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MAJOR ARTICLE

Measles in the United States


during the Postelimination Era
Amy Parker Fiebelkorn, Susan B. Redd, Kathleen Gallagher, Paul A. Rota,
Jennifer Rota, William Bellini, and Jane Seward
Division of Viral Diseases, National Center for Immunization and Respiratory Diseases, Centers
for Disease Control and Prevention, Atlanta, Georgia

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 7


October 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 Control
and 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 of
America, Washington DC, 2528 October 2008 (oral presentation); Pediatric
Academic Societies Annual Conference, Honolulu, Hawaii, 36 May 2008 (platform
oral presentation).
Reprints or correspondence: Amy Parker Fiebelkorn, CDC/NCIRD MS A-47, 1600
Clifton Rd, Bldg 16, Atlanta, GA 30333 (AParker@cdc.gov).
The Journal of Infectious Diseases 2010; 202(10):15201528
This article is in the public domain, and no copyright is claimed.
0022-1899/2010/20210-0010
DOI: 10.1086/656914

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

1963, it was estimated that 34 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 recommended for all US children [2]. The first dose should
be administered at 1215 months of age and the second
dose at 46 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 vaccine is recommended. Two doses are recommended if

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Background. Measles affected entire birth cohorts in the prevaccine era but was declared eliminated in the
United 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 Disease
Control and Prevention and data on national measles-mumps-rubella (MMR) vaccination coverage during postelimination years 20012008.
Results. During 20012008, a total of 557 confirmed cases of measles (annual median no. of cases, 56) and
38 outbreaks (annual median no. of outbreaks, 4) were reported in the United States; 232 (42%) of the cases were
imported from 44 countries, including European countries. Among case-patients who were US residents, the
highest incidences of measles were among infants 611 months of age and children 1215 months of age (3.5 and
2.6 cases/1 million person-years, respectively). From 2001 through 2008, national 1-dose MMR vaccine coverage
among children 1935 months of age ranged from 91% to 93%. From 2001 through 2008, a total of 285 USresident case-patients (65%) were considered to have preventable measles (ie, the patients were eligible for vaccination but unvaccinated). During 20042008, a total of 68% of vaccine-eligible US-resident case-patients claimed
exemptions for personal beliefs.
Conclusions. The United States maintained measles elimination from 2001 through 2008 because of sustained
high vaccination coverage. Challenges to maintaining elimination include large outbreaks of measles in highly
traveled developed countries, frequent international travel, and clusters of US residents who remain unvaccinated
because of personal belief exemptions.

METHODS
Reporting of measles cases to public health authorities by
healthcare providers and clinical laboratories is legally mandated 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 Notifiable Diseases Surveillance System. The CDC performs molecular typing of measles viruses according to WHO-recommended protocols [810]. 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, European Region, Eastern Mediterranean Region, or Western Pacific 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 classified either as internationally imported (ie, measles cases in
which exposure to measles virus occurred outside the United
States 721 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 (USacquired 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 internationally 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 endemic transmission within the United States could not be established after a thorough investigation) [7, 11].
We analyzed all cases of measles reported in the United States
during 20012008. However, we differentiated between US
case-patients and foreign-visitor case-patients (ie, foreign
tourists, international students, new international adoptees, recent 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 vaccination 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. Nonpreventable 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 persons 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 vaccination coverage among children 1935 months of age from 2001
through 2008, as well as those of 2-dose coverage among adolescents from 2006 through 2008 (the only years for which
data were available), using data from the National Immunization Survey, which supplies provider-verified, populationbased 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
Measles in the Postelimination Era JID 2010:202 (15 November) 1521

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the adult is in a high-risk group (ie, healthcare workers, international travelers, or students at posthigh school educational 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 epidemiological 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 20012008.

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 1215 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-patients (66%) and 77 foreign-visitor case-patients (65%) were
unvaccinated, 80 US-resident case-patients (18%) and 12 foreign-visitor case-patients (10%) were vaccinated, and 71 USresident case-patients (16%) and 30 foreign-visitor case-patients (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 unvaccinated, 57 (18%) were vaccinated, and 70 (22%) had an unknown 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 proportion 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 children 1935 months of age ranged from 91% to 93% from 2001
through 2008 [14], and rates of 2-dose coverage among adolescents ranged from 87% to 89% from 2006 through 2008
[14, 15].
Of the 438 measles cases that occurred among US residents,

Figure 1. Reported measles cases and incidence by year, United States, 19892008. Inset, Reported measles cases and incidence by year, United
States, 20012008. Gray shading denotes the number of cases, and the black line denotes measles incidence.

