notifiable communicable diseases in childcare workers in community facilities for 2016–19 showed an increased risk of infection with varicella. Since 2009, two-dose vaccination has been generally recommended for children in this country (21). Currently in Germany, 87.8% of children starting school have received the first and 84.3% the second varicella vaccination (22). This meant that the incidence was substantially reduced (23), but the duration of vaccine protection after two doses and the effects on the development of passive immunity in infants remain uncertain (23, 24).

Rubella

Rubella has been considered eliminated in the entire Americas region since 2005 (25), but rubella infections can still re-occur. Although Canada continues to recommend the vaccination of children and childcare workers (26), the methodologically adequate Canadian study found that 4–20% of female childcare workers of childbearing age tested seronegative (18). In the study from France (15), almost all female childcare workers and comparator persons tested seropositive, with a tendency for fewer childcare workers to have been vaccinated against rubella. In France as in Germany, rubella remains endemic (10). In Germany, 12 cases of congenital rubella infection have been notified since 2001; since 2015 no further cases have been reported (27). But the risk remains: In the past 4 years, 14 cases of rubella infection have been reported among persons working in community facilities. This translates into a risk increase of 47% in this occupational group compared with the general population, although the difference is not statistically significant.

Hepatitis A

HAV seroconversion mostly does not occur in children of day-care age; only 0.8–3.4% of Canadian children up to age 13 years (28) and 7.2% of German children aged up to 6 years (29) tested seropositive for HAV. In outbreak situations, an increased risk of infection has been described for day-care centers (30, 31). According to the DEGS1 results, a higher proportion of 18- to 29-year-old childcare workers than of women in the general population had been vaccinated and tested seropositive for HAV. Nevertheless, an average of 50.6–64.4% of childcare workers had no HAV antibodies, and this proportion was even higher in certain subpopulations: 84.1% of childcare workers born in Canada (19) and 65.2–72.4% of German female childcare workers aged between 30 and 49 years (14). An association was found between the length of time spent in the job and HAV seropositivity (19). Furthermore, the analysis of surveillance data for notifiable disease in Germany found a 21% increase in the risk of being infected with HAV for workers in community facilities.

Pertussis

A greater proportion of the childcare workers than of persons in the general population had been vaccinated (in the USA, 45.8% [20] against 31.7% [32]; in Germany, 22.5% against 14.3% [14]); however, the data also indicated that a high proportion of childcare workers had not received a pertussis booster vaccination in the preceding 10 years. Since the protection conferred by the pertussis vaccine mostly lasts no longer than 5–7 years after vaccination (33, 34, 35, 36, e1), these childcare workers are at risk of infection. As a matter of fact, the German surveillance data indicated that the risk of pertussis for workers in community facilities is roughly double than in the general population.

Measles and mumps

The seroprevalence rates for measles and mumps in Germany were high in both the exposure group and the reference group (86–90%). However, 3–16% of female childcare workers had no measles antibodies. Almost one in five female childcare workers tested seronegative for measles and mumps. The risk of mumps infection was almost three times higher for workers in community facilities. The risk of infection was not increased for measles, however. One possible explanation for the differences in risk is the decrease in protection offered by the mumps vaccine over time (37, 38).

Lack of immunity in childcare workers

Overall, the results indicate that a substantial proportion of childcare workers are at risk of infection. Possible reasons for the lack of immunity include inadequate occupational healthcare arrangements and insufficient awareness among childcare workers of the importance of vaccine protection.

Strengths and limitations

The main strengths of this article lie in the systematic approach to the review: The study protocol was drawn up and published a priori. The literature search on the basis of a sensitive search was carried out by two scientists independently of one another, as was the quality evaluation.

Because of the low number of studies, the results of the review should be interpreted with caution. Only two studies (18, 19) showed a low risk for bias. One of these two high-quality studies (19) found an increased risk of infection with HAV for female childcare workers. The cross-sectional design of the reviewed studies means that it is not possible to pinpoint the date of seroconversion. The individual patients’ medical histories or vaccination histories, the most important factors influencing seropositivity, had not been asked about at all or only to an unsatisfactory degree. There is a risk of recall bias due to the self-reporting of vaccination history. Furthermore, there was mostly no adequate description of occupational characteristics and socioeconomic background Relevant confounders, such as travel abroad or whether the participant had children of their own, were not considered. In some studies (15, 16, 17), all childcare workers were included, independently of their contact with children. The study populations investigated to date have consisted almost exclusively of women. Men are increasingly working in child care (39) and should be included to a greater extent in the future.

