Timing of Measles Immunizatioon and Effective Population Vaccine Coverage - Magda Delicia

7/30/2019 Timing of Measles Immunizatioon and Effective Population Vaccine Coverage - Magda Delicia

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DOI: 10.1542/peds.2012-0132; originally published online August 20, 2012;2012;130;e600Pediatrics

Julia A. Bielicki, Rita Achermann and Christoph BergerTiming of Measles Immunization and Effective Population Vaccine Coverage

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Timing of Measles Immunization and Effective

Population Vaccine Coverage

WHATS KNOWN ON THIS SUBJECT: Many children are vaccinatedagainst measles with a delay. This may influence effective measles

vaccine coverage even in countries with high overall

immunization levels. Official vaccine coverage statistics do not

usually report on the impact of timeliness of measles vaccination.

WHAT THIS STUDY ADDS: Delayed measles vaccination results in

48.6% effective coverage in children aged 6 months to 2 years

when 84.5% of 25-month-olds are up-to-date for 1 measles

vaccination. Analyzing patterns of measles vaccination could help

to address low coverage in infants and toddlers.

abstractOBJECTIVE: To describe measles vaccination patterns in a cohort

of Swiss children aged up to 3 years insured with a single health

insurer.

METHODS: A dynamic cohort study evaluating measles immunizations

patterns in children born between 2006 and 2008 was conducted. Time-

to-event analysis was used to describe timing of measles immunization.

Effective vaccine coverage was calculated by using an area under the

curve approach.RESULTS: In the study cohort, 62.6% of 13-month-old children were up-to-

date for the first measles immunization (recommended at 12 months of

age). Approximately 59% of 25-month-old children were up-to-date for

the second measles immunization (recommended at 1524 months of

age). Most doses were delivered during months in a child s life when

well-child visits are recommended (eg, 12 months of age). For second

measles vaccine dose, accelerations in vaccine delivery occurred at

time points for well-child visits during the months 19 and 25 of age

but with lower final uptake than for the first measles vaccine dose.

Until their second birthday, children in our cohort spent on average 177

days and 89 days susceptible to measles due to policy recommendationsand additional delays, respectively. In a group of children aged 6 months

to 2 years reflecting the age distribution in our cohort, effective vaccine

coverage was only 48.6%.

CONCLUSIONS: Timing and timeliness of measles immunizations influ-

ence effective population vaccine coverage and should be routinely

reported in addition to coverage whenever possible. Proposed timing

and relation of recommended vaccinations to well-child visits could be

relevant aspects in optimizing measles vaccine coverage to reach

measles elimination. Pediatrics 2012;130:e600e606

AUTHORS:Julia A. Bielicki, MD, MPH,

a,b

Rita Achermann,MSc,c,d and Christoph Berger, MDa,b

aDivision of Infectious Diseases and Hospital Epidemiology, andbChildrens Research Centre, University Childrens Hospital,

Zurich, Switzerland; cHelsana Health Insurance Company,

Duebendorf, Switzerland; and dInstitute for Clinical Epidemiology

and Biostatistics, University Hospital Basel, Basel, Switzerland

KEY WORDS

immunization programs, immunization schedule, measles, time

factors, vaccination

ABBREVIATIONS

CIconfidence interval

FOPHSwiss Federal Office of Public Health

MCV1first measles vaccine dose

MCV2second measles vaccine dose

Drs Bielicki and Berger designed the study and, shaped the data

analysis with assistance from Ms Achermann. Ms Achermann

obtained anonymized data from the Helsana Health Insurance

Company database and conducted the data analysis. All authors

contributed to the interpretation of the results. Dr Bielicki

drafted and revised the manuscript. Dr Berger and Ms

Achermann commented on the initial draft and revisions and

approved the final version.

The findings and conclusions in this report are those of the

authors and do not necessarily represent the official position of

Helsana Health Insurance Company.

www.pediatrics.org/cgi/doi/10.1542/peds.2012-0132

doi:10.1542/peds.2012-0132

Accepted for publication May 10, 2012

Address correspondence to Christoph Berger, MD, Division of

Hospital Epidemiology and Infectious Disease, University

Childrens Hospital, Steinwiesstrasse 75, 8032 Zurich, Switzerland.

E-mail: [email protected]

PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).

