j infect dis. 2010 parker fiebelkorn 1520 8

1520 • JID 2010:202 (15 November) • Parker Fiebelkorn et al

M A J O R A R T I C L E

Measles in the United Statesduring the Postelimination Era

Amy Parker Fiebelkorn, Susan B. Redd, Kathleen Gallagher, Paul A. Rota,Jennifer Rota, William Bellini, and Jane SewardDivision of Viral Diseases, National Center for Immunization and Respiratory Diseases, Centersfor Disease Control and Prevention, Atlanta, Georgia

Background. Measles affected entire birth cohorts in the prevaccine era but was declared eliminated in theUnited States in 2000 because of a successful measles vaccination program.

Methods. We reviewed US surveillance data on confirmed measles cases reported to the Centers for DiseaseControl and Prevention and data on national measles-mumps-rubella (MMR) vaccination coverage during post-elimination years 2001�2008.

Results. During 2001�2008, a total of 557 confirmed cases of measles (annual median no. of cases, 56) and38 outbreaks (annual median no. of outbreaks, 4) were reported in the United States; 232 (42%) of the cases wereimported from 44 countries, including European countries. Among case-patients who were US residents, thehighest incidences of measles were among infants 6–11 months of age and children 12–15 months of age (3.5 and2.6 cases/1 million person-years, respectively). From 2001 through 2008, national 1-dose MMR vaccine coverageamong children 19–35 months of age ranged from 91% to 93%. From 2001 through 2008, a total of 285 US-resident case-patients (65%) were considered to have preventable measles (ie, the patients were eligible for vac-cination but unvaccinated). During 2004–2008, a total of 68% of vaccine-eligible US-resident case-patients claimedexemptions for personal beliefs.

Conclusions. The United States maintained measles elimination from 2001 through 2008 because of sustainedhigh vaccination coverage. Challenges to maintaining elimination include large outbreaks of measles in highlytraveled developed countries, frequent international travel, and clusters of US residents who remain unvaccinatedbecause of personal belief exemptions.

Measles is a highly infectious, acute viral disease that

causes rash, respiratory symptoms, and fever. Severe

complications, which may result in death, include

pneumonia and encephalitis. In the decade before the

national measles vaccine program was implemented in

Received 2 April 2010; accepted 10 June 2010; electronically published 7October 2010.

Potential conflicts of interest: none reported.Disclaimer: The findings and conclusions in this article are those of the authors

and do not necessarily represent the views of the Centers for Disease Controland Prevention, US Department of Health and Human Services.

Financial support: No external funding sources were used to gather the data,analyze the data, or write up the findings.

Presented in part: 46th annual meeting of the Infectious Diseases Society ofAmerica, Washington DC, 25–28 October 2008 (oral presentation); PediatricAcademic Societies Annual Conference, Honolulu, Hawaii, 3–6 May 2008 (platformoral presentation).

Reprints or correspondence: Amy Parker Fiebelkorn, CDC/NCIRD MS A-47, 1600Clifton Rd, Bldg 16, Atlanta, GA 30333 ([email protected]).

The Journal of Infectious Diseases 2010; 202(10):1520–1528This article is in the public domain, and no copyright is claimed.0022-1899/2010/20210-0010DOI: 10.1086/656914

1963, it was estimated that 3–4 million people in the

United States acquired measles each year [1]. Of the

∼500,000 measles cases reported annually, 500 resulted

in death, 48,000 resulted in hospitalization, and 1000

resulted in permanent brain damage due to measles

encephalitis [1].

Achieving a high level of population immunity is the

best way to prevent measles. Accordingly, 2 doses of

measles-mumps-rubella (MMR) vaccine are recom-

mended for all US children [2]. The first dose should

be administered at 12–15 months of age and the second

dose at 4–6 years of age. Laws in every state require

age-appropriate vaccination of children enrolled in

child care facilities and documentation of evidence of

measles immunity at the time of entry into kindergarten

or first grade [3]. As the vaccinated cohorts age, all

children in kindergarten through grade 12 should be

covered by the requirements [3]. For adults without

evidence of measles immunity, one dose of MMR vac-

cine is recommended. Two doses are recommended if

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Measles in the Postelimination Era • JID 2010:202 (15 November) • 1521

the adult is in a high-risk group (ie, healthcare workers, in-

ternational travelers, or students at post–high school educa-

tional institutions) [2].