In 2013, compulsory notification was introduced for all of the communicable diseases reported in this review. One difficulty in assessing risks on the basis of surveillance data lay in finding a suitable denominator for all workers in community facilities. Appropriate employee numbers for children’s residential institutions or holiday camps were not available, which means that our estimates of the infection risk may be slightly too high. The inclusion of teaching staff who had contact with children above the age of 6 years and adolescents in the surveillance of notifiable communicable diseases may have led to underestimation of the risks involved in working at day-care centers.

Implications for research

Future studies should determine childcare workers’ serostatus before they start their jobs, to enable later risk assessment according to their duration of employment and their specific activities, taking relevant confounders into account. The inclusion of appropriate comparator groups is crucial.

Occupational and infection protection in Germany

In the occupational area of children’s preschool education, the increased risk of infection mandates the duty of prevention, in accordance with the German Labor Protection Act and the Ordinance on Occupational Health Care. Before starting a job, and thereafter at regular intervals, childcare workers have to be educated about their immunoprotection. The provision of vaccinations is integral not only to general healthcare but also to workplace protection measures for which the employer is responsible. Seronegative women of childbearing age are at risk of pregnancy complications and connatal infections. This means that the provisions of the German Maternity Protection Act also apply. In the case of justified suspicion of an occupational (also connatal) infection, a duty of disclosure exists in the context of statutory occupational accident insurance.

The measures of Germany’s Infection Protection Act (IfSG) for children’s day-care centers to date include a temporary work ban for childcare workers with MMR, varicella, or pertussis (§ 34 IfSG), as well as a ban on entering a facility in the case of a measles outbreak unless immunity has been confirmed (§ 28 section 2 IfSG).

Since the diseases we have been discussing are highly contagious, and infection can be transmitted before symptoms develop, the existing legal provisions do not yet ensure the effective prevention of disease outbreaks in day-care centers. Strengthening prevention by means of vaccination, as was achieved for medical hospitals/clinics and facilities by the German Prevention Act, could help attain this goal. In this setting, employers are permitted to collect information on the vaccination status and serostatus of their employees in order to decide about the start date or nature of employment if the diseases are vaccine preventable (§ 23a IfSG).

Conclusions

The results of our study show that working in children’s day-care centers and schools is associated with a higher risk of infection with hepatitis A, mumps, rubella, pertussis, and varicella. We also found indications that childcare workers in day-care centers are lacking immunity against HAV, pertussis, and mumps, as well as—especially for female childcare workers of childbearing age—measles and rubella. Appropriate advice from a pediatrician and a primary-care physician before starting a new job is therefore very important in prevention of risk, as are occupational healthcare services providing clear information and vaccination advice. Family physicians and gynecologists know their patients’ occupations and should work towards effective vaccination protection.

Funding
This study received financial funding from the Professional Association of Health and Welfare Services (BGW).

Acknowledgments
We wish to thank the Robert Koch Institute for giving us access to the DEGS1 data set and surveillance data, as well as its support in analyzing these.

In particular, we thank Dr Antje Gößwald and Dr Dorothea Matysiak-Klose.

Conflict of interest statement
The authors declare that no conflict of interest exists

Manuscript received on 2 August 2019, revised version accepted on 19 March 2020.

Translated from the original German by Birte Twisselmann, PhD.

Corresponding author
Dr. rer. medic. Karla Romero Starke, MSc.
Institut und Poliklinik für Arbeits- und Sozialmedizin
Medizinische Fakultät Carl Gustav Carus
Technische Universität Dresden
Fetscherstr. 74
01307 Dresden, Germany
karla.romero_starke@tu-dresden.de

Cite this as
Kofahl M, Romero Starke K, Hellenbrand W, Freiberg A, Schubert M,
Schmauder S, Groß ML, Hegewald J, Kämpf D, Stranzinger J, Nienhaus A,
Seidler A: Vaccine-preventable infections in childcare workers—
a systematic review and analysis of the DEGS1 study and of notifiable disease
surveillance data. Dtsch Arztebl Int 2020; 117: 365–72.
DOI: 10.3238/arztebl.2020.0365

