M A J O R A R T I C L E
Health Care–Associated Measles Outbreak in the
United States After an Importation: Challenges
and Economic Impact
Sanny Y. Chen,1,2Shoana Anderson,2Preeta K. Kutty,3Francelli Lugo,4Michelle McDonald,4Paul A. Rota,3
Ismael R. Ortega-Sanchez,3Ken Komatsu,2Gregory L. Armstrong,3Rebecca Sunenshine,2,5and Jane F. Seward3
1Epidemic Intelligence Service, Office of Workforce and Career Development, Centers for Disease Control and Prevention, Atlanta, Georgia;2Bureau of
Epidemiology and Disease Control Services, Arizona Department of Health Services, Phoenix;3Division of Viral Diseases, Centers for Disease Control
and Prevention, Atlanta, Georgia;4Division of Disease Control and Prevention, Pima County Health Department, Tucson, Arizona; and5Career
Epidemiology Field Office, Office of Public Health Preparedness and Response, Centers for Disease Control and Prevention, Atlanta, Georgia
(See the editorial commentary by Ostroff, on pages 1507–9.)
initiated a predominantly health care–associated measles outbreak involving 14 cases. We investigated risk factors
that might have contributed to health care–associated transmission and assessed outbreak-associated hospital costs.
Methods. Epidemiologic data were obtained by case interviews and review of medical records. Health care
personnel (HCP) immunization records were reviewed to identify non–measles-immune HCP. Outbreak-
associated costs were estimated from 2 hospitals.
Results.Of 14 patients with confirmed cases, 7 (50%) were aged $18 years, 4 (29%) were hospitalized, 7 (50%)
acquired measles in health care settings, and all (100%) were unvaccinated or had unknown vaccination status. Of
the 11 patients (79%) who had accessed health care services while infectious, 1 (9%) was masked and isolated
promptly after rash onset. HCP measles immunity data from 2 hospitals confirmed that 1776 (25%) of 7195 HCP
lacked evidence of measles immunity. Among these HCPs, 139 (9%) of 1583 tested seronegative for measles
immunoglobulin G, including 1 person who acquired measles. The 2 hospitals spent US$799,136 responding to and
containing 7 cases in these facilities.
Conclusions. Suspecting measles as a diagnosis, instituting immediate airborne isolation, and ensuring rapidly
retrievable measles immunity records for HCPs are paramount in preventing health care–associated spread and in
minimizing hospital outbreak–response costs.
On 12 February 2008, an infected Swiss traveler visited hospital A in Tucson, Arizona, and
Measles is a highly infectious viral disease spread by
airborne transmission. During the late 1950s, an esti-
mated 3–4 million measles cases occurred annually in
the United States, with 48,000 reported hospitalizations
and 450 reported deaths [1, 2]. After implementation of
a 1-dose measles vaccine program in 1963, measles cases
decreased . In 1989, administration of a second dose
of measles, mumps, and rubella (MMR) vaccine was
recommended routinely for school children, health care
personnel (HCP), students attending post–high school
institutions, and international travelers without ac-
ceptable evidence of immunity . Elimination of en-
demic measles transmission was declared in the United
States in 2000 . During 2001–2008, a median of 56
cases (range, 37–140 cases) were reported annually, with
importations causing outbreaks among unvaccinated
populations in certain community settings .
Because of measles severity, patients often seek care
in health care settings, posing a high risk for trans-
mission to other patients and HCP [5, 6]. Studies con-
ducted during the 1980s documented that HCP have
a 2–19-fold higher risk of acquiring measles than the
general population [6, 7]. Health care–associated out-
Received 28 September 2010; accepted 30 December 2010.
Potential conflicts of interest: none reported.
Presented in part: 48th Annual Interscience Conference on Antimicrobial Agents
and Chemotherapy/Infectious Diseases Society of America (ICAAC/IDSA) 46th
Annual Meeting; Washington, DC; October 2008. Abstract 4978.
Correspondence: Sanny Y. Chen, PhD, MHS, Centers for Disease Control and
Prevention, 1600 Clifton Rd, MS E-30, Atlanta, GA 30333 (e-mail: email@example.com).