Because of the success of the measles vaccine program in

achieving and maintaining high 1- and 2-dose MMR vaccine

coverage in preschool and school-aged children and improved

control of measles throughout Central and South America,

measles was declared eliminated from the United States in 2000

[4] and from the World Health Organization (WHO) Region

of the Americas in 2002 [5]. Elimination is defined as the

absence of transmission of endemic disease (ie, no epidemio-

logical or virological evidence that measles virus transmission

is continuously occurring in a defined geographical area for

�12 months). However, in 2008, it was estimated that there

were 20 million cases of measles worldwide and 164,000 related

deaths [6]. Importation of measles virus from abroad continues

to test the status of elimination in the United States. In this

report, we summarize the epidemiology of measles in the

United States during measles postelimination years 2001–2008.

METHODS

Reporting of measles cases to public health authorities by

healthcare providers and clinical laboratories is legally man-

dated in all states. Measles cases are identified and classified

using standard case definitions and case classifications [7]. A

confirmed case of measles is either laboratory confirmed or

epidemiologically linked to a patient with laboratory-confirmed

measles infection [7]. State health departments electronically

transmit data on confirmed cases of measles to the Centers for

Disease Control and Prevention (CDC) via the National No-

tifiable Diseases Surveillance System. The CDC performs mo-

lecular typing of measles viruses according to WHO-recom-

mended protocols [8–10]. Molecular epidemiologic data

obtained from viral isolates are used to confirm the links to

outbreaks occurring in other countries. Viral isolates that are

genotyped are categorized by the WHO region (ie, African

Region, Region of the Americas, South-East Asia Region, Eu-

ropean Region, Eastern Mediterranean Region, or Western Pa-

cific Region) from which the virus was imported.

In the United States, an outbreak of measles is defined as a

chain of transmission with �3 confirmed cases. Cases are clas-

sified either as internationally imported (ie, measles cases in

which exposure to measles virus occurred outside the United

States 7–21 days before the onset of rash and in which rash

developed within 21 days of entrance into the United States,

with no known exposure to measles occurring in the United

States during that time) or acquired in the United States (US-

acquired cases; ie, case-patients either had not been outside the

United States during the 21 days before the onset of rash or

were known to have been exposed to measles within the United

States). US-acquired cases were subclassified into 4 mutually

exclusive groups: (1) import-linked cases (ie, any case in a chain

of transmission that was epidemiologically linked to an inter-

nationally imported case), (2) imported-virus cases (ie, cases

in which an epidemiologic link to an internationally imported

case was not identified but viral genetic evidence indicated an

imported measles genotype within the chain of transmission),

(3) endemic cases (ie, cases in which transmission of measles

virus was continuous for �12 months within the United

States), and (4) unknown source cases (ie, cases in which an

epidemiological or virological link to importation or to en-

demic transmission within the United States could not be es-

tablished after a thorough investigation) [7, 11].

We analyzed all cases of measles reported in the United States

during 2001–2008. However, we differentiated between US

case-patients and “foreign-visitor” case-patients (ie, foreign

tourists, international students, new international adoptees, re-

cent immigrants, refugees, and cruise ship employees) when

we calculated incidence, so we could use 2008 US Census data

as the denominator [12], as well as when we reported vacci-

nation status, because the US vaccination recommendations

apply only to its US residents. This distinction allowed the

differentiation of cases that would have been preventable had

the recommended vaccination policy been implemented. Non-

preventable cases were defined as measles cases that occurred

among US residents who either (1) had received �1 dose of

measles-containing vaccine, (2) were vaccinated as recommended

if traveling internationally, (3) were not vaccinated but had other

evidence of immunity (ie, were born before 1957 and therefore

were presumed to be immune from natural disease in childhood,

had laboratory evidence of immunity, or had documentation of

physician-diagnosed disease), or (4) belonged to a category (such

as infants !1 year of age) for whom vaccination is not routinely

recommended. “Personal belief exemptors” were defined as per-

sons who were vaccine eligible, according to recommendations

of the Advisory Committee on Immunization Practices (ACIP)

[2] or the WHO [6], but remained unvaccinated because of

personal or parental beliefs.

We examined the rates of national 1-dose measles vaccina-

tion coverage among children 19–35 months of age from 2001

through 2008, as well as those of 2-dose coverage among ad-

olescents from 2006 through 2008 (the only years for which

data were available), using data from the National Immuni-

zation Survey, which supplies provider-verified, population-

based rates of immunization with 95% confidence intervals.