1522 JID 2010:202 (15 November) Parker Fiebelkorn et al

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an annual incidence of !1 case per million population (Figure 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 14 years
of age, 45 (51%) were 1215 months of age. A total of 41 casepatients (7%) were 59 years of age, 115 (21%) were 1019
years of age, 156 (28%) were 2039 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 2039 years of age therefore comprised the majority of cases (Figure 2).
Of the 557 reported case-patients, 126 (23%) were hospitalized (annual median no. of hospitalized case-patients, 16
[range, 529 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 attributed to measles encephalitis in a 1-dosevaccinated 13-yearold 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 unknown vaccination status and an unknown history of measles
disease who developed measles pneumonitis and encephalopathy [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

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 611 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 20012008, 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 imported 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 20052008, 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 20012008 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 20012008 were D3-D9, H1, H2, and B3. These genotypes
are found in various Asian, African, and European countries.
During 20012008, there were 38 outbreaks (annual median
no. of outbreaks, 4 [range, 210 outbreaks]). Of the 557 casepatients 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, 334 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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Figure 2. Percentage of case-patients with measles, by age group (by year), in the United States, 20012008. 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 bars
denote children 14 years of age. This age group had the highest percentage of measles cases in 2004, when a multistate outbreak occurred among
toddlers adopted from China. Striped vertical bars denote those 519 years of age. This age group had the highest percentage of measles cases in
2003, 2005, and 2008, when large outbreaks occurred among unvaccinated school children. Gray bars denote adults 2039 years of age. This age
group had the highest percentage of measles cases in 2006, when a large outbreak occurred in an office building. Dark gray bars denote adults 40
years of age.

Table 1.
2008

Age Group and Vaccination Status of Patients with Reported Measles Cases, by US residence status, United States, 2001

US residents

Age group

Unvaccinated

!6 months

All

Incidence

Unvaccinated

Vaccinated

Unknown
vaccination
status

All

Total
casepatients

4 (1)

0.2

2 (100)

2 (2)

6 (1)

611 months

58 (98)

1 (2)

59 (13)

3.5

25 (100)

25 (21)

84 (15)

1215 months

24 (80)

3 (10)

3 (10)

30 (7)

2.6

13 (87)

15 (13)

45 (8)

16 months to 4 years

30 (79)

6 (16)

2 (5)

38 (9)

0.3

5 (4)

43 (8)

59 years

35 (90)

3 (8)

1 (3)

39 (9)

1019 years

71 (78)

18 (20)

2 (2)

91 (21)

2039 years

35 (30)

43 (37)

38 (33)

116 (26)

0.13

16 (40)

4059 years

26 (47)

6 (11)

23 (42)

55 (13)

0.08

3 (60)

2 (33)

6 (1)

0.01

1 (100)

60 years
Total

4 (100)

Vaccinated

Unknown
vaccination
status

Foreign visitors

4 (67)
287 (66)

0
80 (18)

71 (16)

438

1 (7)

1 (7)

5 (100)

0.3

1 (50)

1 (50)

2 (2)

41 (7)

0.3

11 (46)

5 (21)

8 (33)

24 (20)

115 (21)

6 (15)

18 (45)

40 (34)

156 (28)

2 (40)

5 (4)

60 (11)

1 (1)

0.14

77 (65)

12 (10)

30 (25)

119

7 (1)
557

Per million population.

bation periods (ie, 1324 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 personal 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 preventing measles; the vast majority of case patients were unvaccinated. 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 importations will likely continue to cause outbreaks in communities that have sizeable clusters of unvaccinated persons, posing 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 annually [1618], and 12.9 million US citizens traveled to Eu1524 JID 2010:202 (15 November) Parker Fiebelkorn et al

ropean countries annually [1921]; however, it experienced a


much smaller number of travelers to and from Africa [1621]
and Asia [1621], 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 reported thousands of cases [22, 23], primarily among unvaccinated or partially vaccinated children [24]. During the past decade in the United Kingdom, decreasing rates of 1-dose MMR
vaccination coverage (range, 91% coverage during 19971998
to 80% coverage during 20032004) [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 Kingdom. 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]. Molecular epidemiology is an important tool for confirming the
source of these importations, because measles genotypes are
geographically distributed in regions that have not yet eliminated 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 20012008 were smaller
than those occurring during the preelimination era. Before measles elimination occurring during 19932000, a total of 110 outbreaks were reported, with an average outbreak size of 16 cases
[29], compared with the 38 outbreaks reported from 2001

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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.