Supplementary material

For eReferences please refer to:
www.aerzteblatt-international.de/ref2120

eTables, eBoxes, eFigure:
www.aerzteblatt-international.de/20m0365

1.
Robert Koch-Institut: SurvStat@RKI 2.0, www.survstat.rki.de (last accessed on 14 November 2019).
2.
European Centre for Disease Prevention and Control: Pertussis. Annual epidemiological report for 2017. Stockholm: ECDC 2019.
3.
European Centre for Disease Prevention and Control: Who is at risk for measles in the EU/EEA? Identifying susceptible groups to close immunity gaps towards measles elimination. Stockholm: ECDC; 2019.
4.
Centers for Disease Control and Prevention: Epidemiology and prevention of vaccine-preventable diseases. 13 edition. Washington D. C.: Public Health Foundation 2015.
5.
European Centre for Disease Prevention and Control (ECDC): Vaccine schedules in all countries of the European Union www.vaccine-schedule.ecdc.europa.eu/ (last accessed on 28 June 2019).
6.
Bitzegeio J, Majowicz S, Matysiak-Klose D, Sagebiel D, Werber D: Estimating age-specific vaccine effectiveness using data from a large measles outbreak in Berlin, Germany, 2014/15: evidence for waning immunity. Euro Surveill 2019; 24 CrossRef MEDLINE PubMed Central
7.
Eberhart-Phillips JE, Frederick PD, Baron RC, Mascola L: Measles in pregnancy: a descriptive study of 58 cases. Obstet Gynecol 1993; 82: 797–801.
8.
Enders M, Biber M, Exler S: Measles, mumps and rubella virus infection in pregnancy. Possible adverse effects on pregnant women, pregnancy outcome and the fetus. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2007; 50: 1393–8 CrossRef MEDLINE
9.
Trotta M, Borchi B, Niccolai A, et al.: Epidemiology, management and outcome of varicella in pregnancy: a 20-year experience at the Tuscany Reference Centre for Infectious Diseases in Pregnancy. Infection 2018; 46: 693–9 CrossRef MEDLINE
10.
World Health Organization Regional Office for Europe: Eighth meeting of the European Regional Verification Commission for Measles and Rubella Elimination (RVC). 2019. www.euro.who.int/__data/assets/pdf_file/0019/413236/8th-RVC-Report.pdf?ua=1 (last accessed on 7 April 2020).
11.
Romero Starke K, Kofahl M, Freiberg A, et al.: Are daycare workers at a higher risk of parvovirus B19 infection? A systematic review and meta-analysis. Int J Environ Res Public Health 2019; 16 CrossRef MEDLINE PubMed Central
12.
Romero Starke K, Kofahl M, Freiberg A, et al.: The risk of cytomegalovirus infection in daycare workers: a systematic review and meta-analysis. Int Arch Occup Environ Health 2020; 93: 11–28 CrossRef MEDLINE
13.
Elsner G, Petereit-Haack G, Nienhaus A: Berufsbedingte Infektionen bei Erzieherinnen und Erziehern in Kindergärten. Zentralblatt für Arbeitsmedizin, Arbeitsschutz und Ergonomie 2009; 59: 34–42 CrossRef
14.
Robert Koch-Institut: Studie zur Gesundheit Erwachsener in Deutschland (DEGS1). https://edoc.rki.de/handle/176904/6172# (last accessed on 7 April 2020).
15.
De Villemeur AB, Gratacap-Cavallier B, Casey R, et al.: Occupational risk for cytomegalovirus, but not for parvovirus B19 in child-care personnel in France. J Infect 2011; 63: 457–67 CrossRef MEDLINE
16.
Reignier F, Romano L, Thiry N, et al.: Varicella-zoster virus seroprevalence in nursery and day-care workers in Lyon (France). Med Mal Infect 2005; 35: 192–6 CrossRef MEDLINE
17.
van Rijckevorsel GGC, Bovée LPJ, Damen M, Sonder GJ, van der Loeff MFS, van den Hoek A: Increased seroprevalence of IgG-class antibodies against cytomegalovirus, parvovirus B19, and varicella-zoster virus in women working in child day care. BMC Public Health 2012; 12: 475 CrossRef MEDLINE PubMed Central
18.
Gyorkos TW, Beliveau C, Rahme E, Muecke C, Joseph S, Soto JC: High rubella seronegativity in daycare educators. Clin Invest Med 2005; 28: 105–11.
19.
Muecke CJ, Beliveau C, Rahme E, Soto JC, Gyorkos TW: Hepatitis A seroprevalence and risk factors among day-care educators. Clin Invest Med 2004; 27: 259–64.
20.
Rebmann T, Loux TM, Lew D, Wakefield M: Pertussis vaccination among childcare center staff, administrators, and parents: uptake, policies, and beliefs. Matern Child Health J 2018; 22: 166–74 CrossRef MEDLINE