RESULTS

In the United States, from 2001 through 2008, a total of 557

confirmed measles cases were reported from 37 states and the

District of Columbia (annual median no. of cases reported, 56

[range, 37 cases in 2004 to 140 cases in 2008]), representing

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Figure 1. Reported measles cases and incidence by year, United States, 1989�2008. Inset, Reported measles cases and incidence by year, UnitedStates, 2001�2008. Gray shading denotes the number of cases, and the black line denotes measles incidence.

an annual incidence of !1 case per million population (Fig-

ure 1).

Of the 557 reported case-patients, 292 (52%) were female.

The median age of the case-patients was 16 years (range, 2

weeks to 89 years of age). Ninety case-patients (16%) were !1

year of age. Of the 88 case-patients (16%) who were 1–4 years

of age, 45 (51%) were 12–15 months of age. A total of 41 case-

patients (7%) were 5–9 years of age, 115 (21%) were 10–19

years of age, 156 (28%) were 20–39 years of age, and 67 (12%)

were �40 years of age. The age groups most affected varied by

year, depending on the setting of the outbreak. In 2002, the

majority of cases occurred in infants !1 year of age, because

of an outbreak in a child care center, compared with 2006,

when a large office building was the epicenter of an outbreak

and persons 20–39 years of age therefore comprised the ma-

jority of cases (Figure 2).

Of the 557 reported case-patients, 126 (23%) were hospi-

talized (annual median no. of hospitalized case-patients, 16

[range, 5–29 case-patients]). Of these 126 case-patients, at least

5 were admitted to an intensive care unit. Two deaths were

reported, both of which occurred in 2003. One death was at-

tributed to measles encephalitis in a 1-dose–vaccinated 13-year-

old boy with chronic granulomatous disease who had received

a bone marrow transplant 3 months earlier [13]. The other

death involved a 75-year-old international traveler with an un-

known vaccination status and an unknown history of measles

disease who developed measles pneumonitis and encephalop-

athy [13].

US residents comprised 438 case-patients (79%), and foreign

visitors comprised 119 case-patients (21%) (Table 1). Among

US-resident case-patients from 2001 through 2008, infants 6–

11 months of age had the highest incidence of measles of any

age group (59 cases, or 3.5 cases/1 million person-years), and

children 12–15 months of age had the second highest incidence

(30 cases, or 2.6 cases/1 million person-years).

During all postelimination years, 287 US-resident case-pa-

tients (66%) and 77 foreign-visitor case-patients (65%) were

unvaccinated, 80 US-resident case-patients (18%) and 12 for-

eign-visitor case-patients (10%) were vaccinated, and 71 US-

resident case-patients (16%) and 30 foreign-visitor case-pa-

tients (25%) had an unknown vaccination status; most of the

patients with unknown vaccination status were adults. Of the

317 index and coindex case-patients, 190 (60%) were unvac-

cinated, 57 (18%) were vaccinated, and 70 (22%) had an un-

known vaccination status. Of the 240 nonindex (ie, secondary)

case-patients, 176 (73%) were unvaccinated, 32 (13%) were

vaccinated, and 32 (13%) had an unknown vaccination status.

Of the 308 patients with measles related to outbreaks, 229

(74%) were unvaccinated, 43 (14%) were vaccinated, and 36

(12%) had an unknown vaccination status, whereas of the 249

patients with measles not related to outbreaks, 137 (55%) were

unvaccinated, 46 (18%) were vaccinated, and 66 (27%) had an

unknown vaccination status. On an annual basis, the propor-

tion of case-patients who were unvaccinated or who had an

unknown vaccination status ranged from 73% in 2001 and 2006

to 95% in 2008.

National rates of 1-dose vaccination coverage among chil-

dren 19–35 months of age ranged from 91% to 93% from 2001

through 2008 [14], and rates of 2-dose coverage among ado-

lescents ranged from 87% to 89% from 2006 through 2008

[14, 15].