Copyright 2012 by the American Academy of Pediatrics

FINANCIAL DISCLOSURE: Ms Achermann was head of the

division of health sciences at Helsana Health Insurance

Company when this study was conceived. There were no

financial incentives provided by the company for work on this

article. Ms Achermann has since moved to the Centre for

Biostatistics and Clinical Epidemiology at the University of Basel.

Permission was granted to complete this article after her

employment with Helsana Health Insurance Company

terminated. The other authors have indicated they have no

financial relationships relevant to this article to disclose.

FUNDING: No external funding.

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Vaccination is a key and highly suc-

cessful element of well-child care

worldwide. Over the last few decades,

effective vaccines and immunization

programshave dramatically reducedthe

impact of several vaccine-preventable

diseases on population and individualhealth.1 Adequate population coverage

to achieve high individual protection as

well as for induction and maintenance

of herd immunity is an important issue

in the fight against many vaccine-

preventable diseases.2

Despite being vaccine preventable,

measles is still a relevant disease that

continues to be a major focus for im-

munization programs.3 Available mea-

sles vaccines are highly efficacious andare an adequate instrument to elimi-

nate endemic measles transmission if

coverage is maintained at .95%, the

level necessary to achieve herd immu-

nity.2,4 After intense vaccination efforts,

interruption of endemic transmission of

measles has been achieved in Finland

and Iceland, as well as American

countries, showing that measles vac-

cines can be effective in a population

setting.

5,6

Immunization programs withcarefully chosen evidence-based rec-

ommended times for vaccination are

key to ensure that elimination of mea-

sles can be achieved.7 In addition, such

programs must be well accepted by

the target populations.8 In Switzerland,

measles vaccination coverage much

below the desirable 95% coverage has

been recorded repeatedly.9,10 Moreover,

significant delays to measles immuni-

zation have been described for 1 region

of Switzerland.11 A similar picture pres-

ents itself in many European countries,with reported vaccination coverage

#84% in 2009 for, among others, Aus-

tria, Belgium, and the United Kingdom.12

Appropriate and valid information on

vaccine coverage is crucial to main-

taining, supplementing, and expanding

measles immunization programs.7

The aims of the current study were to

assess measles immunizationlevels and

patterns in a Swiss cohort of children

bornbetween2006and2008andinsuredwith a single health insurer. Specific

objectives were to evaluate the value of

incorporating timeliness and timing of

firstand seconddose of measles vaccine

administration in describing vaccine

coverage for the study population.

METHODS

Setting

Health care in Switzerland is providedwithin a system of compulsory health

insurance administrated through a

number of federally recognized insur-

ance funds (see Supplemental Informa-

tion).13 Health insurance is divided into

basic mandatory insurance and voluntary

top-up plans covering a limited range of

additionalservices.At least 90%of costs

of vaccinations and well-child visits are

covered by basic insurance with a max-

imum annual copayment of 350 Swiss

francs. Vaccinations in Switzerland are

overwhelmingly administered by physi-cians in an office-based setting. Invoices

for outpatient care are standardized,

and vaccines can be identified by codes

or text from submitted bills.

In the Swiss national vaccination

schedule, thefirst measles vaccine dose

(MCV1) is recommended at 12 months

of age, with earlier immunization at 6 or

9 months of age advised for children

considered at high risk of exposure to

measles. For example, early measlesvaccinationfrom9monthsofagemaybe

considered for children attending day

care. The second dose (MCV2) is gen-

erally recommended at 15 to 24 months

of age. Infantswho were immunizedwith

MCV1 aged,12 months should be given

MCV2 at 12 months of age.14 Seven well-

child visits are recommended between

2 and 24 months of age (Fig 1).15

Study Design

A dynamic cohort study was conducted

retrospectively looking at claims data

from Helsana Health Insurance Com-

pany (hereafter referred to as Helsana)

inSwitzerland.Allchildrenbornbetween

January 1, 2006, and June 30, 2008,

FIGURE 1Recommendedvaccinationschedule andwell-childvisitsfor children upto 2 years of agein Switzerlandin 2011.19,20DTaP IPV +Hib,diphtheria-tetanus-acellular

pertussis vaccine, inactivated poliovirus vaccine, Haemophilus influenzaetype b conjugate vaccine; Men C, meningococcal serogroup C conjugate vaccine;

MMR, measles-mumps-rubella vaccine; PCV13, 13-valent pneumococcal conjugate vaccine.

