Original Studies
Cost of Measles Containment in an Ambulatory Pediatric Clinic
Kristen A. Wendorf, MD, MS,*† Meagan Kay, DVM, MPVM,* Ismael R. Ortega-Sanchez, PhD,‡
Meaghan Munn, MPH,*§ and Jeffrey Duchin, MD*
Background: Measles is highly infectious; prompt containment of illnesses
is necessary to prevent spread. In August 2013, a 13-year-old male with
measles exposed patients and employees in a pediatric clinic. We studied
containment costs to identify avoidable costs.
Methods: Measles exposure was defined as in-person contact with or presence in the same room <2 hours after the measles patient. Costs were calculated retrospectively using published costs of measles–mumps–rubella
vaccine, cost-to-charge ratios for inpatient care in urban Washington State
and local emergency department charges for post-exposure immunoglobulin (IG). Personnel costs were calculated by multiplying hourly wages by
time for employees who worked on the response; overhead was excluded.
Results: Fifty-two patients, 60 caretakers and 10 employees were exposed.
Personnel time cost $1961. Exposed patients had a mean age of 9.6 years
(range: 2 months–19 years); 34 (65%) were fully vaccinated, and 18 (35%)
were <12 months of age and too young to be vaccinated. Five patients (10%)
were <6 months of age and required IG; 13 infants (25%) 6–11 months of age
required measles–mumps–rubella vaccination. Caretakers followed up with
their physicians for evidence of immunity. One employee had documented
evidence of immunity; 9 required measles antibody testing or vaccination.
Management of exposed persons cost $3694; overall clinic costs were $5655.
Conclusion: Responding to 1 measles case cost the pediatric clinic more
than $5000, despite isolating the patient promptly after examination. Documentation of employee immunity, vaccination of eligible patients and strict
infection control precautions might reduce ambulatory costs associated
with measles containment.
Key Words: measles, costs and cost analysis, infant, measles–mumps–
rubella vaccine
(Pediatr Infect Dis J 2015;34:589–593)
M
easles is a highly contagious disease that can lead to severe
illness, complications and death, especially among young
children.1 Before the availability of a measles vaccine in 1963,
approximately half a million cases were reported, and hundreds of
deaths occurred annually in the US.1,2
Although measles is no longer endemic in the US, measles
remains endemic in much of the Eastern Hemisphere,3 and substantial outbreaks continue to occur in Europe, Asia and Africa.4–6
Consequently, during the past decade, the vast majority of measles
cases in the US have been importations associated with unvaccinated
From the *Communicable Disease Epidemiology & Immunization Section,
Public Health—Seattle & King County, Seattle, WA; †Epidemic Intelligence
Service, Centers for Disease Control and Prevention; ‡Division of Viral
Diseases, National Center for Immunization and Respiratory Diseases, Centers
for Disease Control and Prevention; and §Council of State and Territorial
Epidemiologists, Atlanta, GA.
No funding was secured for this investigation. No financial relationships relevant
to this article. The findings and conclusions in this report are those of the
author(s) and do not necessarily represent the official position of the Centers
for Disease Control and Prevention.
Address for correspondence: Kristen Wendorf, MD, MS, Public Health—Seattle
& King County, 401 5th Ave, Suite 900, Seattle, WA 98104-1818. E-mail:
[email protected].
Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
ISSN: 0891-3668/15/3406-0589
DOI: 10.1097/INF.0000000000000682
and undervaccinated travelers and their contacts. An MMWR article
reported that during the first 8 months of 2013, approximately 99%
of 159 US cases were imported from other countries, with approximately half of the imported cases coming from Europe.7 Although
2-dose measles vaccine coverage (with measles-mumps-rubella
[MMR] vaccine) in the US remains relatively high at approximately
90% (recommended at 12–15 months and 4–6 years), the overall coverage rate can mask groups of underimmunized persons in communities who are more susceptible to measles introduction and spread.
Prompt recognition and containment of measles cases in
the US is imperative to prevent outbreaks. Economic analyses of
measles exposures have included containment costs incurred by
hospitals caring for patients with measles8 and costs incurred by
public health departments9,10 in investigating cases and controlling
further spread. Other studies have focused on the cost-effectiveness
of vaccination, which demonstrates that prevention through vaccination is more cost-effective than treatment and containment.11–13
No study has evaluated the economic effect of measles exposures
on outpatient pediatric practices, although these clinics are often
the first to treat a patient with measles.
In August 2013, an unvaccinated 13-year-old male who had
recently returned home from travel in Europe, presented to his primary pediatric clinic with a temperature of 104°F, malaise, cough,
coryza, conjunctivitis and 2 days of rash. He arrived in the waiting
room of his pediatric clinic for an appointment during the busiest time of day and was escorted into a clinic room without being
masked, although surgical masks are recommended for all patients
with respiratory symptoms old enough for the patients to wear a
mask.14 Upon evaluation, measles was suspected. After the patient
left the clinic, the exam room was not used during the next 2 hours.