Of the 438 measles cases that occurred among US residents,

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Figure 2. Percentage of case-patients with measles, by age group (by year), in the United States, 2001�2008. Striped diagonal bars denote infants!1 year of age. This age group had the highest percentage of measles cases in 2002, when an outbreak occurred in a child care center. Black barsdenote children 1–4 years of age. This age group had the highest percentage of measles cases in 2004, when a multistate outbreak occurred amongtoddlers adopted from China. Striped vertical bars denote those 5–19 years of age. This age group had the highest percentage of measles cases in2003, 2005, and 2008, when large outbreaks occurred among unvaccinated school children. Gray bars denote adults 20–39 years of age. This agegroup had the highest percentage of measles cases in 2006, when a large outbreak occurred in an office building. Dark gray bars denote adults �40years of age.

285 (65%) were considered preventable (Table 2). More than

two-thirds (196 [69%]) of the preventable cases were acquired

in the United States. Of the 119 US-resident case-patients who

traveled internationally, 94 (79%) were unvaccinated or had an

unknown vaccination status; of these case-patients, 89 (95%)

were considered to have preventable measles, including 20

(21%) who were 6–11 months of age (Table 2). During 2004–

2008, a total of 110 (68%) of 162 vaccine-eligible US-resident

case-patients were known to be unvaccinated because they or

their parents self-declared a personal belief exemption. (Data

on reasons for remaining unvaccinated were not systematically

collected until 2004.)

During 2001–2008, a total of 232 cases (42%) were imported

from 44 countries (annual median no. of cases imported, 26

[range, 18 cases in 2002 to 54 cases in 2001]). Of the 123 im-

ported cases from 2001 through 2004, the majority (68 [55%])

were from the WHO Western Pacific Region (Figure 3), including

28 cases from China, 23 from Japan, and 10 from the Philippines.

Whereas, of the 109 imported cases from 2005 through 2008,

the WHO European Region contributed the largest number (42

cases [39%]), including 7 cases each from Italy and the United

Kingdom and 6 cases imported from Ukraine. However, India

was the country from which the largest number of imported

cases came from during 2005–2008, with 20 cases. A median of

29 US-acquired cases were reported annually (range, 10 cases in

2004 to 115 cases in 2008). The 325 US-acquired cases reported

during 2001–2008 were classified as follows: 167 (51%) were

import-linked cases, 94 (29%) were imported-virus cases, 0 were

endemic cases, and 64 (20%) cases were of an unknown source.

The transmission setting was known for 235 (72%) of the 325

US-acquired cases. Transmission occurred in the home for 71

cases (30%), in the community for 35 (15%), at church for 26

(11%), in a healthcare facility for 23 (10%), at school/college/

boarding school for 21 (9%), at a child care center for 14 (6%),

at work for 14 (6%), at home school for 10 (4%), and at other

locations for 21 cases (9%). The measles genotypes identified

during 2001–2008 were D3-D9, H1, H2, and B3. These genotypes

are found in various Asian, African, and European countries.

During 2001–2008, there were 38 outbreaks (annual median

no. of outbreaks, 4 [range, 2–10 outbreaks]). Of the 557 case-

patients reported from 2001 through 2008, a total of 308 (55%)

were outbreak-related cases. The average outbreak size was 9

cases (median no. of outbreak cases, 5 [range, 3–34 cases]).

Outbreak duration (ie, the time between the onset of rash in

the first case and that in the last case) ranged from 3 to 79

days (median outbreak duration, 27 days). Of 38 outbreaks

occurring from 2001 through 2008, a total of 6 (16%) lasted

1 incubation period (ie, �12 days), 11 (29%) lasted 2 incu-

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Table 1. Age Group and Vaccination Status of Patients with Reported Measles Cases, by US residence status, United States, 2001–2008

Age group

US residents Foreign visitors

Totalcase-

patientsUnvaccinated Vaccinated

Unknownvaccination

status All Incidencea Unvaccinated Vaccinated

Unknownvaccination

status All

!6 months 4 (100) 0 0 4 (1) 0.2 2 (100) 0 0 2 (2) 6 (1)

6�11 months 58 (98) 1 (2) 0 59 (13) 3.5 25 (100) 0 0 25 (21) 84 (15)

12�15 months 24 (80) 3 (10) 3 (10) 30 (7) 2.6 13 (87) 1 (7) 1 (7) 15 (13) 45 (8)

16 months to 4 years 30 (79) 6 (16) 2 (5) 38 (9) 0.3 5 (100) 0 0 5 (4) 43 (8)

5�9 years 35 (90) 3 (8) 1 (3) 39 (9) 0.3 1 (50) 0 1 (50) 2 (2) 41 (7)

