Publications by authors named "Jacco Wallinga"

108 Publications

Impact of physical distancing measures against COVID-19 on contacts and mixing patterns: repeated cross-sectional surveys, the Netherlands, 2016-17, April 2020 and June 2020.

Euro Surveill 2021 02;26(8)

Department of Biomedical Data Sciences, Leiden University Medical Center, Leiden, the Netherlands.

BackgroundDuring the COVID-19 pandemic, many countries have implemented physical distancing measures to reduce transmission of SARS-CoV-2.AimTo measure the actual reduction of contacts when physical distancing measures are implemented.MethodsA cross-sectional survey was carried out in the Netherlands in 2016-17, in which participants reported the number and age of their contacts the previous day. The survey was repeated among a subsample of the participants in April 2020, after strict physical distancing measures were implemented, and in an extended sample in June 2020, after some measures were relaxed.ResultsThe average number of community contacts per day was reduced from 14.9 (interquartile range (IQR): 4-20) in the 2016-17 survey to 3.5 (IQR: 0-4) after strict physical distancing measures were implemented, and rebounded to 8.8 (IQR: 1-10) after some measures were relaxed. All age groups restricted their community contacts to at most 5, on average, after strict physical distancing measures were implemented. In children, the number of community contacts reverted to baseline levels after measures were eased, while individuals aged 70 years and older had less than half their baseline levels.ConclusionStrict physical distancing measures greatly reduced overall contact numbers, which likely contributed to curbing the first wave of the COVID-19 epidemic in the Netherlands. However, age groups reacted differently when measures were relaxed, with children reverting to normal contact numbers and elderly individuals maintaining restricted contact numbers. These findings offer guidance for age-targeted measures in future waves of the pandemic.
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http://dx.doi.org/10.2807/1560-7917.ES.2021.26.8.2000994DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7908067PMC
February 2021

Delayed rabies post-exposure prophylaxis treatment among Dutch travelers during their stay abroad: a comprehensive analysis.

J Travel Med 2021 Jan 5. Epub 2021 Jan 5.

Department of Infectious Diseases, Leiden University Medical Centre, Leiden, the Netherlands.

Background: After an animal-associated injury (AAI) in rabies-endemic regions, post-exposure prophylaxis (PEP) is needed to prevent infection.1,3 PEP consist of rabies vaccinations (RV) and in some cases also additional rabies immune globulins (RIG). Not always PEP medication, and RIG in particular, is accessible. Along with an increased number of exposure notifications among Dutch travelers, this might lead to treatment delay, and thus to increased health risks. Until now, research mainly focused on factors associated with exposition, but none on which factors are associated with PEP delay. This study aimed to identify which general sample characteristics are associated with PEP delay while being abroad.

Methods: A quantitative retrospective observational study was conducted. The study population consisted of insured Dutch international travelers who actively contacted their medical assistance company (2015-2019) because of an animal-associated injury (AAI) (N = 691). The association between general sample characteristics and delay of different PEP treatments was studied using survival analysis.

Results: Travelers without PrEP had an increased hazard, and therefore a shorter delay, for receiving their first RV as compared to travelers with PrEP (HR:1.11, 95%CI:1.01-1.22). The travelers needing both RV and RIG had a decreased hazard, and therefore a longer delay, as compared to travelers only needing RV (HR:0.81, 95%CI:0.67-0.96). General sample characteristic associated with RIG administration delay was travel destination. Travelers to Central and South America, East Mediterranean and Europe had a decreased hazard, and therefore a longer delay, for receiving RIG treatments relative to travelers to South East Asia (HR:0.31, 95%CI:0.13-0.70; HR:0.34, 95%CI:0.19-0.61; HR:0.46, 95%CI:0.24-0.89; HR:0.48, 95%CI:0.12-0.81 respectively).

Conclusions: Our results suggest that the advice for PrEP should be given based travel destination, as these was found to be the main factor for PEP delay, among travelers going to rabies endemic countries.
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http://dx.doi.org/10.1093/jtm/taaa240DOI Listing
January 2021

Practical considerations for measuring the effective reproductive number, Rt.

PLoS Comput Biol 2020 12 10;16(12):e1008409. Epub 2020 Dec 10.

Department of Ecology and Evolution, University of Chicago, Chicago, IL, United States of America.

Estimation of the effective reproductive number Rt is important for detecting changes in disease transmission over time. During the Coronavirus Disease 2019 (COVID-19) pandemic, policy makers and public health officials are using Rt to assess the effectiveness of interventions and to inform policy. However, estimation of Rt from available data presents several challenges, with critical implications for the interpretation of the course of the pandemic. The purpose of this document is to summarize these challenges, illustrate them with examples from synthetic data, and, where possible, make recommendations. For near real-time estimation of Rt, we recommend the approach of Cori and colleagues, which uses data from before time t and empirical estimates of the distribution of time between infections. Methods that require data from after time t, such as Wallinga and Teunis, are conceptually and methodologically less suited for near real-time estimation, but may be appropriate for retrospective analyses of how individuals infected at different time points contributed to the spread. We advise caution when using methods derived from the approach of Bettencourt and Ribeiro, as the resulting Rt estimates may be biased if the underlying structural assumptions are not met. Two key challenges common to all approaches are accurate specification of the generation interval and reconstruction of the time series of new infections from observations occurring long after the moment of transmission. Naive approaches for dealing with observation delays, such as subtracting delays sampled from a distribution, can introduce bias. We provide suggestions for how to mitigate this and other technical challenges and highlight open problems in Rt estimation.
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http://dx.doi.org/10.1371/journal.pcbi.1008409DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7728287PMC
December 2020

Authors' response: Estimating the generation interval for COVID-19 based on symptom onset data.

Euro Surveill 2020 07;25(29)

Centre for Health Economics Research and Modelling Infectious Diseases (CHERMID), Vaccine and Infectious Disease Institute, University of Antwerp, Antwerp, Belgium.

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http://dx.doi.org/10.2807/1560-7917.ES.2020.25.29.2001269DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7384288PMC
July 2020

Practical considerations for measuring the effective reproductive number, Rt.

medRxiv 2020 Jun 20. Epub 2020 Jun 20.