The Journal of Infectious Diseases
Published by Oxford University Press on behalf of the Infectious Diseases Society of
0022-1899 (print)/1537-6613 (online)/2011/20311-0004$14.00
Health Care–Associated Measles Outbreak in Arizona
d JID 2011:203 (1 June)
by guest on November 3, 2015
breaks can disrupt health care delivery and result in substantial
morbidity or mortality among immunocompromised persons
On 20 February 2008, a measles case was reported to the
confirmed by the Arizona State Public Health Laboratory
(ASPHL; Phoenix, AZ). Through 21 July, an additional 13
confirmed cases were identified in health care settings and the
community. This report describes the epidemiology of the out-
break, examines outbreak-associated costs and risk factors that
might have contributed to health care–associated transmission,
Case Investigation and Outbreak Response
We used the Council of State and Territorial Epidemiologists
measles clinical case definition: (1) fever (temperature, $101?F
[$38.3?C]), (2) a generalized maculopapular rash lasting $3
days, and (3) presence of cough, coryza, and/or conjunctivitis
. Confirmed cases were those that were laboratory confirmed
or met the clinical case definition and were epidemiologically
linked to another confirmed case. Suspected cases were those
in which a generalized rash illness and a fever (temperature,
$38.3?C) were present. Vaccination status was determined by
written confirmation of receipt of a measles-containing vaccine.
Self-reported receipt of vaccine without written documentation
was classified as unknown vaccination status.
After the first measles case report, Pima County Health
Department (PCHD; Tucson, AZ) and ADHS enhanced passive
surveillance and established active surveillance in health and
laboratory facilities at all 7 major community hospitals in
Tucson. Activities included daily surveillance of emergency
departments (EDs), urgent care, and inpatient and outpatient
logs for febrile rash illnesses and measles tests. Commercial
laboratories throughout the state were reminded to report
positive measles test results. A screening tool was developed
to evaluate ED patients who presented with a generalized rash
and fever, to guide infection-control measures, and to prompt
immediate reporting of suspected measles cases to PCHD.
Patients with suspected measles were interviewed to obtain
demographic, clinical, and medical information and a list of
potential contacts. Urine, serum, and nasopharyngeal specimens
were collected for laboratory testing. Recommendations were
made to place any hospitalized or ED patient in whom the
diagnosis of measles was suspected or confirmed on airborne
precautions during their period of infectiousness.
Household contacts who lacked evidence of measles immu-
nity were offered MMR vaccine or immune globulin (IG) .
Community contacts were informed of their potential exposure
through telephone calls, letters, television, radio, or print media
and instructed to contact their physicians. A hospital contact was
defined as any HCP (physicians, nurses, technicians, clerical and
support staff, trainees, and volunteers) who had worked in the
medical facility on the day of the exposure or as any patient or
visitor who had shared the same room at the same time as (or
Inpatient contacts without evidence of immunity were vacci-
nated or offered IG. Other hospital contacts who lacked evidence
of immunity were directed to special immunizations clinics.
Laboratory testing was conducted at ASPHL and confirmed at
the Centers for Disease Control and Prevention (CDC; Atlanta,
GA). Cases were classified as laboratory confirmed by demon-
stration of measles IgM antibody in acute-phase serum samples
by enzyme immunoassay (Microimmune), isolation of measles
virus in cell culture (Vero/hSLAM cells), or detection of measles
RNA by reverse-transcription polymerase chain reaction .
and sequenced to determine measles virus genotype [10, 11].
Evidence of Immunity for HCPs
We used the 1998 definition of acceptable evidence of measles
Committee on Immunization Practices and the Healthcare
Infection Control Practice Advisory Committee , modified to
exclude documentation of physician-diagnosed measles, as fol-
lows: (1) serologic evidence of immunity or (2) written confir-
mation of receipt of measles-containing vaccine according to
birth year (defined as at least 1 dose for HCP born before 1957
and 2 doses for HCP born during or after 1957).