10�19 years 71 (78) 18 (20) 2 (2) 91 (21) 0.3 11 (46) 5 (21) 8 (33) 24 (20) 115 (21)

20�39 years 35 (30) 43 (37) 38 (33) 116 (26) 0.13 16 (40) 6 (15) 18 (45) 40 (34) 156 (28)

40�59 years 26 (47) 6 (11) 23 (42) 55 (13) 0.08 3 (60) 0 2 (40) 5 (4) 60 (11)

�60 years 4 (67) 0 2 (33) 6 (1) 0.01 1 (100) 0 0 1 (1) 7 (1)

Total 287 (66) 80 (18) 71 (16) 438 0.14 77 (65) 12 (10) 30 (25) 119 557

NOTE. Data are number of cases in age group (% of age group with the vaccination status specified) or the total number of cases (% of total for age group),unless otherwise indicated.

a Per million population.

bation periods (ie, 13–24 days), 12 (32%) lasted 3 incubation

periods, and 6 (16%) lasted 4 incubation periods; 1 outbreak

each lasted 5 (3%), 6 (3%), and 7 (3%) incubation periods,

respectively. The largest outbreaks are summarized in Table 3,

with the largest 3 outbreaks occurring primarily among per-

sonal belief exemptors. The index case-patient in at least 9

(41%) of the 22 outbreaks occurring from 2004 through 2008

was a personal belief exemptor.

DISCUSSION

Measles surveillance data from 2001 through 2008 show record

low numbers of reported measles cases and small, short-lived

outbreaks, confirming that measles elimination in the United

States has been maintained. This achievement is the result of

sustained high vaccine coverage among American children [14,

15]. Two doses of measles vaccine are highly effective in pre-

venting measles; the vast majority of case patients were un-

vaccinated. In an era when 20 million cases of measles occur

globally per year, measles virus will continue to be imported

from abroad until measles is eradicated globally [6]. These im-

portations will likely continue to cause outbreaks in commu-

nities that have sizeable clusters of unvaccinated persons, pos-

ing a continued threat to the status of measles elimination in

the United States. This report also demonstrates the severity

of measles; 2 case-patients died, and 23% were hospitalized,

some with severe complications.

Measles importations reflect both the incidence of measles

in countries around the world and travel patterns. From 2006

through 2008, the United States experienced the arrival of an

average of 10.9 million nonresidents from Western Europe an-

nually [16–18], and 12.9 million US citizens traveled to Eu-

ropean countries annually [19–21]; however, it experienced a

much smaller number of travelers to and from Africa [16–21]

and Asia [16–21], where the incidence of measles is higher [6].

Since 2005, a majority of measles importations into the United

States came from the WHO European Region, which has re-

ported thousands of cases [22, 23], primarily among unvacci-

nated or partially vaccinated children [24]. During the past de-

cade in the United Kingdom, decreasing rates of 1-dose MMR

vaccination coverage (range, 91% coverage during 1997–1998

to 80% coverage during 2003–2004) [25] among children 2

years of age and 2-dose coverage among children 5 years of

age (range, 73%–76%) [25] provided inadequate population

immunity to sustain measles elimination in the United King-

dom. By 2008, endemic measles transmission in the United

Kingdom was reestablished.

Because of the volume of international travel and the high

incidence of measles in some countries, importation of measles

cases is expected to continue in the United States [26]. Mo-

lecular epidemiology is an important tool for confirming the

source of these importations, because measles genotypes are

geographically distributed in regions that have not yet elimi-

nated measles [27]. For example, genotype D5 was circulating

in large European outbreaks in 2008. Viruses with identical

sequences were detected in the 2008 California and Arizona

outbreaks, both of which had sources imported from Europe

[28].

Measles outbreaks occurring during 2001–2008 were smaller

than those occurring during the preelimination era. Before mea-

sles elimination occurring during 1993–2000, a total of 110 out-

breaks were reported, with an average outbreak size of 16 cases

[29], compared with the 38 outbreaks reported from 2001

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Table 2. Number of Patients with Preventable and Nonpreventable Reported Measles Cases ( ) among USn p 438Residents, by Age, Travel History, and Measles Vaccination Status, United States, 2001�2008