Department of Ecology and Evolution, University of Chicago, Chicago, IL, USA.

Estimation of the effective reproductive number, R , is important for detecting changes in disease transmission over time. During the COVID-19 pandemic, policymakers and public health officials are using R to assess the effectiveness of interventions and to inform policy. However, estimation of R from available data presents several challenges, with critical implications for the interpretation of the course of the pandemic. The purpose of this document is to summarize these challenges, illustrate them with examples from synthetic data, and, where possible, make methodological recommendations. For near real-time estimation of R , we recommend the approach of Cori et al. (2013), which uses data from before time and empirical estimates of the distribution of time between infections. Methods that require data from after time , such as Wallinga and Teunis (2004), are conceptually and methodologically less suited for near real-time estimation, but may be appropriate for some retrospective analyses. We advise against using methods derived from Bettencourt and Ribeiro (2008), as the resulting R estimates may be biased if the underlying structural assumptions are not met. A challenge common to all approaches is reconstruction of the time series of new infections from observations occurring long after the moment of transmission. Naive approaches for dealing with observation delays, such as subtracting delays sampled from a distribution, can introduce bias. We provide suggestions for how to mitigate this and other technical challenges and highlight open problems in R estimation.
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http://dx.doi.org/10.1101/2020.06.18.20134858DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7325187PMC
June 2020

Evidence for transmission of COVID-19 prior to symptom onset.

Elife 2020 06 22;9. Epub 2020 Jun 22.

Simon Fraser University, Burnaby, Canada.

We collated contact tracing data from COVID-19 clusters in Singapore and Tianjin, China and estimated the extent of pre-symptomatic transmission by estimating incubation periods and serial intervals. The mean incubation periods accounting for intermediate cases were 4.91 days (95%CI 4.35, 5.69) and 7.54 (95%CI 6.76, 8.56) days for Singapore and Tianjin, respectively. The mean serial interval was 4.17 (95%CI 2.44, 5.89) and 4.31 (95%CI 2.91, 5.72) days (Singapore, Tianjin). The serial intervals are shorter than incubation periods, suggesting that pre-symptomatic transmission may occur in a large proportion of transmission events (0.4-0.5 in Singapore and 0.6-0.8 in Tianjin, in our analysis with intermediate cases, and more without intermediates). Given the evidence for pre-symptomatic transmission, it is vital that even individuals who appear healthy abide by public health measures to control COVID-19.
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http://dx.doi.org/10.7554/eLife.57149DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7386904PMC
June 2020

Preferential differences in vaccination decision-making for oneself or one's child in The Netherlands: a discrete choice experiment.

BMC Public Health 2020 Jun 1;20(1):828. Epub 2020 Jun 1.

Centre for Nutrition, Prevention and Healthcare, National Institute for Public Health and the Environment, Bilthoven, The Netherlands.

Background: To optimize the focus of future public information campaigns in The Netherlands promoting the uptake of vaccines among adults and children, we quantified the contribution of several attributes to the vaccination decision.

Method: We performed a discrete choice experiment (DCE) among Dutch adults including six attributes, i.e. vaccine effectiveness, vaccine-preventable burden of disease (specified in severity and frequency), accessibility of vaccination in terms of co-payment and prescription requirements, frequency of mild side-effects, population-level vaccination coverage and local vaccination coverage among family and friends. Participants answered the DCE from their own perspective ('oneself' group) or with regard to a vaccine decision for their youngest child ('child' group). The data was analysed by means of panel mixed logit models.

Results: We included 1547 adult participants (825 'oneself' and 722 'child'). Vaccine effectiveness was the most important attribute in the 'oneself' group, followed by burden of disease (relative importance (RI) 78%) and accessibility (RI 76%). In the 'child' group, burden of disease was most important, but tied closely with vaccine effectiveness (RI 97%). Of less importance was the risk of mild vaccine-related side-effects and both population and local vaccination coverage. Interestingly, participants were more willing to vaccinate when uptake among the population or family and friends was high, indicating that social influence and social norms plays a role.

Conclusions: Vaccine effectiveness and disease severity are key attributes in vaccination decision-making for adults making a decision for themselves and for parents who decide for their children. Hence, public information campaigns for both adult and child vaccination should primarily focus on these two attributes. In addition, reinforcing social norms may be considered.
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http://dx.doi.org/10.1186/s12889-020-08844-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7268356PMC
June 2020

Determination of the time-dependent association between ciprofloxacin consumption and ciprofloxacin resistance using a weighted cumulative exposure model compared with standard models.

J Antimicrob Chemother 2020 08;75(8):2326-2333

Centre for Infectious Disease Control, National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands.

Objectives: To obtain comprehensive insight into the association of ciprofloxacin use at different times in the past with the current risk of detecting resistance.

Methods: This retrospective nested case-control study of ciprofloxacin users used Dutch data from the PHARMO Database Network and one laboratory for the period 2003-14. Cases and controls were selected as patients with an antibiotic susceptibility test (AST) indicating ciprofloxacin resistance or susceptibility, respectively. We performed univariable and multivariable conditional logistic regression analyses, defining time-dependent exposure using standard definitions (current ciprofloxacin use, used 0-30, 31-90, 91-180 and 181-360 days ago) and a flexible weighted cumulative effect (WCE) model with four alternative time windows of past doses (0-30, 0-90, 0-180 and 0-360 days).

Results: The study population consisted of 230 cases and 909 controls. Under the standard exposure definitions, the association of ciprofloxacin use with resistance decreased with time [current use: adjusted OR 6.8 (95% CI 3.6-12.4); used 181-360 days ago: 1.3 (0.8-1.9)]. Under the 90 day WCE model (best-fitting model), more recent doses were more strongly associated with resistance than past doses, as was longer or repeated treatment. The 180 day WCE model, which fitted the data equally well, suggested that doses taken 91-180 days ago were also significantly associated with resistance.

Conclusions: The estimates for the association between ciprofloxacin use at different times and resistance show that ciprofloxacin prescribers should consider ciprofloxacin use 0-180 days ago to ensure that patients receive suitable treatment. The OR of ciprofloxacin resistance could be reduced by eliminating repeated ciprofloxacin prescription within 180 days and by treating for no longer than necessary.
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http://dx.doi.org/10.1093/jac/dkaa141DOI Listing
August 2020

Estimating the generation interval for coronavirus disease (COVID-19) based on symptom onset data, March 2020.