We reviewed HCP immunization records for evidence of
measles immunity in 2 of 7 Tucson community hospitals. HCPs
without evidence of measles immunity had blood samples
drawn for serological testing and were offered MMR or IG on
the same day. A second dose was administered $28 days after
the first dose to those who were seronegative before the first
MMR vaccine dose. All HCP without evidence of immunity
were furloughed from work on days 5–21 after last exposure.
Costs were assessed in 2 hospitals. Data collected included the
number of HCPs furloughed, time spent reviewing employee
records for evidence of measles immunity (median, 15 min per
record), and time spent conducting serologic tests and admin-
istering vaccine doses (median, 10 min per HCP). Furloughed
hours were calculated by multiplying the number of HCP
furloughed, the number of days in furlough, and a normal work
shift (8 h). For the dollar value estimate of personnel time fur-
loughed or spent reviewing employee records, we used the mean
hourly earnings for full-time hospital health care practitioner
and technical occupations in Arizona ($29.39), as reported by
the US Bureau of Labor Statistics. The number of test kits or
vaccine doses was assumed to be equal to the number of titers
d JID 2011:203 (1 June)
d Chen et al
by guest on November 3, 2015
was performed from a hospital perspective and did not include
costs incurred by the state and local health departments, private
families. Better strategies are needed to ensure compliance with
current guidelines to prevent measles transmission in medical
settings [3, 5]. Hospitals that are notin compliance risk incurring
substantial costs when faced with a measles exposure. Standard
guidance for preventing measles transmission in health care set-
tings include (1) increasing measles awareness among providers,
especially among persons presenting with fever, rash, and travel
history; (2) ensuring all HCP have evidence of measles immunity
at the time of employment and have such data electronically
available at the work site; (3) allowing only HCP with evidence of
measles immunity to provide care to patients with measles ;
and (4) instituting a screening plan to identify suspected measles
cases for immediate isolation during a measles outbreak.
Centers for Disease Control and Prevention and the State of Arizona
provided funding to support this investigation.
We acknowledge the staff at the Employee Health Services at Tucson
Medical Center and Northwest Medical Center for their support and
assistance in estimating the cost of the measles outbreak, infection-control
practitioners at all 7 major community hospitals in the Tucson area and the
Measles Investigation Team for their hard work in controlling the measles
outbreak, and Kris Bisgard for careful review of the manuscript. Members
of the Measles Investigation Team are as follows: Pima County Health
Department: R. Beeson, E. Botwright, S. Daniels, G. Diaz, D. Douglas,
J. Guthrie, L. Hulette, B. Johnson, I. Luna, E. MacNeil, R. Melland,
K. Merritt, F. Miller, R. Norrish, D. Perkins, R. Peyton, K. Reeve,
N. Siemsen, A. Taylor, P. Taylor, L. Valenzuela, P. Woodcock; Arizona
Department of Health Services: A. D’Souza, L. Erhart, K. Fredrickson,
P. Gast, S. Goodykoontz, D. Herrington, W. Humble, S. Imholte, K. Lewis,
C. Martinez, J. Meyer, C. Ogden, M. Seiter, C. Tsang, V. Waddell, J. Weiss,
C. Wiedeman, C. Yu; Centers for Disease Control and Prevention (asterisks
indicate members of the Epidemic Intelligence Service) A. Allman,
W. Bellini,E.Bolyard,D. Ehrhardt*,K. Gallagher,P. Gould*,P.Gresham,J.
Leung, L. Lowe, C. Pannazo, J. Rosen*, J. Rota, D. Sarecha, A. Srinivasan,
The findings and conclusions in this report are those of the authors
and do not necessarily represent the official position of the Centers for
Disease Control and Prevention. Use of trade names and commercial
sources are for identification purposes only and does not imply endorse-
ment by the Public Health Service or the US Department of Health and
1. Orenstein WA, Papania MJ, Wharton ME. Measles elimination in the
United States. J Infect Dis 2004; 189:S1–S3.
2. Bloch AB, Orenstein WA, Stetler HC, et al. Health impact of measles
vaccination in the United States. Pediatrics 1985; 76:524–32.