Caregivers were asked to isolate the child at home until 4 days after
rash onset. The diagnosis was confirmed by both positive measlesspecific IgM and reverse transcription-polymerase chain reaction.
During the course of the clinic visit, multiple patients and their caregivers, health care providers and clinic staff were exposed to measles. We studied costs of measles case response actions related to
the ambulatory clinic exposure to more fully understand economic
consequences of measles cases for outpatient health care providers
and the health care system.
MATERIALS AND METHODS
Definitions
Measles cases were identified and classified using standard case definitions and classifications.15 Measles exposures were
defined as having had contact with or having been in the same
room as the ill patient up until 2 hours after the patient was present.
Investigation activities were defined as time spent by employees in
identifying and contacting exposed patients and employees, documenting evidence of immunity to measles, consulting with public
health regarding response activities and responding to caretakers’
concerns regarding exposure. Evidence of measles immunity was
defined as serologic evidence of immunity, laboratory evidence of
disease, birth date before 1957 or written confirmation of receipt of
1 measles vaccine after age 12 months for preschool aged patients
and their caregivers or 2 measles vaccines after 12 months for
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Wendorf et al
The Pediatric Infectious Disease Journal • Volume 34, Number 6, June 2015
school age children, adolescents and healthcare workers; healthcare personnel without evidence of immunity, regardless of postexposure vaccine, are excluded from work from days 5 to 21 after
their exposure.15,16 Costs to the health care system included costs
attributed to the vaccine program and to private insurance.
Cost Calculations
The costs to the pediatric practice related to investigation,
follow-up care and post-exposure prophylaxis response activities. Costs were calculated using data collected with a questionnaire administered to the lead health care worker who managed
the response to the measles exposure and identified the personnel
involved along with the time allocated to the response.
Activities identified in the response related to post-exposure
prophylaxis included arranging passive vaccination with intravenous
immunoglobulin (IVIG) for infants aged <6 months and identified
≤6 days after exposure (intramuscular immunoglobulin was unavailable in the local hospital) and active vaccination with MMR vaccine
≤72 hours after exposure for infants aged 6–11 months and for persons aged ≥ 12 months who did not have acceptable evidence of measles immunity.16 Investigation costs were calculated by multiplying
the hours each employee spent on specific activities by their hourly
wage. Caretakers’ exposures were discussed during the initial phone
calls with the families and contributed to the time spent during these
phone calls, but caretakers were asked to check their vaccination status and to follow up with their physicians, and caretakers’ vaccination
records were not verified by the pediatric clinic. Employee follow-up
costs were based on the bills the pediatric clinic paid for MMR vaccine doses and laboratory tests for employees.
Other costs not paid directly by the pediatric clinic but
that might contribute to the total cost of the response were also
tabulated. For example, because the pediatric clinic did not charge
patients for vaccination visits resulting from this measles exposure,
the estimated clinic costs were based on the vaccine administration
reimbursement by the Centers for Medicare and Medicaid Services
(CMS) reimbursement for code 90460 (for vaccination administration for children aged <18 years through any route with counseling by any heath care professional).17 Cost of the MMR vaccine
for patients was based on the private-sector price of purchasing
the vaccine in a pediatric clinic.18 Additionally, for follow-up care
requiring an emergency department (ED) visit for IVIG, estimated
charges were based on the lowest possible amount charged for the
ED doctor visit, IV placement with medication push and IVIG
at the local hospital treating the majority of our patients. These
charges were converted into costs by using the Washington State
average operating cost-to-charge ratio, which estimates the average
monetary value of reimbursement for acute care urban hospitals.19
Human Subjects Review
This investigation was conducted as part of a measles case
investigation by Public Health—Seattle & King County in collaboration with the affected pediatric clinic. The investigation was classified as nonresearch by the Washington State Institutional Review
Board and the Centers for Disease Control and Prevention (CDC).
RESULTS
Patient Care Follow-up Costs
Fifty-two patients with mean age of 9.6 years (range:
2 months to 19 years) were identified as having been exposed to
measles at the pediatric clinic. Of these, 34 (65%) were already
fully vaccinated; 18 (35%) were aged <12 months and unvaccinated. Five patients (10%) were aged <6 months and were referred
to an ED to receive IVIG (Fig. 1) because it was unavailable at
FIGURE 1. Post-exposure response for patients and employees exposed to measles.
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The Pediatric Infectious Disease Journal • Volume 34, Number 6, June 2015
the clinic. Thirteen (25%) exposed infants aged 6–11 months were
identified and vaccinated ≤72 hours after exposure at the pediatric
clinic. The pediatric clinic has a specific area of the clinic dedicated
to vaccinations, and these 13 patients did not need an additional
visit with the physician before vaccination. However, the clinic did
not charge the families the standard fee for vaccine administration,
which is typically reimbursed at $28.80 per patient, amounting to a
total loss of $374.40.
Investigation Costs
Four employees spent 23 hours identifying and contacting
exposed patients and caretakers, costing $1056 in employee wages.