Euro Surveill 2020 04;25(17)

Centre for Health Economics Research and Modelling Infectious Diseases (CHERMID), Vaccine and Infectious Disease Institute, University of Antwerp, Antwerp, Belgium.

BackgroundEstimating key infectious disease parameters from the coronavirus disease (COVID-19) outbreak is essential for modelling studies and guiding intervention strategies.AimWe estimate the generation interval, serial interval, proportion of pre-symptomatic transmission and effective reproduction number of COVID-19. We illustrate that reproduction numbers calculated based on serial interval estimates can be biased.MethodsWe used outbreak data from clusters in Singapore and Tianjin, China to estimate the generation interval from symptom onset data while acknowledging uncertainty about the incubation period distribution and the underlying transmission network. From those estimates, we obtained the serial interval, proportions of pre-symptomatic transmission and reproduction numbers.ResultsThe mean generation interval was 5.20 days (95% credible interval (CrI): 3.78-6.78) for Singapore and 3.95 days (95% CrI: 3.01-4.91) for Tianjin. The proportion of pre-symptomatic transmission was 48% (95% CrI: 32-67) for Singapore and 62% (95% CrI: 50-76) for Tianjin. Reproduction number estimates based on the generation interval distribution were slightly higher than those based on the serial interval distribution. Sensitivity analyses showed that estimating these quantities from outbreak data requires detailed contact tracing information.ConclusionHigh estimates of the proportion of pre-symptomatic transmission imply that case finding and contact tracing need to be supplemented by physical distancing measures in order to control the COVID-19 outbreak. Notably, quarantine and other containment measures were already in place at the time of data collection, which may inflate the proportion of infections from pre-symptomatic individuals.
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http://dx.doi.org/10.2807/1560-7917.ES.2020.25.17.2000257DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7201952PMC
April 2020

Incubation period of 2019 novel coronavirus (2019-nCoV) infections among travellers from Wuhan, China, 20-28 January 2020.

Euro Surveill 2020 02;25(5)

Department of Biomedical Data Sciences, Leiden University Medical Center, Leiden, Netherlands.

A novel coronavirus (2019-nCoV) is causing an outbreak of viral pneumonia that started in Wuhan, China. Using the travel history and symptom onset of 88 confirmed cases that were detected outside Wuhan in the early outbreak phase, we estimate the mean incubation period to be 6.4 days (95% credible interval: 5.6-7.7), ranging from 2.1 to 11.1 days (2.5th to 97.5th percentile). These values should help inform 2019-nCoV case definitions and appropriate quarantine durations.
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http://dx.doi.org/10.2807/1560-7917.ES.2020.25.5.2000062DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7014672PMC
February 2020

Vaccinating children against influenza: overall cost-effective with potential for undesirable outcomes.

BMC Med 2020 01 14;18(1):11. Epub 2020 Jan 14.

Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Antonie Van Leeuwenhoeklaan 9, 3721 MA, Bilthoven, The Netherlands.

Background: The present study aims to assess the cost-effectiveness of an influenza vaccination program for children in the Netherlands. This requires an evaluation of the long-term impact of such a program on the burden of influenza across all age groups, using a transmission model that accounts for the seasonal variability in vaccine effectiveness and the shorter duration of protection following vaccination as compared to natural infection.

Methods: We performed a cost-effectiveness analysis based on a stochastic dynamic transmission model that has been calibrated to reported GP visits with influenza-like illness in the Netherlands over 11 seasons (2003/2004 to 2014/2015). We analyzed the costs and effects of extending the current program with vaccination of children aged 2-16 years at 50% coverage over 20 consecutive seasons. We measured the effects in quality-adjusted life-years (QALYs) and we adopted a societal perspective.

Results: The childhood vaccination program is estimated to have an average incremental cost-effectiveness ratio (ICER) of €3944 per QALY gained and is cost-effective in the general population (across 1000 simulations; conventional Dutch threshold of €20,000 per QALY gained). The childhood vaccination program is not estimated to be cost-effective for the target-group itself with an average ICER of €57,054 per QALY gained. Uncertainty analyses reveal that these ICERs hide a wide range of outcomes. Even though introduction of a childhood vaccination program decreases the number of infections, it tends to lead to larger epidemics: in 23.3% of 1000 simulations, the childhood vaccination program results in an increase in seasons with a symptomatic attack rate larger than 5%, which is expected to cause serious strain on the health care system. In 6.4% of 1000 simulations, the childhood vaccination program leads to a net loss of QALYs. These findings are robust across different targeted age groups and vaccination coverages.

Conclusions: Modeling indicates that childhood influenza vaccination is cost-effective in the Netherlands. However, childhood influenza vaccination is not cost-effective when only outcomes for the children themselves are considered. In approximately a quarter of the simulations, the introduction of a childhood vaccination program increases the frequency of seasons with a symptomatic attack rate larger than 5%. The possibility of an overall health loss cannot be excluded.
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http://dx.doi.org/10.1186/s12916-019-1471-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6958762PMC
January 2020

Preexposure prophylaxis for men who have sex with men in the Netherlands: impact on HIV and Neisseria gonorrhoeae transmission and cost-effectiveness.

AIDS 2020 03;34(4):621-630

Department of Epidemiology and Surveillance, National Institute for Public Health and the Environment (RIVM), Bilthoven.

Objectives: To assess the impact of a preexposure prophylaxis (PrEP) programme for high-risk men who have sex with men (MSM), which includes gonorrhoea testing and treatment, on the transmission of HIV and Neisseria among MSM in the Netherlands and the cost-effectiveness of such programme with and without risk compensation (in the form of reduced condom use).

Methods: We developed a stochastic agent-based transmission model of HIV and gonorrhoea. We simulated a capped (max 2.5% of MSM) and uncapped (5.5% of MSM in 2018 declining to 3% in 2027) daily PrEP programme for high-risk MSM, with 3-monthly HIV and gonorrhoea testing, with and without risk compensation. Epidemiological outcomes were calculated from the transmission model and used in an economic model to calculate costs, quality-adjusted life-years (QALY), and incremental cost-effectiveness ratios (ICER), over 2018-2027, taking a healthcare payer perspective.

