Professional Documents
Culture Documents
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
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.
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.
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
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
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
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
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
Unvaccinated
Unvaccinated
PBE
PBE
28 (82)
28 (93)
17 (89)
2005
2008
34
30
Church, home
Home school, household
2008
19
12 years
PBE
2006
17
Work
36 years
India (D8)
Unvaccinated
Not specified
2008
14
Healthcare
20 years
Switzerland (D5)
Unvaccinated
PBE
3 (21)
2001
14
11 months
China (unknown)
Unvaccinated
Too young
2008
13
Multiple settings
15 months
Israel (D4)
Unvaccinated
2 (15)
2002
13
10 months
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
Unknownb
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.
References
1. Strebel PM, Papania MJ, Dayan GH, Halsey NA. Measles vaccine. In:
Plotkin SA, Orenstein WA, eds. Vaccines. Philadelphia: Elsevier, 2008:
35398.
2. Watson JC, Hadler SC, Dykewicz CA, Reef S, Phillips L. Measles,
mumps, and rubellavaccine use and strategies for elimination of
19.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
49.
50.
20. Office of Travel and Tourism Industries, International Trade Administration, US Department of Commerce. Final U.S. citizen air traffic
to overseas regions, Canada & Mexico 2007. Washington, DC: US
Department of Commerce, 2008. http://tinet.ita.doc.gov/view/m-2007
-O-001/index.html. Accessed 26 February 2010.
21. Office of Travel and Tourism Industries, International Trade Administration, U.S. Department of Commerce. Final U.S. citizen air traffic
to overseas regions, Canada & Mexico 2006. Washington, DC: U.S.
Department of Commerce; 2008. http://tinet.ita.doc.gov/view/m-2006
-O-001/index.html. Accessed 26 February 2010.
22. Muscat M, Bang H, Wohlfahrt J, Glismann S, Mlbak K. Measles in
Europe: an epidemiological assessment. Lancet. 2009; 373:3839.
23. World Health Organization. WHO calls for scaling up of measles vaccination. Children in affluent European countries have a higher risk of
infection. http://www.euro.who.int/en/what-we-publish/information
-for-the-media/sections/press-releases/2009/02/who-calls-for-scaling
-up-of-measles-vaccination.-children-in-affluent-european-countries
-have-a-higher-risk-of-infection. Accessed 26 February 2010.
24. Measles once again endemic in the United Kingdom. Euro Surveill
2008; 13:18919.
25. The National Health Service (NHS) Information Centre. NHS Immunisation Statistics England 200809: The NHS Information Centre.
2009. http://www.ic.nhs.uk/statistics-and-data-collections/health-and
-lifestyles/immunisation/nhs-immunisation-statistics-england-2008
-09. Accessed 26 February 2010.
26. Oster NV, Harpaz R, Redd, SB, Papania MJ. International importation of measles virusUnited States, 19932001. J Infect Dis 2004;
189(Suppl 1):S4853.
27. Rota PA, Featherstone DA, Bellini WJ. Molecular epidemiology of measles virus. Curr Top Microbiol Immunol 2009; 330:12950.
28. Centers for Disease Control and Prevention. MeaslesUnited States,
January 1April 25, 2008. http://www.cdc.gov/mmwr/preview/mmwr
html/mm57e501a1.htm. Accessed 25 February 2010.
29. Yip FY, Papania MJ, Redd SB. Measles outbreak epidemiology in the
United States, 19932001. J Infect Dis 2004; 189(Suppl 1):S5460.
30. MacIntyre CR, Gay NJ, Gidding HF, Hull BP, Gilbert GL, McIntyre
PB. A mathematical model to measure the impact of the Measles Control Campaign on the potential for measles transmission in Australia.
Int J Infect Dis 2002; 6:27782.
31. Marin M, Nguyen HQ, Langidrik JR, et al. Measles transmission and
vaccine effectiveness during a large outbreak on a densely populated
island: implications for vaccination policy. Clin Infect Dis 2006; 42:
3159
32. Watson JC, Pearson JA, Markowitz LE, et al. An evaluation of measles
revaccination among school-entry-aged children. Pediatrics 1996; 97:
6138.
33. Vitek CR, Aduddell M, Brinton MJ, Hoffman RE, Redd SC. Increased
protections during a measles outbreak of children previously vaccinated
with a second dose of measles-mumps-rubella vaccine. Pediatr Infect
Dis J 1999; 18:6203.
34. Salmon DA, Haber M, Gangarosa EJ, Philips L, Smith NJ, Chen RT.