21.
European Centre for Disease Prevention and Control: Varicella vaccination in the European Union. Stockholm: ECDC 2015.
22.
Robert Koch-Institut: Epidemiologisches Bulletin Nr. 16. Berlin: RKI 2018.
23.
Siedler A, Hecht J, Rieck T, Tolksdorf K, Hengel H: [Varicella vaccination in Germany. A provisional appraisal in the context of MMR vaccination]. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2013; 56: 1313–20 CrossRef MEDLINE
24.
Marin M, Meissner HC, Seward JF: Varicella prevention in the United States: a review of successes and challenges. Pediatrics 2008; 122: e744–51 CrossRef MEDLINE
25.
Pan American Health Association: Americas region is declared the world‘s first to eliminate rubella. www.paho.org/hq/index.php?option=com_content&view=article&id=10798:2015-americas-free-of-rubella&Itemid=1926&lang=en (last accessed on 18 January 2019).
26.
Government of Canada: Rubella vaccine: Canadian immunization guide. www.canada.ca/en/public-health/services/publications/healthy-living/canadian-immunization-guide-part-4-active-vaccines/page-20-rubella-vaccine.html#p4c19a5 (last accessed on 19 January 2019).
27.
Robert Koch-Institut: Infektionsepidemiologisches Jahrbuch meldepflichtiger Krankheiten für 2017. Berlin: RKI 2018.
28.
Duval B, De Serres G, Ochnio J, Scheifele D, Gilca V: Nationwide canadian study of hepatitis a antibody prevalence among children eight to thirteen years old. Pediatr Infect Dis J 2005; 24: 514–9 CrossRef MEDLINE
29.
Michaelis K, Poethko-Muller C, Kuhnert R, Stark K, Faber M: Hepatitis A virus infections, immunisations and demographic determinants in children and adolescents, Germany. Sci Rep 2018; 8: 16696 CrossRef MEDLINE PubMed Central
30.
Jackson LA, Stewart LK, Solomon SL, et al.: Risk of infection with hepatitis A, B or C, cytomegalovirus, varicella or measles among child care providers. Pediatr Infect Dis J 1996; 15: 584–9 CrossRef MEDLINE
31.
Venczel LV, Desai MM, Vertz PD, et al.: The role of child care in a community-wide outbreak of hepatitis A. Pediatrics 2001; 108: E78 CrossRef MEDLINE
32.
Centers for Disease Control and Prevention (CDC): Vaccination coverage among adults in the United States., National Health Interview Survey, 2017. www.cdc.gov/vaccines/imz-managers/coverage/adultvaxview/pubs-resources/NHIS-2017.html (last accessed on 14 June 2019).
33.
McGirr A, Fisman DN: Duration of pertussis immunity after DTaP immunization: a meta-analysis. Pediatrics 2015; 135: 331–43 CrossRef MEDLINE
34.
Cherry JD: Epidemic pertussis and acellular pertussis vaccine failure in the 21st Century. Pediatrics 2015; 135: 1130–2 CrossRef MEDLINE
35.
Acosta AM, DeBolt C, Tasslimi A, et al.: Tdap vaccine effectiveness in adolescents during the 2012 Washington State pertussis epidemic. Pediatrics 2015; 135: 981–9 CrossRef MEDLINE PubMed Central
36.
Klein NP, Bartlett J, Fireman B, Baxter R: Waning Tdap effectiveness in adolescents. Pediatrics 2016; 137: e20153326 CrossRef MEDLINE
37.
Lewnard JA, Grad YH: Vaccine waning and mumps re-emergence in the United States. Sci Transl Med 2018; 10: eaao5945 CrossRef MEDLINE PubMed Central
38.
Bankamp B, Hickman C, Icenogle JP, Rota PA: Successes and challenges for preventing measles, mumps and rubella by vaccination. Curr Opin Virol 2019; 34: 110–6 CrossRef MEDLINE
39.
OECD: Good Practice for Good Jobs in Early Childhood Education and Care. Paris: OECD Publishing 2019.
e2.
Moher D, Liberati A, Tetzlaff J, Altman DG, Group P: Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 2009; 339: b2535 CrossRef MEDLINE PubMed Central
e3.
von Elm E, Altman DG, Egger M, et al.: Strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. BMJ 2007; 335: 806–8 CrossRef MEDLINEPubMed Central
e4.
Bakkalbasi N, Bauer K, Glover J, Wang L: Three options for citation tracking: Google Scholar, Scopus and Web of Science. Biomed Digit Libr 2006; 3: 7 CrossRef MEDLINE PubMed Central
e5.
Giles J: Science in the web age: start your engines. Nature 2005; 438: 554–5 CrossRef MEDLINE
e6.