Results: Without risk compensation, PrEP can lead to a reduction of 61 or 49% in the total number of new HIV infections in 2018-2027, if the programme is uncapped or capped to 2.5% of MSM, respectively. With risk compensation, this reduction can be 63 or 46% in the uncapped and capped programmes, respectively. In all scenarios, gonorrhoea prevalence decreased after introducing PrEP. Without risk compensation, 92% of simulations were cost-effective (of which 52% cost-saving). With risk compensation, 73% of simulations were cost-effective (of which 23% was cost-saving).

Conclusion: A nationwide PrEP programme for high-risk MSM can result in substantial reductions in HIV and gonorrhoea transmission and be cost-effective, even with risk compensation.
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http://dx.doi.org/10.1097/QAD.0000000000002469DOI Listing
March 2020

Preexposure prophylaxis for men who have sex with men in the Netherlands: impact on HIV and Neisseria gonorrhoeae transmission and cost-effectiveness.

AIDS 2020 03;34(4):621-630

Department of Epidemiology and Surveillance, National Institute for Public Health and the Environment (RIVM), Bilthoven.

Objectives: To assess the impact of a preexposure prophylaxis (PrEP) programme for high-risk men who have sex with men (MSM), which includes gonorrhoea testing and treatment, on the transmission of HIV and Neisseria among MSM in the Netherlands and the cost-effectiveness of such programme with and without risk compensation (in the form of reduced condom use).

Methods: We developed a stochastic agent-based transmission model of HIV and gonorrhoea. We simulated a capped (max 2.5% of MSM) and uncapped (5.5% of MSM in 2018 declining to 3% in 2027) daily PrEP programme for high-risk MSM, with 3-monthly HIV and gonorrhoea testing, with and without risk compensation. Epidemiological outcomes were calculated from the transmission model and used in an economic model to calculate costs, quality-adjusted life-years (QALY), and incremental cost-effectiveness ratios (ICER), over 2018-2027, taking a healthcare payer perspective.

Results: Without risk compensation, PrEP can lead to a reduction of 61 or 49% in the total number of new HIV infections in 2018-2027, if the programme is uncapped or capped to 2.5% of MSM, respectively. With risk compensation, this reduction can be 63 or 46% in the uncapped and capped programmes, respectively. In all scenarios, gonorrhoea prevalence decreased after introducing PrEP. Without risk compensation, 92% of simulations were cost-effective (of which 52% cost-saving). With risk compensation, 73% of simulations were cost-effective (of which 23% was cost-saving).

Conclusion: A nationwide PrEP programme for high-risk MSM can result in substantial reductions in HIV and gonorrhoea transmission and be cost-effective, even with risk compensation.
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http://dx.doi.org/10.1097/QAD.0000000000002469DOI Listing
March 2020

Trends in governmental expenditure on vaccination programmes in the Netherlands, a historical analysis.

Vaccine 2019 09 13;37(38):5698-5707. Epub 2019 Aug 13.

Unit of PharmacoTherapy, -Epidemiology & -Economics, University of Groningen, Groningen Research Institute of Pharmacy, Groningen, the Netherlands; Faculty of Economics and Business, University of Groningen, Groningen, the Netherlands; Department of Health Sciences, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands.

Background: Health economic evaluations are often required before implementing a vaccination programme. Such evaluations rarely consider the historical context of a vaccination programme. We review the financial history of vaccination programmes in the Netherlands, and compare these to demographic and macroeconomic developments as well as avoided mortality burden.

Methods: Previously uncatalogued historical expenditures on the Dutch National Immunisation Programme (NIP) and influenza vaccination were obtained from official reports. Costs were adjusted for inflation using Consumer Price Indices and expressed in Euro of 2016. Estimates on mortality burden averted were obtained from previous research and used to calculate the ratio of expenses to averted mortality burden for vaccinations against diphtheria, tetanus, pertussis, polio, measles, mumps and rubella for birth cohorts 1953-1992.

Results: Developments towards a uniform government funded NIP started early 1950s with vaccinations against diphtheria, pertussis and tetanus, culminating in its official launch in 1957 together with polio vaccinations. Since the 1980s, expenditure increased nearly five-fold mostly due to the addition of new vaccines, while spending on already implemented vaccinations tended to decline. Overall, expenditure increased from € 5 million in 1957 to € 93 million in 2014. Relative to total healthcare expenditure, the NIP contributed little, ranging between 0.05% and 0.14%. Spending on influenza vaccination increased from € 37 million in 1996 to € 52 million in 2014, while relative to total healthcare expenditure it decreased from 0.069% to 0.055%. In 2014, 0.15% of healthcare expenditure and € 533 per birth was spent on vaccination programmes. Overall, for birth cohorts 1953-1992, € 5.4 thousand (95% confidence interval: 4.0-7.3) was expended per year-of-life-lost averted.

Conclusion: The actual costs per year-of-life gained are more favorable than estimated here since averted medical costs were not included. Although expenditure on vaccination programmes increased substantially, the contribution to overall healthcare expenditure remained small.
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http://dx.doi.org/10.1016/j.vaccine.2019.07.097DOI Listing
September 2019

Radiological Signs of Latent Tuberculosis on Chest Radiography: A Systematic Review and Meta-Analysis.

Open Forum Infect Dis 2019 Jul;6(7)

Department of Infectious Diseases, Leiden University Medical Center, the Netherlands.

Objective: Current guidelines recommend screening for latent tuberculosis infection (LTBI) with a tuberculin skin test (TST) or interferon gamma release assay (IGRA), or both. Many also recommend chest radiography (CXR), although its added value is uncertain. This systematic review assessed the prevalence of abnormalities suggestive of LTBI on CXR (LTBI-CXR lesions) and evaluated the strength of the association.

Method: We searched 4 databases up to September 2017 and systematically reviewed cross-sectional and cohort studies reporting LTBI-CXR lesions in individuals with a positive TST or IGRA, or both, result. Prevalence estimates were pooled using random effects models and odds ratios (ORs) were used to calculate risk estimates.