ARTICLE

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insured from no later than 4 weeks of

age with Helsana were included. Chil-

dren with unknown places of residence

or notresidentin Switzerland at thetime

of birth were excluded.

The date of vaccination for each child in

the cohort was assumed to coincidewith the dispensing date specified on

the submittedinvoice. Each individualin

the cohort was continuously observed

from registration until the end of the

observation period on June 30, 2010.

Censoring of observation occurred at

the following events: death of the child,

change of health insurance, or erro-

neous billing for vaccines (eg, identical

invoices with treatment dates ,10

days apart).During the observation period, vacci-

nations against measles alone (Mea-

sles Vaccine [live], Pro VaccineAG, Baar,

Switzerland)orincombinationwith mumps

and rubella (Priorix, GlaxoSmithKline AG,

Mnchenbuchsee, Switzerland; M-M-

RVaxPro, Sanofi Pasteur MSD AG, Baar,

Switzerland) delivered in an ambulatory

setting were recorded as significant

events.

Data Analysis

Statistical analyses were conducted by

using R version 2.12.2 (R Foundation for

Statistical Computing, Vienna, Austria).

Health insurance data have previously

been shown to provide valid estimates

of vaccine coverage.16 Data from the

claims database were used to calcu-

late vaccination coverage by using a

time-to-event analysis.17 The age at

vaccination in days was calculatedfrom date of birth to the visit date on

submitted invoices. Inverse Kaplan-Meier

curves were plotted to display cumu-

lative measles vaccine coverage. Pro-

portion of children vaccinated with

MCV1 and MCV2 was considered at

13 and 25 months of age to reflect

immunization levels at the recom-

mended ages for measles vaccination

in Switzerland.14 Up-to-date vaccination

was defined as occurring within 30 days

of the recommended age.18 Ninety-five

percent confidence intervals (95% CIs)

were calculated by using the Greenwood

formula. All data presented are adjusted

for market share of the health insurance

on the level of canton and gender.19

To assess the validity of calculated

measles vaccination levels in our co-

hort, we compared our data against

official nationwide estimates for 24- to

35-month-old children published by the

Federal Office of Public Health (FOPH)

for 20052007.9 Official vaccine cover-

age estimates are based on data from

postal surveys with review of vaccina-

tion cards for 24- to 35-month-olds.9

The response rate to these surveys is85%. Nonrespondents are known to

be more likely German-speaking, non-

Swiss, and urban, but the exact effect

of these findings cannot be quantified.

The average measles vaccine coverage

in the same age range was calculated

from our data by using an area under

the curve approach.20 95% CIs were

calculated for these proportions with

bootstrapping (80% sample with re-

placement).The same area under thecurve approach was used to estimate

effective vaccine coverage for children

up to the age of 2 to 3 years, taking into

account any delays in immunization.20

All information in thedatabasewas fully

anonymized in accordance with Swiss

data protection laws.

RESULTS

Description of Study Cohort andAdministered Vaccine Doses

A total of 42 950 infants (52% males)

born between January 1, 2006, and

June 30, 2008, were included in the

cohort. The cohort represents just

,20% of children born in Switzerland

during the same period (19.6% for

males, 19.1% for females). The average

observation period for successive an-

nual birth cohorts was 978 days, 868

days, and 601 days for infants born in

2006, 2007, and 2008, respectively.

During the observation period, 45 605

measles-containing vaccine doses were

administered to children in our cohort.

For MCV1 and MCV2, a combination

vaccine of measles, mumps, and rubellawas used in 99.3% and 99.5% of cases,

respectively. The remaining immuniza-

tions consisted of a stand-alone mea-

sles vaccine.

There were a total of 145 invalid mea-

sles vaccinations either because of

immunization before therecommended

minimum age (before 6 months of age

for MCV1 and before 12 months of age

for MCV2, respectively; n=92)ordueto

an insufficient time interval betweenvaccinations (,4 weeks, n= 53). These

constituted 0.003% (145 of 45 605) of all

observed measles vaccinations and

were ignored for subsequent analyses.