Ijaz S, Verbeek J, Seidler A, et al.: Night-shift work and breast cancer—a systematic review and meta-analysis. Scand J Work Environ Health 2013; 39: 431–47 CrossRef CrossRef
e7.
Scottish Intercollegiate Guidelines Network (SIGN): Critical appraisal notes and checklists. www.sign.ac.uk/checklists-and-notes.html (last accessed on 10 December 2018).
e8.
Critical Appraisal Skills Programme (CASP): CASP Appraisal Checklists. https://casp-uk.net/casp-tools-checklists/ (last accessed on 10 December 2018).
e9.
Kamtsiuris P, Lange M, Hoffmann R, et al.: Die erste Welle der Studie zur Gesundheit Erwachsener in Deutschland (DEGS1). Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2013; 56: 620–30 CrossRef MEDLINE
e10.
Scheidt-Nave C, Kamtsiuris P, Gosswald A, et al.: German health interview and examination survey for adults (DEGS)—design, objectives and implementation of the first data collection wave. BMC Public Health 2012; 12: 730 CrossRef MEDLINE PubMed Central
e11.
Gößwald A, Lange M, Dölle R, Hölling H: Die erste Welle der Studie zur Gesundheit Erwachsener in Deutschland (DEGS1). Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2013; 56: 611–9 CrossRef MEDLINE
e12.
Poethko-Müller C, Schmitz R: Impfstatus von Erwachsenen in Deutschland. Ergebnisse der Studie zur Gesundheit Erwachsener in Deutschland (DEGS1). Bundesgesundheitsbl 2013. 56: 845–5 CrossRef MEDLINE
e13.
Poethko-Müller C, Zimmermann R, Hamouda O, et al.: Die Seroepidemiologie der Hepatitis A, B und C in Deutschland. Ergebnisse der Studie zur Gesundheit Erwachsener in Deutschland (DEGS1). Bundesgesundheitsbl 2013. 56:707–15 CrossRef MEDLINE
e14.
Bundesagentur für Arbeit: Klassifikation der Berufe 2010 – Band 1: Systematischer und alphabetischer Teil mit Erläuterungen. Nürnberg: Bundesagentur für Arbeit 2011.
e15.
Statistisches Bundesamt: Statistiken der Kinder- und Jugendhilfe/Kinder und tätige Personen in Tageseinrichtungen und in öffentlich geförderter Kindertagespflege www.destatis.de/GPStatistik/receive/DESerie_serie_00002286 (last accessed on 28 February 2020).
e16.
Statistisches Bundesamt: Fachserie 11, Bildung und Kultur. 1, Allgemeibildende Schulen. www.destatis.de/GPStatistik/receive/DESerie_serie_00000110 (last accessed on 28 February 2020).
e17.
Statistisches Bundesamt: Fachserie 11, Bildung und Kultur. 2, Berufliche Schulen. www.destatis.de/GPStatistik/receive/DESerie_serie_00000111 (last accessed on 28 February 2020).
*Joint first authors
Institute and Polyclinic for Occupational and Social Medicine (IPAS), Faculty of Medicine Carl Gustav Carus, Technische Universität Dresden, Dresden: Marlen Kofahl, MPH; Dr. rer. medic. Karla Romero Starke, Dr. rer. medic. Alice Freiberg, MPH; Dr. rer. nat. Melanie Schubert, Dr. med. Stefanie Schmauder, Mascha Luisa Groß, Dr. rer. biol. hum. Janice Hegewald, Dr. med. Daniel Kämpf, Prof. Dr. med. Andreas Seidler, MPH
Immunization Unit, Department of Infectious Disease Epidemiology, Robert Koch Institute, Berlin: Dr. med. Wiebke Hellenbrand, MPH
Institution for Statutory Social Accident Insurance and Prevention in the Health Care and Welfare Services (BGW), Basic Principles of Prevention and Rehabilitation,Section Occupational Health, Hamburg, Germany: Dr. med. Johanna Stranzinger, Prof. Dr. med. Albert Nienhaus, MPH
Competence Centre for Epidemiology and Health Services Research for Healthcare Professionals (CVcare), University Medical Center Hamburg-Eppendorf (UKE), Hamburg: Prof. Dr. med. Albert Nienhaus, MPH
Inclusion and exclusion criteria for systematic review
Table 1
Inclusion and exclusion criteria for systematic review
Assessing the quality of the included studies
Table 2
Assessing the quality of the included studies
Results of the systematic review and the German Health Interview and Examination Survey for Adults (DEGS1)
Table 3
Results of the systematic review and the German Health Interview and Examination Survey for Adults (DEGS1)
Relative risk in community facilities caring for minors versus general population, 2016–2019
Table 4
Relative risk in community facilities caring for minors versus general population, 2016–2019