Results: In the 26 included studies, the pooled proportion of individuals with LTBI having LTBI-CXR lesions was 0.15 (95% confidence interval [CI], 0.12-0.18]. In 16 studies that reported on individuals with LTBI and uninfected controls, LTBI-CXR lesions were associated with a positive TST result ≥ 5 mm or ≥ 10 mm (OR, 2.45; 95% CI, 1.00-5.99; and OR, 2.06; 95% CI, 1.38-3.09, respectively) and with a positive QuantiFERON result (OR, 1.99; 95% CI, 1.17-3.39) compared to CXR in uninfected controls. Although few studies reported specified lesions, calcified nodules were most frequently reported in individuals with LTBI (proportion, 0.07; 95% CI, 0.02-0.11).

Conclusions: Lesions on CXR suggestive of previous infection with Mycobacterium tuberculosis were significantly associated with positive tests for LTBI, although the sensitivity was only 15%. This finding may have added value when detection of past LTBI is important but immunodiagnostic tests may be unreliable.
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http://dx.doi.org/10.1093/ofid/ofz313DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6667719PMC
July 2019

A Systematic Review of Social Contact Surveys to Inform Transmission Models of Close-contact Infections.

Epidemiology 2019 09;30(5):723-736

From the Interuniversity Institute for Biostatistics and Statistical Bioinformatics, Hasselt University, Agoralaan Gebouw D, Diepenbeek, Belgium.

Background: Researchers increasingly use social contact data to inform models for infectious disease spread with the aim of guiding effective policies about disease prevention and control. In this article, we undertake a systematic review of the study design, statistical analyses, and outcomes of the many social contact surveys that have been published.

Methods: We systematically searched PubMed and Web of Science for articles regarding social contact surveys. We followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines as closely as possible.

Results: In total, we identified 64 social contact surveys, with more than 80% of the surveys conducted in high-income countries. Study settings included general population (58%), schools or universities (37%), and health care/conference/research institutes (5%). The largest number of studies did not focus on a specific age group (38%), whereas others focused on adults (32%) or children (19%). Retrospective (45%) and prospective (41%) designs were used most often with 6% using both for comparison purposes. The definition of a contact varied among surveys, e.g., a nonphysical contact may require conversation, close proximity, or both. We identified age, time schedule (e.g., weekday/weekend), and household size as relevant determinants of contact patterns across a large number of studies.

Conclusions: We found that the overall features of the contact patterns were remarkably robust across several countries, and irrespective of the study details. By considering the most common approach in each aspect of design (e.g., sampling schemes, data collection, definition of contact), we could identify recommendations for future contact data surveys that may be used to facilitate comparison between studies.
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http://dx.doi.org/10.1097/EDE.0000000000001047DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6684224PMC
September 2019

Nowcasting the Number of New Symptomatic Cases During Infectious Disease Outbreaks Using Constrained P-spline Smoothing.

Epidemiology 2019 09;30(5):737-745

From the National Institute for Public Health and the Environment-RIVM, Bilthoven, the Netherlands.

During an infectious disease outbreak, timely information on the number of new symptomatic cases is crucial. However, the reporting of new cases is usually subject to delay due to the incubation period, time to seek care, and diagnosis. This results in a downward bias in the numbers of new cases by the times of symptoms onset towards the current day. The real-time assessment of the current situation while correcting for underreporting is called nowcasting. We present a nowcasting method based on bivariate P-spline smoothing of the number of reported cases by time of symptoms onset and delay. Our objective is to predict the number of symptomatic-but-not-yet-reported cases and combine these with the already reported symptomatic cases into a nowcast. We assume the underlying two-dimensional reporting intensity surface to be smooth. We include prior information on the reporting process as additional constraints: the smooth surface is unimodal in the reporting delay dimension, is (almost) zero at a predefined maximum delay and has a prescribed shape at the beginning of the outbreak. Parameter estimation is done efficiently by penalized iterative weighted least squares. We illustrate our method on a large measles outbreak in the Netherlands. We show that even with very limited information the method is able to accurately predict the number of symptomatic-but-not-yet-reported cases. This results in substantially improved monitoring of new symptomatic cases in real time.
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http://dx.doi.org/10.1097/EDE.0000000000001050DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6684223PMC
September 2019

Capturing multiple-type interactions into practical predictors of type replacement following human papillomavirus vaccination.

Philos Trans R Soc Lond B Biol Sci 2019 05;374(1773):20180298

1 Centre for Infectious Diseases Control, National Institute for Public Health and the Environment (RIVM), 3720 BA Bilthoven , The Netherlands.

Current HPV vaccines target a subset of the oncogenic human papillomavirus (HPV) types. If HPV types compete during infection, vaccination may trigger replacement by the non-targeted types. Existing approaches to assess the risk of type replacement have focused on detecting competitive interactions between pairs of vaccine and non-vaccine types. However, methods to translate any inferred pairwise interactions into predictors of replacement have been lacking. In this paper, we develop practical predictors of type replacement in a multi-type setting, readily estimable from pre-vaccination longitudinal or cross-sectional prevalence data. The predictors we propose for replacement by individual non-targeted types take the form of weighted cross-hazard ratios of acquisition versus clearance, or aggregate odds ratios of coinfection with the vaccine types. We elucidate how the hazard-based predictors incorporate potentially heterogeneous direct and indirect type interactions by appropriately weighting type-specific hazards and show when they are equivalent to the odds-based predictors. Additionally, pooling type-specific predictors proves to be useful for predicting increase in the overall non-vaccine-type prevalence. Using simulations, we demonstrate good performance of the predictors under different interaction structures. We discuss potential applications and limitations of the proposed methodology in predicting type replacement, as compared to existing approaches. This article is part of the theme issue 'Silent cancer agents: multi-disciplinary modelling of human DNA oncoviruses'.
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http://dx.doi.org/10.1098/rstb.2018.0298DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6501909PMC
May 2019

Visual tools to assess the plausibility of algorithm-identified infectious disease clusters: an application to mumps data from the Netherlands dating from January 2009 to June 2016.