Proportion of Children Up-to-Date

for MCV1 and MCV2

Only 62.6% (95% CI: 62.362.8) of

13-month-old children in our cohort had

received MCV1 and were up-to-date with

respect to the recommended schedule.Still, only 84.5% (95% CI: 84.384.7) of

25-month-old children had been given

MCV1. An even larger discrepancy was

noted for MCV2, with only 59.4% of

children immunized at 25 months of age

(95% CI: 59.159.6).

Measles immunization levels in the study

cohort were compared with survey-

based estimates produced by the FOPH

for the period 20052007.9 Our results

for average proportions of childrenimmunized with MCV1 and MCV2 by age

24 to 35 months broadly corresponded

to officially reported immunization lev-

els (Table 1). A basic sensitivity analysis

to explore various proportions of MCV

coverage for the nonrespondents in the

FOPH survey found that the current

data were compatible with official esti-

mates unless all nonrespondents are

unvaccinated (Table 2).

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Timeliness and Timing of Measles

Vaccination

In addition to considering measles vac-

cination statusby looking at proportion

of children up-to-date at specified time

points, theeffectof timeliness andtiming

on vaccination coverage was explored

(Fig 2).

Of the MCV1 doses in our cohort, about

one-half were administered within anarrow time band between 365 (19.6%

immunized) and 395 days (62.6% im-

munized) of age, corresponding to the

recommended age for MCV1 adminis-

tration. Another 21.9% of children re-

ceived MCV1 thereafter up to the age

of 25 months. Almost 20% of MCV1

immunizations occurred before the

generally recommended age of 12

months (2.7% immunized at 9 months,

19.4%immunized at 11 monthsof age),

probably reflecting vaccine uptake be-

fore daycare attendance.Themajorityof

MCV2 doses also were administered

during the recommended interval (6.6%

immunized at 15 months, 59.4% at 25

months). However, delivery occurred

more spread out over time, with the rate

of MCV2 vaccination accelerating at 15

monthsbut even more so during months

19 and 25 of age at times of recom-

mended well-child visits. MCV2 admin-

istration continued to occur after 25

months of age, reaching 71.2% (95% CI:

71.071.5) for 36-month-olds.

Cohort Effect of DelayedVaccination on Vulnerability to

Measles

For calculations of effective population

coverage, we assumed waning of ma-

ternal antibodiesat 6 months of age and

92.5% and 94% vaccine effectiveness

for MCV1 and MCV2, respectively.4,21

Therefore, children were taken to be

susceptible to measles from 6 months

before the recommended age for

MCV1. Taking into account the timingand timeliness of measles immuniza-

tion, children in our cohort spent on

average 266 days (95% CI: 265.1266.8)

unvaccinated and susceptible to mea-

sles until their second birthday. Of the

susceptible days, 66.5% were spent

susceptible due to the policy of rec-

ommending MCV1 for 12-month-olds

and despite early uptake of MCV1 be-

tween 9 and 12 months by 20%

in our cohort. Conversely, 33.5% of

susceptible days were due to delayed

vaccinations.

To investigate the impact of vaccination

timing and timeliness on effective cov-

erage among young children, we cal-

culated the proportion of susceptiblechildren for a hypothetic group of in-

fants and toddlers aged 6 months to

2 years. The chosen age range is rep-

resentative of a substantial propor-

tion of c hildren in day care groups in

Switzerland and elsewhere, an envi-

ronment where measles transmissions

could easily occur during an outbreak.

The relative age distribution and mea-

sles vaccination levels in this group

reflected that in our cohort. In sucha group and under the same assump-

tions as detailed previously, on average

48.6% of children are susceptible to

measles at current levels of vaccina-

tion. The recommended timing of MCV1

and the resulting 6 months that chil-

dren may spend susceptible to mea-

sles even when up-to-date with respect

to the immunization schedule had the

largest impact on effective coverage.

Inclusion of older children in this hy-pothetical group shows the additional

effects of timeliness. Among children

aged 6 months to 3 years, effective

vaccine coverage would be 61.3%, the

higher coverage largely reflecting on-

going immunization activity after the

recommended ages for MCV1 and MCV2

vaccination.