3. Centers for Disease Control and Prevention. Measles, mumps,
and rubella—vaccine use and strategies for elimination of measles,
rubella, and congenital rubella syndrome and control of mumps:
recommendations of the Advisory Committee on Immunization
Practices (ACIP). MMWR Morb Mortal Wkly Rep 1998; 47:1–57.
4. Fiebelkorn AP, Redd SB, Gallagher K, et al. Measles in the United
States during the post-elimination era. J Infect Dis 2010; 202:1520–8.
5. Biellik RJ, Clements CJ. Strategies for minimizing nosocomial
measles transmission. Bull World Health Organ 1997; 75:367–75.
6. Steingart KR, Thomas AR, Dykewicz CA, Redd SC. Transmission
of measles virus in healthcare settings during a communitywide
outbreak. Infect Control Hosp Epidemiol 1999; 20:115–9.
7. Atkinson WL, Markowitz LE, Adams NC, Seastrom GR. Transmission
of measles in medical settings—United States, 1985–1989. Am J Med
1991; 91(Suppl 3B):320S–324S.
8. Centers for Disease Control and Prevention. Nationally notifiable
infectiousdiseases, UnitedStates 2009.Atlanta, GA.http://www.cdc.gov/
ncphi/disss/nndss/casedef/measles_2009.htm. Accessed 4 March 2009
9. Centers for Disease Control and Prevention. ACIP provisional
recommendations for measles-mumps-rubella (MMR) 2009 ‘evidence
of immunity’ requirements for healthcare personnel. www.cdc.gov/
vaccines/recs/provisional/default.htm. Accessed 9 March 2009
Centers for Disease Control and Prevention, Atlanta, GA.
10. World Health Organization. Standardization of the nomenclature
for describing the genetic characteristics of wild-type measles viruses.
Wkly Epidemiol Rec 1998; 73:265–72.
11. World Health Organization. New genotype of measles virus and
update on global distribution of measles genotypes. Wkly Epidemiol
Rec 2005; 40:347–51.
12. Richard JL, Masserey-Spicher V. Large measles epidemic in Switzerland
from 2006 to 2009: consequences for the elimination of measles in
Europe. Euro Surveill 2009; 14:pii: 19443.
13. Parker AA, Staggs W, Dayan GH, et al. Implications of a 2005
measles outbreak in Indiana for sustained elimination of measles in
the United States. N Engl J Med 2006; 355:447–55.
14. Rivera ME, Mason WH, Ross LA, Wright HT Jr. Nosocomial measles
infection in a pediatric hospital during a community-wide epidemic.
J Pediatr 1991; 119:183–6.
15. Grgic-Vitek M, Frelih T, Ucakar V, et al. Spotlight on measles
2010: a cluster of measles in a hospital setting in Slovenia, March 2010.
Euro Surveill 2010; 15:pii: 19573.
16. Weston KM, Dwyer DE, Ratnamohan M, et al. Nosocomial
and community transmission of measles virus genotype D8 imported
by a returning traveler from Nepal. Commun Dis Intell 2006; 30:
17. Groth C, Bottiger B, Plesner A, Christiansen A, Glismann S, Hogh B.
Nosocomial measles cluster in Denmark following an imported
case, December 2008–January 2009. Euro Surveill 2009; 14:pii: 19126.
18. SiegelJD, RhinehartE, Jackson
Infection Control Practices Advisory Committee. 2007 guideline for
isolation precautions: preventing transmission of infectious agents
inhealthcare settings. http://www.cdc.gov/ncidod/dhqp/pdf/isolation2007.
pdf. Accessed 9 March 2010.
19. Committee on Infectious Diseases, American Academy of Pediatrics.
Infection prevention and control in pediatric ambulatory settings.
Pediatrics 2007; 120:650–665. http://www.pediatrics.org/cgi/content/
full/120/3/650. Accessed 22 November 2010.
20. Helfand RF, Heath JL, Anderson LJ, Maes EF, Guris D, Bellini WJ.
Diagnosis of measles with an IgM capture EIA: the optimal timing
of specimen collection after rash onset. J Infect Dis 1997; 175:
M, ChiarelloL; Healthcare
Health Care–Associated Measles Outbreak in Arizona
d JID 2011:203 (1 June)
by guest on November 3, 2015