Euro Surveill 2019 Mar;24(12)

Medical Statistics, Department of Biomedical Data Sciences, Leiden University Medical Center, Leiden, The Netherlands.

IntroductionWith growing amounts of data available, identification of clusters of persons linked to each other by transmission of an infectious disease increasingly relies on automated algorithms. We propose cluster finding to be a two-step process: first, possible transmission clusters are identified using a cluster algorithm, second, the plausibility that the identified clusters represent genuine transmission clusters is evaluated.AimTo introduce visual tools to assess automatically identified clusters.MethodsWe developed tools to visualise: (i) clusters found in dimensions of time, geographical location and genetic data; (ii) nested sub-clusters within identified clusters; (iii) intra-cluster pairwise dissimilarities per dimension; (iv) intra-cluster correlation between dimensions. We applied our tools to notified mumps cases in the Netherlands with available disease onset date (January 2009 - June 2016), geographical information (location of residence), and pathogen sequence data (n = 112). We compared identified clusters to clusters reported by the Netherlands Early Warning Committee (NEWC).ResultsWe identified five mumps clusters. Three clusters were considered plausible. One was questionable because, in phylogenetic analysis, genetic sequences related to it segregated in two groups. One was implausible with no smaller nested clusters, high intra-cluster dissimilarities on all dimensions, and low intra-cluster correlation between dimensions. The NEWC reports concurred with our findings: the plausible/questionable clusters corresponded to reported outbreaks; the implausible cluster did not.ConclusionOur tools for assessing automatically identified clusters allow outbreak investigators to rapidly spot plausible transmission clusters for mumps and other human-to-human transmissible diseases. This fast information processing potentially reduces workload.
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http://dx.doi.org/10.2807/1560-7917.ES.2019.24.12.1800331DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6440581PMC
March 2019

Cost-effectiveness of increased HIV testing among MSM in The Netherlands.

AIDS 2019 10;33(12):1807-1817

Department of Epidemiology and Surveillance, National Institute for Public Health and the Environment (RIVM), Bilthoven.

Objectives: To assess the cost-effectiveness of increased consistent HIV testing among MSM in the Netherlands.

Methods: Among MSM testing at sexually transmitted infection clinics in the Netherlands in 2014-2015, approximately 20% tested consistently every 6 months. We examined four scenarios with increased percentage of MSM testing every 6 months: a small and a moderate increase among all MSM; a small and a moderate increase only among MSM with at least 10 partners in the preceding 6 months. We used an agent-based model to calculate numbers of HIV infections and AIDS cases prevented with increased HIV testing. These numbers were used in an economic model to calculate costs, quality-adjusted life-years (QALYs), and incremental cost-effectiveness ratios (ICERs) due to increased testing, over 2018-2027, taking a healthcare payer perspective.

Results: A small increase in the percentage testing every 6 months among all MSM resulted in 490 averted HIV infections and an average ICER of &OV0556;27 900/QALY gained. A moderate increase among all MSM, resulted in 1380 averted HIV infections and an average ICER of &OV0556;36 700/QALY gained. Both were not cost-effective, with a &OV0556;20 000 willingness-to-pay threshold. Increasing the percentage testing every 6 months only among MSM with at least 10 partners in the preceding 6 months resulted in less averted HIV infections than increased testing among all MSM, but was on average cost-saving.

Conclusion: Increased HIV testing can prevent considerable numbers of new HIV infections among MSM, but may be cost-effective only if targeted at high-risk individuals, such as those with many partners.
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http://dx.doi.org/10.1097/QAD.0000000000002199DOI Listing
October 2019

Echovirus type 6 transmission clusters and the role of environmental surveillance in early warning, the Netherlands, 2007 to 2016.

Euro Surveill 2018 11;23(45)

Centre for Infectious Disease Control (CIb), National Institute for Public Health and the Environment (RIVM), Bilthoven, the Netherlands.

BackgroundIn the Netherlands, echovirus type 6 (E6) is identified through clinical and environmental enterovirus surveillance (CEVS and EEVS). AimWe aimed to identify E6 transmission clusters and to assess the role of EEVS in surveillance and early warning of E6. MethodsWe included all E6 strains from CEVS and EEVS from 2007 through 2016. CEVS samples were from patients with enterovirus illness. EEVS samples came from sewage water at pre-specified sampling points. E6 strains were defined by partial VP1 sequence, month and 4-digit postcode. Phylogenetic E6 clusters were detected using pairwise genetic distances. We identified transmission clusters using a combined pairwise distance in time, place and phylogeny dimensions. ResultsE6 was identified in 157 of 3,506 CEVS clinical episodes and 92 of 1,067 EEVS samples. Increased E6 circulation was observed in 2009 and from 2014 onwards. Eight phylogenetic clusters were identified; five included both CEVS and EEVS strains. Among these, identification in EEVS did not consistently precede CEVS. One phylogenetic cluster was dominant until 2014, but genetic diversity increased thereafter. Of 14 identified transmission clusters, six included both EEVS and CEVS; in two of them, EEVS identification preceded CEVS identification. Transmission clusters were consistent with phylogenetic clusters, and with previous outbreak reports. ConclusionAlgorithms using combined time-place-phylogeny data allowed identification of clusters not detected by any of these variables alone. EEVS identified strains circulating in the population, but EEVS samples did not systematically precede clinical case surveillance, limiting EEVS usefulness for early warning in a context where E6 is endemic.
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http://dx.doi.org/10.2807/1560-7917.ES.2018.23.45.1800288DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6234528PMC
November 2018

Influenza vaccination in patients with lung cancer receiving anti-programmed death receptor 1 immunotherapy does not induce immune-related adverse events.

Eur J Cancer 2018 11 24;104:182-187. Epub 2018 Oct 24.

Department of Thoracic Oncology, Antoni van Leeuwenhoek Hospital, Amsterdam, the Netherlands. Electronic address:

Background: Influenza vaccination is recommended in patients with cancer to reduce influenza-related complications. Recently, more immune-related adverse events (irAEs) were demonstrated in patients with lung cancer who were vaccinated with the trivalent seasonal influenza vaccine during anti-programmed death receptor 1 (PD-1) immunotherapy. Confirmation of these findings is essential before recommendations on influenza vaccination may be revoked.