Additional information about the systematic literature search
eBox 1
Additional information about the systematic literature search
Data analysis of the German Health Interview and Examination Survey for Adults (DEGS1)
eBox 2
Data analysis of the German Health Interview and Examination Survey for Adults (DEGS1)
Evaluation of data from the surveillance of notifiable communicable diseases
eBox 3
Evaluation of data from the surveillance of notifiable communicable diseases
Description of the studies in the systematic review
eBox 4
Description of the studies in the systematic review
Selection process for publications
eFigure
Selection process for publications
Search algorithm of the systematic database interrogation
eTable 1
Search algorithm of the systematic database interrogation
Instrument for evaluating the quality of studies included in the systematic review
eTable 2a
Instrument for evaluating the quality of studies included in the systematic review
eTable 2 a continued
eTable 2b
eTable 2 a continued
Characteristics of the included studies
eTable 3
Characteristics of the included studies
Characteristics of the DEGS1 population
eTable 4
Characteristics of the DEGS1 population
Results of the included studies and DEGS1
eTable 5
Results of the included studies and DEGS1
Expanded table of DEGS1 results
eTable 6
Expanded table of DEGS1 results
Risk for workers in German community facilities caring for minors (2016–2019)
eTable 7
Risk for workers in German community facilities caring for minors (2016–2019)
Relative risk for certain infectious diseases in workers of community facilities caring for minors versus the general population in Germany (men and women, 2016–2019)
eTable 8
Relative risk for certain infectious diseases in workers of community facilities caring for minors versus the general population in Germany (men and women, 2016–2019)
1.Robert Koch-Institut: SurvStat@RKI 2.0, www.survstat.rki.de (last accessed on 14 November 2019).
2.European Centre for Disease Prevention and Control: Pertussis. Annual epidemiological report for 2017. Stockholm: ECDC 2019.
3.European Centre for Disease Prevention and Control: Who is at risk for measles in the EU/EEA? Identifying susceptible groups to close immunity gaps towards measles elimination. Stockholm: ECDC; 2019.
4.Centers for Disease Control and Prevention: Epidemiology and prevention of vaccine-preventable diseases. 13 edition. Washington D. C.: Public Health Foundation 2015.
5.European Centre for Disease Prevention and Control (ECDC): Vaccine schedules in all countries of the European Union www.vaccine-schedule.ecdc.europa.eu/ (last accessed on 28 June 2019).
6.Bitzegeio J, Majowicz S, Matysiak-Klose D, Sagebiel D, Werber D: Estimating age-specific vaccine effectiveness using data from a large measles outbreak in Berlin, Germany, 2014/15: evidence for waning immunity. Euro Surveill 2019; 24 CrossRef MEDLINE PubMed Central
7.Eberhart-Phillips JE, Frederick PD, Baron RC, Mascola L: Measles in pregnancy: a descriptive study of 58 cases. Obstet Gynecol 1993; 82: 797–801.
8.Enders M, Biber M, Exler S: Measles, mumps and rubella virus infection in pregnancy. Possible adverse effects on pregnant women, pregnancy outcome and the fetus. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2007; 50: 1393–8 CrossRef MEDLINE
9.Trotta M, Borchi B, Niccolai A, et al.: Epidemiology, management and outcome of varicella in pregnancy: a 20-year experience at the Tuscany Reference Centre for Infectious Diseases in Pregnancy. Infection 2018; 46: 693–9 CrossRef MEDLINE
10.World Health Organization Regional Office for Europe: Eighth meeting of the European Regional Verification Commission for Measles and Rubella Elimination (RVC). 2019. www.euro.who.int/__data/assets/pdf_file/0019/413236/8th-RVC-Report.pdf?ua=1 (last accessed on 7 April 2020).
11.Romero Starke K, Kofahl M, Freiberg A, et al.: Are daycare workers at a higher risk of parvovirus B19 infection? A systematic review and meta-analysis. Int J Environ Res Public Health 2019; 16 CrossRef MEDLINE PubMed Central