Case-patients, by age group or case type

International travel No international travel

TotalVaccinated

Not vaccinatedor unknown

vaccination status Vaccinated

Not vaccinatedor unknown

vaccination status

!6 months 0 0 0 4 46�11 months 1 20a 0 38 5912�15 months 1 11a 2 16 3016 months to 4 years 2 8a 3 25a 385�9 years 1 5a 1 32a 3910�19 years 3 9a 15 64a 9120�29 years 2 10a 12 27a 5130�39 years 13 10a 16 26a 65�40 years 2 21b 4 34c 61

Total case-patients 25 94 53 266 438Total with preventable cases 0 89 0 196 285Total with nonpreventable casesd 25 5 53 70 153

a Case-patients with preventable measles were case-patients for whom vaccination was recommended by the Advisory Committee onImmunization Practices but who had not received �1 dose of measles-containing vaccine.

b Sixteen of the 21 cases were preventable; 5 cases occurred in persons born before 1957 and were classified as nonpreventablebecause measles-containing vaccine is not recommended for that age group.

c Of the 34 cases, 22 were preventable; the other 12 cases occurred in persons born before 1957 and were classified as nonpreventablebecause measles-containing vaccine is not recommended for this age group.

d Cases were defined as nonpreventable if they occurred among US-resident case-patients who had received �1 dose of measles-containing vaccine, were vaccinated as recommended if traveling internationally, or were not vaccinated but had other evidence of immunity(ie, were born before 1957 and therefore were presumed to be immune from natural disease in childhood, had laboratory evidence ofimmunity, or had documentation of physician-diagnosed disease) or for whom vaccination is not recommended.

through 2008, for which the average size was 9 cases. Outbreak

duration during 1993–2000 ranged from 3 to 131 days (median,

29 days); in the postelimination era, outbreaks had a shorter

range (from 3 to 79 days; median, 27 days). Whereas 93% of

outbreaks (35 of 38) occurring in 2001–2008 lasted �4 incu-

bation periods (ie, �48 days), only 73% (80 of 110) outbreaks

occurring in 1993–2000 lasted �4 incubation periods.

Mathematical models show that maintaining measles elim-

ination requires that the proportion of susceptible individuals,

which is estimated using rates of MMR vaccine coverage in the

population and rates of effectiveness of the vaccine, is less than

the epidemic threshold [30]. The limited size and duration of

recent measles outbreaks in the United States can be attributed

to several factors. First, levels of national measles vaccination

coverage among preschool-aged and school-aged children are

high [14, 15]. Second, MMR vaccine is highly effective (ie, 2

MMR vaccine doses administered after 12 months of age are

95%–100% effective in preventing measles [31–33]). Finally,

there is an aggressive and effective public health response to

reported measles cases in the United States that helps limit

further disease transmission.

Despite high overall rates of measles vaccination at the na-

tional and state levels [14, 15], there are communities and coun-

ties where vaccine exemption rates are several times higher than

state averages [34, 35]. Clustering of susceptible persons in such

communities may result in population immunity below the herd

immunity threshold of 93%–95% [36] and an increased risk of

outbreaks [37, 38]. In the measles postelimination era, a majority

of the measles outbreaks that occurred in the United States were

among personal belief exemptors [28, 37, 39–41]. Salmon et al

[42] found that the most common reason that parents claimed

vaccine exemptions was fear that the vaccine might cause harm.

As the incidence of a vaccine-preventable disease like measles

decreases, the public perception tends to shift to a belief that the

severity of the disease and susceptibility to the virus have also

decreased [43]. Concurrently, over the past decade, public con-

cern about real or perceived adverse events associated with vac-

cines has increased [42, 44, 45].

Enactment and enforcement of school immunization laws

has been shown to be an important factor in achieving high

immunization coverage [3]. However, in many states, home-

schooled children are not covered by school-entry vaccination

requirements. Between 1991 and 2004, the average proportion

of schoolchildren whose parents claimed exemptions from vac-

cination because of personal belief exemptions increased [46].

All 50 states allow medical exemptions from vaccination before

school entry, 48 states allow religious exemptions (Mississippi

and West Virginia do not), and 20 states allow philosophical/

personal belief exemptions for entry into primary school [47].

States that allow personal belief exemptions have higher non-

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Figure 3. Importations of measles to the United States, by World Health Organization region, 2001�2008. “Unknown” denotes importations ofunknown origin.