Methods: In this cohort study in patients with lung cancer receiving nivolumab 3 mg/kg every 2 weeks during two influenza seasons (2015/16-2016/17), irAEs have been monitored. Incidence, timing and severity of irAEs were compared between vaccinated patients and non-vaccinated patients.

Findings: In a compassionate use programme, 127 patients with lung cancer had been treated with at least one dose of nivolumab during two national influenza vaccination campaigns from September until December of 2015 and 2016. Forty-two patients had received the influenza vaccine, and 85 patients were not vaccinated. Median follow-up period was 118 days (interquartile range 106-119). Mean age was 64 years (range 46-83). In vaccinated and non-vaccinated patients, the incidence of irAEs was 26% and 22%, respectively, rate ratio 1.20 (95% confidence interval [CI] 0.51-2.65). The incidence of serious irAEs was 7% and 4%, respectively, rate ratio 2.07 (95% CI 0.28-15.43). Influenza vaccination while receiving nivolumab did not result in significant differences in the rates of discontinuation, death, clinical deterioration or tumour response between the groups.

Interpretation: Influenza vaccination in patients with lung cancer receiving anti-PD-1 immunotherapy does not induce irAEs in our cohort. With this result, influenza vaccination should not be deterred from this group of patients.
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http://dx.doi.org/10.1016/j.ejca.2018.09.012DOI Listing
November 2018

[Quantifying the impact of mass vaccination programmes on notified cases in the Netherlands].

Ned Tijdschr Geneeskd 2018 09 20;162. Epub 2018 Sep 20.

Centrum Infectieziektebestrijding, RIVM, Bilthoven, Nederland.

Objective: To quantify the impact of long-standing vaccination programmes on notified cases in the Netherlands.

Design: Estimates based on model projections of historical morbidity data.

Method: We collected and digitised previously unavailable monthly case notifications of diphtheria, poliomyelitis, mumps and rubella in the Netherlands over the period 1919-2015. Poisson regression models accounting for seasonality, multi-year cycles, secular trends and auto-correlation were fit to pre-vaccination periods. Cases averted were calculated as the difference between observed and expected cases based on model projections.

Results: In the first 13 years of mass vaccinations, case notifications declined rapidly with 18,900 (95%-CI: 12,000-28,600) notified cases of diphtheria averted, 5100 (95%-CI: 2200-13,500) cases of poliomyelitis, and 1800 (95%-CI: 1000-3200) cases of mumps. Vaccination of 11-year-old girls against rubella averted 13700 (95%-CI: 1400-38,300) cases, while universal rubella vaccination averted 700 (95%-CI: 80-2300) cases.

Conclusion: These findings show that vaccination programmes have contributed substantially to the reduction of infectious diseases in the Netherlands.
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September 2018

Metropolitan versus small-town influenza.

Authors:
Jacco Wallinga

Science 2018 10;362(6410):29-30

Center for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands.

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http://dx.doi.org/10.1126/science.aav1003DOI Listing
October 2018

Inferring Pathogen Type Interactions Using Cross-sectional Prevalence Data: Opportunities and Pitfalls for Predicting Type Replacement.

Epidemiology 2018 09;29(5):666-674

From the Center for Infectious Diseases Control, National Institute for Public Health and the Environment, Bilthoven, The Netherlands.

Background: Many multivalent vaccines target only a subset of all pathogenic types. If vaccine and nonvaccine types compete, vaccination may lead to type replacement. The plausibility of type replacement has been assessed using the odds ratio (OR) of co-infections in cross-sectional prevalence data, with OR > 1 being interpreted as low risk of type replacement. The usefulness of the OR as a predictor for type replacement is debated, as it lacks a theoretical justification, and there is no framework explaining under which assumptions the OR predicts type replacement.

Methods: We investigate the values that the OR can take based on deterministic S usceptible- I infected- S usceptible and S usceptible- Infected- Recovered- S usceptible multitype transmission models. We consider different mechanisms of type interactions and explore parameter values ranging from synergistic to competitive interactions.

Results: We find that OR > 1 might mask competition because of confounding due to unobserved common risk factors and cross-immunity, as indicated by earlier studies. We prove mathematically that unobserved common risk factors lead to an elevation of the OR, and present an intuitive explanation why cross-immunity increases the OR. We find that OR < 1 is predictive for type replacement in the absence of immunity. With immunity, OR < 1 remains predictive under biologically reasonable assumptions of unidirectional interactions during infection, and an absence of immunity-induced synergism.

Conclusions: Using the OR in cross-sectional data to predict type replacement is justified, but is only unambiguous under strict assumptions. An accurate prediction of type replacement requires pathogen-specific knowledge on common risk factors and cross-immunity.
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http://dx.doi.org/10.1097/EDE.0000000000000870DOI Listing
September 2018

The Reduction of Measles Transmission During School Vacations.

Epidemiology 2018 07;29(4):562-570

From the Centre for Infectious Disease Control, Netherlands Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands.

Background: Historically, measles incidence has shown clear seasonal patterns driven by the school calendar, but since the start of mass vaccination in developed countries there are only occasional outbreaks, which may have changed the effect of school vacations on transmission. In 2013-2014, a large measles epidemic took place in a low vaccination coverage area in The Netherlands, allowing us to quantify current-day measles transmission and the effect of school vacations.

Methods: We fitted a dynamic transmission model to notification and hospitalization time series data of the Dutch 2013-2014 measles epidemic. Our primary aim was to estimate the reduction in contact rate during school vacations and the number of cases averted due to the vacation. In addition, because the summer vacations were time-staggered in three regions, we could distinguish within-region from across-region effects of school vacations.

Results: We estimated a 53% (95% credible interval: 45%, 60%) reduction in contact rate during school vacations, resulting in 4900 (3400-7100) averted cases (estimated outbreak size: 16,600 [12,600-23,200]). There was a shift from mainly local transmission during school term to mainly cross-regional transmission during vacations. With seroprevalence data, we derived a current-day estimate of 15 to 27 for R0 (number of secondary cases per primary case in a susceptible population).