12.Romero Starke K, Kofahl M, Freiberg A, et al.: The risk of cytomegalovirus infection in daycare workers: a systematic review and meta-analysis. Int Arch Occup Environ Health 2020; 93: 11–28 CrossRef MEDLINE
13.Elsner G, Petereit-Haack G, Nienhaus A: Berufsbedingte Infektionen bei Erzieherinnen und Erziehern in Kindergärten. Zentralblatt für Arbeitsmedizin, Arbeitsschutz und Ergonomie 2009; 59: 34–42 CrossRef
14.Robert Koch-Institut: Studie zur Gesundheit Erwachsener in Deutschland (DEGS1). https://edoc.rki.de/handle/176904/6172# (last accessed on 7 April 2020).
15.De Villemeur AB, Gratacap-Cavallier B, Casey R, et al.: Occupational risk for cytomegalovirus, but not for parvovirus B19 in child-care personnel in France. J Infect 2011; 63: 457–67 CrossRef MEDLINE
16.Reignier F, Romano L, Thiry N, et al.: Varicella-zoster virus seroprevalence in nursery and day-care workers in Lyon (France). Med Mal Infect 2005; 35: 192–6 CrossRef MEDLINE
17.van Rijckevorsel GGC, Bovée LPJ, Damen M, Sonder GJ, van der Loeff MFS, van den Hoek A: Increased seroprevalence of IgG-class antibodies against cytomegalovirus, parvovirus B19, and varicella-zoster virus in women working in child day care. BMC Public Health 2012; 12: 475 CrossRef MEDLINE PubMed Central
18.Gyorkos TW, Beliveau C, Rahme E, Muecke C, Joseph S, Soto JC: High rubella seronegativity in daycare educators. Clin Invest Med 2005; 28: 105–11.
19.Muecke CJ, Beliveau C, Rahme E, Soto JC, Gyorkos TW: Hepatitis A seroprevalence and risk factors among day-care educators. Clin Invest Med 2004; 27: 259–64.
20.Rebmann T, Loux TM, Lew D, Wakefield M: Pertussis vaccination among childcare center staff, administrators, and parents: uptake, policies, and beliefs. Matern Child Health J 2018; 22: 166–74 CrossRef MEDLINE
21.European Centre for Disease Prevention and Control: Varicella vaccination in the European Union. Stockholm: ECDC 2015.
22.Robert Koch-Institut: Epidemiologisches Bulletin Nr. 16. Berlin: RKI 2018.
23.Siedler A, Hecht J, Rieck T, Tolksdorf K, Hengel H: [Varicella vaccination in Germany. A provisional appraisal in the context of MMR vaccination]. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2013; 56: 1313–20 CrossRef MEDLINE
24.Marin M, Meissner HC, Seward JF: Varicella prevention in the United States: a review of successes and challenges. Pediatrics 2008; 122: e744–51 CrossRef MEDLINE
25.Pan American Health Association: Americas region is declared the world‘s first to eliminate rubella. www.paho.org/hq/index.php?option=com_content&view=article&id=10798:2015-americas-free-of-rubella&Itemid=1926&lang=en (last accessed on 18 January 2019).
26.Government of Canada: Rubella vaccine: Canadian immunization guide. www.canada.ca/en/public-health/services/publications/healthy-living/canadian-immunization-guide-part-4-active-vaccines/page-20-rubella-vaccine.html#p4c19a5 (last accessed on 19 January 2019).
27.Robert Koch-Institut: Infektionsepidemiologisches Jahrbuch meldepflichtiger Krankheiten für 2017. Berlin: RKI 2018.
28.Duval B, De Serres G, Ochnio J, Scheifele D, Gilca V: Nationwide canadian study of hepatitis a antibody prevalence among children eight to thirteen years old. Pediatr Infect Dis J 2005; 24: 514–9 CrossRef MEDLINE
29.Michaelis K, Poethko-Muller C, Kuhnert R, Stark K, Faber M: Hepatitis A virus infections, immunisations and demographic determinants in children and adolescents, Germany. Sci Rep 2018; 8: 16696 CrossRef MEDLINE PubMed Central
30.Jackson LA, Stewart LK, Solomon SL, et al.: Risk of infection with hepatitis A, B or C, cytomegalovirus, varicella or measles among child care providers. Pediatr Infect Dis J 1996; 15: 584–9 CrossRef MEDLINE
31.Venczel LV, Desai MM, Vertz PD, et al.: The role of child care in a community-wide outbreak of hepatitis A. Pediatrics 2001; 108: E78 CrossRef MEDLINE
32.Centers for Disease Control and Prevention (CDC): Vaccination coverage among adults in the United States., National Health Interview Survey, 2017. www.cdc.gov/vaccines/imz-managers/coverage/adultvaxview/pubs-resources/NHIS-2017.html (last accessed on 14 June 2019).