Table 3. Largest Measles Outbreaks in the United States during 2001�2008

YearCases,

no. Primary setting of outbreakMedian age ofcase-patients Source (genotype)

Vaccination status ofindex case-patient

Reason index casewas not vaccinated

Total number(%) of PBEs

2005 34 Church, home 13 years Romania (D4) Unvaccinated PBE 28 (82)2008 30 Home school, household 10 years Italy (D4) Unvaccinated PBE 28 (93)2008 19 Household, school, church 12 years Possibly Japan (D5) Unvaccinated PBE 17 (89)2006 17 Work 36 years India (D8) Unvaccinated Not specified 02008 14 Healthcare 20 years Switzerland (D5) Unvaccinated PBE 3 (21)2001 14 Community (exposed in or-

phanage abroad)11 months China (unknown) Unvaccinated Too young 0

2008 13 Multiple settings 15 months Israel (D4) Unvaccinated Delayedvaccination

2 (15)

2002 13 Child care center 10 months The Philippines (D3) Unvaccinated Too young 02003 13 Community 12 months Unknown (H1) Unvaccinated Not specified Unknown2008 12 Healthcare, household,

school6 years Switzerland (D5) Unvaccinated PBE 8 (67)

2003 11 Boarding school 17 years Lebanon (D4) Unvaccinated Unknown but vac-cine eligible

Unknowna

2001 11 Community 16 years Korea (H1) Unvaccinated Unknown but vac-cine eligible

Unknownb

NOTE. PBE, personal belief exemption.a However, 4 were unvaccinated and vaccine eligible.b However, 3 were unvaccinated and vaccine eligible.

medical exemption rates than states that only offer religious ex-

emptions. States that easily grant exemptions have higher ex-

emption rates than states with moderate and difficult processes

for granting exemptions [46].

Measles virus is highly infectious and can cause severe com-

plications or death [1]. Susceptible individuals who remain un-

vaccinated may be unaware of the potential risk of acquiring

measles disease. Once a person becomes infected, there is the

risk of the virus being spread to other susceptible persons,

including those for whom vaccination is not recommended

because of medical reasons or those who are too young for

vaccination. From 2001 through 2008, infants 6–11 months of

age had the highest age-specific incidence (3.5 cases/1 million

person-years); infants in this age group are not recommended

for MMR vaccination unless they are traveling internationally.

Compared with vaccinated persons, individuals who are exempt

from vaccination are 22–224 times more likely to become in-

fected with measles [34, 48, 49].

Healthcare providers play an important role in influencing par-

ents as to whether they vaccinate their children. Nearly 40%

of parents who change their minds after considering delaying

or refusing a vaccine for their child credit information they

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receive from the child’s healthcare provider as the reason they

decided not to delay or refuse [50]. Healthcare providers play

an important role in sustaining elimination by maintaining a

high awareness of measles in international travelers and un-

protected populations and by rapidly implementing isolation

precautions if measles is suspected in a patient. In addition,

providers can facilitate measles prevention by encouraging pa-

tients who are planning international travel to be up to date

with immunizations.

The epidemiology of measles in the United States during the

postelimination era highlights the importance of implementing

existing policy recommendations. Of the 119 US-resident case-

patients who traveled internationally and were vaccine eligible,

89 (75%) were unvaccinated. Had existing MMR vaccine rec-

ommendations been followed, 285 US cases (65%) could have

been prevented. Because the second-highest age-specific inci-

dence among US residents in the postelimination era occurred

among those 12–15 months of age, providers should be en-

couraged to offer vaccination as soon as possible once children

reach 12 months of age. In addition, vaccination recommen-

dations for adults should be followed, because several sizeable

outbreaks primarily affected adults.

CONCLUSION

Despite its status as an eliminated disease in the United States,

measles importation is continuing to occur and occasionally

leads to outbreaks. Because of the widespread circulation of

measles virus, especially in highly traveled European countries,

the ease and volume of international travel, and the geographic

clustering of unvaccinated persons in the United States, the risk

for imported measles virus and subsequent spread remains. To

maintain elimination, it will be necessary to sustain high rates

of 2-dose measles vaccination coverage at the national and local

levels, understand attitudes about vaccines and parents’ ratio-

nales for exemptions, work with healthcare providers to reach

out to persons who have questions about vaccines, find im-

proved methods to communicate vaccine safety information,

and continue with rapid public health containment measures

when importations of measles virus occur.

Acknowledgments

We thank Cedric Brown and Claudia Chesley for their assistance withthis manuscript.

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