Conclusions: School vacations are associated with greatly reduced overall measles transmission. However, transmission is not eliminated, and increased long-distance travel may even promote spread to other areas. Therefore, we estimate that school closure is unlikely to prevent measles epidemics unless there are still few cases and the community is well vaccinated.
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http://dx.doi.org/10.1097/EDE.0000000000000841DOI Listing
July 2018

Benefits and Challenges in Using Seroprevalence Data to Inform Models for Measles and Rubella Elimination.

J Infect Dis 2018 07;218(3):355-364

Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey.

Background: Control efforts for measles and rubella are intensifying globally. It becomes increasingly important to identify and reach remaining susceptible populations as elimination is approached.

Methods: Serological surveys for measles and rubella can potentially measure susceptibility directly, but their use remains rare. In this study, using simulations, we outline key subtleties in interpretation associated with the dynamic context of age-specific immunity, highlighting how the patterns of immunity predicted from disease surveillance and vaccination coverage data may be misleading.

Results: High-quality representative serosurveys could provide a more accurate assessment of immunity if challenges of conducting, analyzing, and interpreting them are overcome. We frame the core disease control and elimination questions that could be addressed by improved serological tools, discussing challenges and suggesting approaches to increase the feasibility and sustainability of the tool.

Conclusions: Accounting for the dynamical context, serosurveys could play a key role in efforts to achieve and sustain elimination.
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http://dx.doi.org/10.1093/infdis/jiy137DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6049004PMC
July 2018

Years of Life Lost Due to Influenza-Attributable Mortality in Older Adults in the Netherlands: A Competing-Risks Approach.

Am J Epidemiol 2018 08;187(8):1791-1798

Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, the Netherlands.

We estimated the influenza mortality burden in adults aged 60 years or older in the Netherlands in terms of years of life lost, taking into account competing mortality risks. Weekly laboratory surveillance data for influenza and other respiratory pathogens and weekly extreme temperature served as covariates in Poisson regression models fitted to weekly mortality data, specific to age group, for the period 1999-2000 through 2012-2013. Burden for age groups 60-64 years through 85-89 years was computed as years of life lost before age 90 (YLL90), using restricted mean lifetime survival analysis and accounting for competing risks. Influenza-attributable mortality burden was greatest for persons aged 80-84 years, at 914 YLL90 per 100,000 persons (95% uncertainty interval: 867, 963), followed by persons aged 85-89 years (787 YLL90/100,000; 95% uncertainty interval: 741, 834). Ignoring competing mortality risks in the computation of influenza-attributable YLL90 would lead to substantial overestimation of burden, from 3.5% for persons aged 60-64 years to 82% for those aged 80-89 years at death. Failure to account for competing mortality risks has implications for the accuracy of disease-burden estimates, especially among persons aged 80 years or older. Because the mortality burden borne by the elderly is notably high, prevention initiatives may benefit from being redesigned to more effectively prevent infection in the oldest age groups.
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http://dx.doi.org/10.1093/aje/kwy021DOI Listing
August 2018

Dose-Optimal Vaccine Allocation over Multiple Populations.

Prod Oper Manag 2018 Jan 19;27(1):143-159. Epub 2017 Oct 19.

Econometric Institute Erasmus School of Economics Erasmus University Rotterdam P.O. Box 1738 3000 DR Rotterdam The Netherlands.

Vaccination is an effective way to prevent an epidemic. It results in immunity for the vaccinated individuals, but it also reduces the infection pressure for unvaccinated people. Thus people may actually escape infection being vaccinated: the so-called "herd effect." We analytically study the relation between the herd effect and the vaccination fraction for the seminal compartmental model, which consists of a set of differential equations describing the time course of an epidemic. We prove that the herd effect is in general convex-concave in the vaccination fraction and give precise conditions on the epidemic for the convex part to arise. We derive the significant consequences of these structural insights for allocating a limited vaccine stockpile to multiple non-interacting populations. We identify for each population a unique vaccination fraction that is most efficient per dose of vaccine: our dose-optimal coverage. We characterize the solution of the vaccine allocation problem and we show the crucial importance of the dose-optimal coverage. A single dose of vaccine may be a drop in the ocean, but multiple doses together can save a population. To benefit from this, policy makers should select a subset of populations to which the vaccines are allocated. Focusing on a limited number of populations can make a significant difference, whereas allocating equally to all populations would be substantially less effective.
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http://dx.doi.org/10.1111/poms.12788DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7168135PMC
January 2018

Estimating the Population-Level Effectiveness of Vaccination Programs in the Netherlands.

Epidemiology 2018 03;29(2):215-223

Background: There are few estimates of the effectiveness of long-standing vaccination programs in developed countries. To fill this gap, we investigate the direct and indirect effectiveness of childhood vaccination programs on mortality at the population level in the Netherlands.

Methods: We focused on three communicable infectious diseases, diphtheria, pertussis, and poliomyelitis, for which we expect both direct and indirect effects. As a negative control, we used tetanus, a noncommunicable infectious disease for which only direct effects are anticipated. Mortality data from 1903 to 2012 were obtained from Statistics Netherlands. Vaccination coverage data were obtained from various official reports. For the birth cohorts 1903 through 1975, all-cause and cause-specific childhood mortality burden was estimated using restricted mean lifetime survival methods, and a model was used to describe the prevaccination decline in burden. By projecting model results into the vaccination era, we obtained the expected burden without vaccination. Program effectiveness was estimated as the difference between observed and expected mortality burden.

Results: Each vaccination program showed a high overall effectiveness, increasing to nearly 100% within 10 birth cohorts. For diphtheria, 14.9% (95% uncertainty interval [UI] = 12.3%, 17.6%) of mortality burden averted by vaccination was due to indirect protection. For pertussis, this was 32.1% (95% UI = 31.3%, 32.8%). No indirect effects were observed for poliomyelitis or tetanus with -2.4% (UI = -16.7%, 7.1%) and 0.6% (UI = -17.9%, 10.7%), respectively.

Conclusion: Vaccination programs for diphtheria and pertussis showed substantial indirect effects, providing evidence for herd protection.
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http://dx.doi.org/10.1097/EDE.0000000000000778DOI Listing
March 2018