33.McGirr A, Fisman DN: Duration of pertussis immunity after DTaP immunization: a meta-analysis. Pediatrics 2015; 135: 331–43 CrossRef MEDLINE
34.Cherry JD: Epidemic pertussis and acellular pertussis vaccine failure in the 21st Century. Pediatrics 2015; 135: 1130–2 CrossRef MEDLINE
35.Acosta AM, DeBolt C, Tasslimi A, et al.: Tdap vaccine effectiveness in adolescents during the 2012 Washington State pertussis epidemic. Pediatrics 2015; 135: 981–9 CrossRef MEDLINE PubMed Central
36.Klein NP, Bartlett J, Fireman B, Baxter R: Waning Tdap effectiveness in adolescents. Pediatrics 2016; 137: e20153326 CrossRef MEDLINE
37.Lewnard JA, Grad YH: Vaccine waning and mumps re-emergence in the United States. Sci Transl Med 2018; 10: eaao5945 CrossRef MEDLINE PubMed Central
38.Bankamp B, Hickman C, Icenogle JP, Rota PA: Successes and challenges for preventing measles, mumps and rubella by vaccination. Curr Opin Virol 2019; 34: 110–6 CrossRef MEDLINE
39.OECD: Good Practice for Good Jobs in Early Childhood Education and Care. Paris: OECD Publishing 2019.
e1.Robert Koch-Institut: Epidemiologisches Bulletin Nr. 34. Berlin: RKI 2019 .
e2.Moher D, Liberati A, Tetzlaff J, Altman DG, Group P: Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 2009; 339: b2535 CrossRef MEDLINE PubMed Central
e3.von Elm E, Altman DG, Egger M, et al.: Strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. BMJ 2007; 335: 806–8 CrossRef MEDLINEPubMed Central
e4.Bakkalbasi N, Bauer K, Glover J, Wang L: Three options for citation tracking: Google Scholar, Scopus and Web of Science. Biomed Digit Libr 2006; 3: 7 CrossRef MEDLINE PubMed Central
e5.Giles J: Science in the web age: start your engines. Nature 2005; 438: 554–5 CrossRef MEDLINE
e6.Ijaz S, Verbeek J, Seidler A, et al.: Night-shift work and breast cancer—a systematic review and meta-analysis. Scand J Work Environ Health 2013; 39: 431–47 CrossRef CrossRef
e7.Scottish Intercollegiate Guidelines Network (SIGN): Critical appraisal notes and checklists. www.sign.ac.uk/checklists-and-notes.html (last accessed on 10 December 2018).
e8.Critical Appraisal Skills Programme (CASP): CASP Appraisal Checklists. https://casp-uk.net/casp-tools-checklists/ (last accessed on 10 December 2018).
e9.Kamtsiuris P, Lange M, Hoffmann R, et al.: Die erste Welle der Studie zur Gesundheit Erwachsener in Deutschland (DEGS1). Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2013; 56: 620–30 CrossRef MEDLINE
e10.Scheidt-Nave C, Kamtsiuris P, Gosswald A, et al.: German health interview and examination survey for adults (DEGS)—design, objectives and implementation of the first data collection wave. BMC Public Health 2012; 12: 730 CrossRef MEDLINE PubMed Central
e11.Gößwald A, Lange M, Dölle R, Hölling H: Die erste Welle der Studie zur Gesundheit Erwachsener in Deutschland (DEGS1). Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2013; 56: 611–9 CrossRef MEDLINE
e12.Poethko-Müller C, Schmitz R: Impfstatus von Erwachsenen in Deutschland. Ergebnisse der Studie zur Gesundheit Erwachsener in Deutschland (DEGS1). Bundesgesundheitsbl 2013. 56: 845–5 CrossRef MEDLINE
e13.Poethko-Müller C, Zimmermann R, Hamouda O, et al.: Die Seroepidemiologie der Hepatitis A, B und C in Deutschland. Ergebnisse der Studie zur Gesundheit Erwachsener in Deutschland (DEGS1). Bundesgesundheitsbl 2013. 56:707–15 CrossRef MEDLINE
e14.Bundesagentur für Arbeit: Klassifikation der Berufe 2010 – Band 1: Systematischer und alphabetischer Teil mit Erläuterungen. Nürnberg: Bundesagentur für Arbeit 2011.
e15.Statistisches Bundesamt: Statistiken der Kinder- und Jugendhilfe/Kinder und tätige Personen in Tageseinrichtungen und in öffentlich geförderter Kindertagespflege www.destatis.de/GPStatistik/receive/DESerie_serie_00002286 (last accessed on 28 February 2020).
e16.Statistisches Bundesamt: Fachserie 11, Bildung und Kultur. 1, Allgemeibildende Schulen. www.destatis.de/GPStatistik/receive/DESerie_serie_00000110 (last accessed on 28 February 2020).
e17.Statistisches Bundesamt: Fachserie 11, Bildung und Kultur. 2, Berufliche Schulen. www.destatis.de/GPStatistik/receive/DESerie_serie_00000111 (last accessed on 28 February 2020).