DISCUSSION

By using health insurance data for acohort of.40 000 Swiss children born

between 2006 and 2008, we were able

to demonstrate that 62.6% and 59.4% of

our cohort were up-to-date for MCV1

and MCV2 at 13 and 25 months of age,

respectively. Average coverage at 24

to 35 months of age was found to be

broadly in the range of official esti-

mates, with 85.7% and 66.7% for MCV1

and MCV2.

TABLE 1 Vaccine Coverage for 24- to 36-Month-Olds Comparing Data for the Study Cohort InsuredWith a Single Health Insurer Between 2006 and 2010 Versus Official Nationwide Postal

Survey-Derived FOPH Data for 2005 to 2007a

Data Source Age Vaccine Coverage, % (95% CI)

MCV1 MCV2

Helsana 13 mob 62.6 (62.362.8)

25 mob 84.5 (84.384.7) 59.4 (59.159.6)

2435 moc 85.7 (85.386.2) 66.7 (66.167.2)

FOPHc 2435 mo 86.9 (NA) 70.8 (NA)

NA, not available.a Data from Lang et al.9

b Cumulative proportion vaccinated at indicated age.c Calculated average proportion vaccinated in indicated age range.

TABLE 2 Calculating Range of PossibleMeasles Vaccine Coverage for

Comparison of Official Nationwide

Survey Data With the Helsana

Cohort: Sensitivity Analysis

Assuming Different Vaccination

Status Among NonrespondentsWith Official Nationwide Surveya

Assumed Vaccination

Status of

Nonrespondentsb

Calculated Vaccine

Coverage, %

MCV1 MCV2

All vaccinated 89.9 76.4

Coverage of

respondents =

nonrespondents

87.5 71.5

All unvaccinated 73.7 60.1

a Data from Lang et al.9

b Total FOPHsurveysamplesize = 9787; respondents = 8286

(84.7%).

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By conducting a time-to-event analysis,

we were able to consider the additional

impact of timeliness and timing of ad-

ministration of measles vaccine on ef-

fective vaccine coverage. In a group ofchildren aged 6 months to 3 years,

40% of children were susceptible to

measles despite a vaccination level of

71.2% for MCV2 at 36 months in our

cohort, clearly demonstrating the

combined impact of policy consid-

erations (time point for recommended

MCV1 and MCV2) and individual delayed

immunization on overall population

coverage.

Our data confirm previous observa-tions that when describing immuni-

zation levels in a given population, the

choice of reported parameters influ-

ences the interpretation of vaccine

coverage.18,20,2225 Where vaccination

achieves much of its population effect

through herd immunity, simply consid-

ering immunization levels at a given

age may overestimate protection in the

population of interest.20,22,24 The effect of

individual delayed childhood vaccina-

tions on the fraction vaccinated in

whole populations was shown to effect

whether critical population immunity

levels could be achieved.24 Time-to-eventanalysis results in a more compre-

hensive representation of population

vaccination levels than proportions of

individuals up-to-date at key ages alone.

Timing is relevant in that spread-out

vaccine delivery can result in relevant

reductionsineffectivevaccinecoverage

even when overall final uptake of vac-

cinations is similar.25 In our cohort,

most vaccinations took place during

the time periods recommended in thenational schedule. This in itself gave

rise to a considerable number of days

spent susceptible when waning im-

munity from maternal antibodies was

assumed to occur at 6 months of age.21

Thus, around two-thirds of, on average,

266 days spent unvaccinated and sus-

ceptible to measles until 2 years of age

were due to a gap between policy rec-

ommendations and waning immunity

with the remainder being down to

delay ed immunizations in the cohort.

For MCV1, timing of recommended vac-

cination seemed to be the key driver for

when children were vaccinated. Con-versely, administration of MCV2 was

drawn out during the recommended

time period of 15 to 24 months, reflect-

ing poor timeliness of vaccination.