Table 2. Number of Patients with Preventable and Nonpreventable Reported Measles Cases (n p 438) among US
Residents, by Age, Travel History, and Measles Vaccination Status, United States, 20012008
International travel

No international travel

Vaccinated

Not vaccinated
or unknown
vaccination status

0
1

0
20a

611 months

38

59

1215 months
16 months to 4 years

1
2

11
8a

16

30

25

59 years
1019 years

1
3

5
9a

1
15

2029 years
3039 years

2
13

10a
10a

40 years
Total case-patients
Total with preventable cases
Total with nonpreventable casesd

2
25
0

25

Case-patients, by age group or case type


!6 months

Vaccinated

Not vaccinated
or unknown
vaccination status

Total

38

32
64a

39
91

12

27a

51

16

26

65

21
94
89

4
53
0

34
266
196

61
438
285

53

70

153

Case-patients with preventable measles were case-patients for whom vaccination was recommended by the Advisory Committee on
Immunization 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 nonpreventable
because 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 nonpreventable
because 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 measlescontaining 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 of
immunity, 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 19932000 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 20012008 lasted 4 incubation periods (ie, 48 days), only 73% (80 of 110) outbreaks
occurring in 19932000 lasted 4 incubation periods.
Mathematical models show that maintaining measles elimination 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 [3133]). 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 national and state levels [14, 15], there are communities and counties 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, 3941]. 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 concern about real or perceived adverse events associated with vaccines 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, homeschooled children are not covered by school-entry vaccination
requirements. Between 1991 and 2004, the average proportion
of schoolchildren whose parents claimed exemptions from vaccination 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 nonMeasles in the Postelimination Era JID 2010:202 (15 November) 1525

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medical exemption rates than states that only offer religious exemptions. States that easily grant exemptions have higher exemption rates than states with moderate and difficult processes
for granting exemptions [46].
Measles virus is highly infectious and can cause severe complications or death [1]. Susceptible individuals who remain unvaccinated 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 611 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 22224 times more likely to become infected with measles [34, 48, 49].
Healthcare providers play an important role in influencing parents 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

Table 3. Largest Measles Outbreaks in the United States during 20012008

Year

Cases,
Median age of
no.
Primary setting of outbreak case-patients
13 years
10 years

Source (genotype)
Romania (D4)
Italy (D4)

Vaccination status of
index case-patient

Reason index case Total number


was not vaccinated (%) of PBEs

Unvaccinated
Unvaccinated

PBE
PBE

28 (82)
28 (93)
17 (89)

2005
2008

34
30

Church, home
Home school, household

2008

19

Household, school, church

12 years

Possibly Japan (D5) Unvaccinated

PBE

2006

17

Work

36 years

India (D8)

Unvaccinated

Not specified

2008

14

Healthcare

20 years

Switzerland (D5)

Unvaccinated

PBE

3 (21)

2001

14

Community (exposed in orphanage abroad)

11 months

China (unknown)

Unvaccinated

Too young

2008

13

Multiple settings

15 months

Israel (D4)

Unvaccinated

2 (15)

2002

13

Child care center

10 months

The Philippines (D3) Unvaccinated

Delayed
vaccination
Too young

2003
2008

13
12

Community
Healthcare, household,
school

12 months
6 years

Unknown (H1)
Switzerland (D5)

Unvaccinated
Unvaccinated

Not specified
PBE

Unknown
8 (67)

2003

11

Boarding school

17 years

Lebanon (D4)

Unvaccinated

Unknown

2001

11

Community

16 years

Korea (H1)

Unvaccinated

Unknown but vaccine eligible


Unknown but vaccine eligible

NOTE. PBE, personal belief exemption.


a
b

However, 4 were unvaccinated and vaccine eligible.


However, 3 were unvaccinated and vaccine eligible.

1526 JID 2010:202 (15 November) Parker Fiebelkorn et al

Unknownb

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Figure 3. Importations of measles to the United States, by World Health Organization region, 20012008. Unknown denotes importations of
unknown origin.

3.
4.
5.

6.

7.

8.

9.

10.
11.

12.

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 rationales for exemptions, work with healthcare providers to reach
out to persons who have questions about vaccines, find improved methods to communicate vaccine safety information,
and continue with rapid public health containment measures
when importations of measles virus occur.

13.

14.

15.

16.

17.

Acknowledgments
We thank Cedric Brown and Claudia Chesley for their assistance with
this manuscript.

18.

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