Greater delays for later vaccinations

in young children have been noted in

other settings.26,27

At current effective coverage levels in

infants and toddlers, a double-pronged

approach may be necessary to reduce

susceptibility to measles in youngchildren. On the one hand, delays in

vaccination will need to be tackled. This

must include addressing parental

concerns and physician knowledge to

ensure children are vaccinated in a

timely fashion in the absence of medical

contraindications.2830 Because delays

in primary vaccination in thefirst months

of life are associated with reduced vacci-

nation levels against measles, an inclusive

FIGURE 2Age-related coverageforMCV1 andMCV2for thestudycohort.Theearliest timepointat which vaccinationwouldbe consideredvalidand theoptimalvaccination

periods recommended (recom) in the Swiss vaccination plan areindicated by vertical bars.19 Recommended well-childvisits are indicated as shaded bars.20

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approach to immunization programs is

necessary.31,32

Conversely, changes to recommended

timing may have to be considered when

evaluating national immunization

schedules. System factors have been

suggested as potentially havinga impactcomparable to individual level risk fac-

tors on untimely vaccination.7,24 In our

cohort, acceleration in the rate of MCV2

vaccination could be observed during

months 19 and 25 of age corresponding

to 2 well-child visits within the recom-

mended time period (Fig 2). This finding

suggests that recommendations for a

specific time point rather than a time

period may lead to better adherence,

especially if the recommended timepoint corresponds to a scheduled well-

child visit. Parental satisfaction with

preventive pediatric care in early life

is associated with fewer immunization

delays.33 Structural features of health

care systems, in particular integration

with key components of primary care

such as well-child visits, thus seem to

encourage parents to accept timely

immunization and enable providers

to offer vaccinations when mostappropriate.7

In fact, the greatest impact on effective

population coverage among preschool-

aged children is achieved by early and

timely MCV1 administration. Assuming

waning immunity from maternal anti-

bodies at 6 months and 84.5% MCV1

vaccine effectiveness for 9 to 12 month-

olds,4 immunization of all children at

9 to 12 months with MCV1 and by

13 months with MCV2 would push the

effective vaccine coverage from 60%

to 80% in a group of 6- month-olds to

3-year-olds with uniform age distribu-

tion. Well-child visits in Switzerland are

recommended at 9 and 12 months of

age. It must therefore be consideredwhether adapted recommendations for

measles vaccination to mirror these

visits(MCV1 at 9 monthsand MCV2 at 12

months of age) may improve effective

coverage in children up to 2 years of

age. This change would shorten the

period children spend at risk for mea-

sles through improved timing of vacci-

nation. However, it would ensure that

2 definitive time points coinciding with

well-child visits are recommended,thereby potentially improving timeli-

ness of vaccination.

Several limitations must be considered

in this type of analysis. Out-of-pocket

payments for vaccination and incom-

plete submissions of invoices may have

led to differential misclassifications in

the vaccination status of some children.

Overall, the proportion of infants with

a high voluntary deductible was very

small (,

1%); therefore, most likelyclaims were made extensively where

applicable. Any children receiving vac-

cinations during an inpatient stay were

not identified as immunized in our

study. Because vaccination opportuni-

ties are known to be underused in the

hospital setting, the impact of this is

likely to be small.34 Lastly, patients join-

ing from other health insurance pro-

grams during the first 2 years of life

were not observed and may differ in

vaccination behavior from patients

who remain with the same insurer

throughout their early childhood.16

CONCLUSIONSFocusing on immunization against

measles,weofferevidenceinsupportof

incorporating data on timeliness of

vaccination in the evaluation of vaccine

coverage.The goodagreement between

our data and official estimates indi-

cates the validity of using health in-

surance data. Such an analysis, using

routinely collected information, may

also be less costly. Vaccine coverage,

timeliness, and patterns of vaccinationactivity in relation to age and recom-

mended schedules can all be identified.

To move toward the eradication of en-

demic measles in Switzerland, several

measures are necessary. First, pro-

moting acceptance of measles immu-

nizationwillhelptoachievehighratesof

vaccine uptake. Second, timely appli-

cation of measles immunization at the

individual level will reduce the time any

1 child spends susceptible to measles.This must include considerations re-

garding the ages at which measles vac-

cinations are recommended. Lastly, the

relationship with overall well-child care

must be considered to reduce system

barriers to optimal measles immuniza-

tion. Such barriers may be contributing

to the slow progress toward the elimi-

nationofendemic measles inSwitzerland

and in other similar settings.

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DOI: 10.1542/peds.2012-0132; originally published online August 20, 2012;2012;130;e600Pediatrics

Julia A. Bielicki, Rita Achermann and Christoph BergerTiming of Measles Immunization and Effective Population Vaccine Coverage

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