Two employees spent another 5 hours identifying and contacting
exposed employees, costing $203 in employee wages. Additionally, 2 employees spent 6 hours in consultation with the local public health department determining a plan of action, costing $352
in employee wages. During the initial investigation, 2 employees
worked overtime to promptly identify and contact exposed persons,
costing the pediatric clinic $242 in employee overtime wages. Furthermore, 1 health care worker spent 1.5 hours on the telephone
responding to employee and patient concerns regarding the measles exposure that cost $107 in employee wages. The total cost of
employee wages to the clinic was $1961.
Employee Follow-Up Costs
Ten employees at the pediatric clinic were exposed to measles. One employee had written documentation of 2 doses of MMR
vaccine, and 9 required measles titers to determine their immune
status and to avoid being excluded from work. Measles titers were
obtained at an off-site laboratory and paid for by the pediatric clinic
at a total cost of $2704. Five employees (50%), who were either
born before 1957 or who had 1 documented previous dose of MMR
vaccine, received a dose of MMR vaccine at the pediatric clinic.
The clinic spent $616 to acquire adult MMR vaccines for staff.
Less than 1 hour was spent vaccinating these staff; employee time
spent administering vaccine was not calculated. The total amount
the pediatric clinic spent responding to employee exposures was
$3320. Titer results demonstrated serologic evidence of immunity
among all 9 tested employees. No employees were furloughed in
response to the measles exposure.
Other Costs
Because of the unique patient demographics in a pediatric
clinic, other costs were incurred as a result of this measles exposure
Measles Containment in a Pediatric Clinic
that, in this case, were not paid for by the pediatric clinic but in
other situations might be billed to the clinic. All 13 patients who
received an outbreak-related MMR vaccine were aged <12 months
but will still require 2 subsequent lifetime doses of MMR vaccine.
Thus, vaccine administered in response to the measles exposure
would be an excess cost to the health care system. In Washington
State, all childhood vaccines are paid for through the state vaccination program. However, the private-sector cost that a pediatric
clinic elsewhere would pay for 1 MMR vaccine is $56.14, which
amounts to a total cost of $730 in extra doses of MMR vaccine not
counting toward the recommended 2-dose series.
All of our patients requiring IVIG at an ED had private
insurance plans that covered the visit costs. The minimum charge
for a visit to the ED at the local hospital is $600 for these infants
who would have been billed for a brief encounter with a physician. In addition, the minimum charge for intravenous line placement with medication administration is $367, and the charge for
the IVIG medication is $480. IVIG is charged according to number
of bottles used; the smallest bottle stocked at the hospital contains
3 g of medication, which would be enough to treat infants weighing
≤7.5 kg (recommended dose of 400 mg/kg body weight).15 Thus,
the minimum charge to insurance companies is $1447 per infant.
The actual cost of treatment on the basis of the urban cost-to-charge
ratio in Washington State of $0.313 would be $452.91 per infant.
In the case of uninsured children, the charge of $1447 per infant
would be billed to the caretakers or to the pediatric clinic. The minimum total charge for the 5 infants visiting the local ED would be
$7235; CMS in an urban Washington State hospital would reimburse a total cost of $2265.
Total Costs
Overall, 122 people were exposed to measles in the pediatric
clinic, costing the clinic $5655, the health insurance system at least
$2265 and the Washington Vaccine Program $730. The total cost to
the health care system was $8650 (Table 1). Approximately 60% of
clinic’s costs were attributed to assessing measles immunity status
among exposed employees, and the remaining 40% was the cost of
identifying and treating exposed infants aged <12 months.
DISCUSSION
We documented substantial costs incurred by an ambulatory
care pediatric clinic and others in the health care system responding to a single measles exposure from an unvaccinated adolescent,
TABLE 1. Costs Related to Measles Exposure in a Pediatric Clinic
Costs to Pediatric
Clinic ($)
Identifying or contacting patients
Identifying or contacting
employees
Working with PHSKC
Employee overtime
Responding to concerns
Costs of investigation
Costs to Private
Insurance ($)
Costs to Washington State
Vaccination Program ($)
All Costs ($)
1056.17
1056.17
203.35
352.10
241.85
107.33
1960.80
203.35
352.1
241.85
107.33
1960.80
MMR vaccine administration
MMR vaccine
Patient ED visits for IVIG
Costs of patient follow-up
347.40
374.40
Employee MMR
Employee laboratory tests
Costs of employee follow-up
Total costs
616
2704
3320
5655.20
2264.56
2264.56
2264.56
729.82
347.40
729.82
2264.56
3341.78
729.82
616
2704
3320
8649.58
729.82
PHSKC, Public Health—Seattle & King County.
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Wendorf et al
The Pediatric Infectious Disease Journal • Volume 34, Number 6, June 2015
resulting in 122 additional exposures of patients, caregivers and
employees. These exposures occurred in addition to multiple community exposures in Washington and Oregon that were investigated
by 6 state health departments, 30 local health departments and at
least 1 Canadian health department. Secondary cases and additional
costs at the pediatric clinic might have been avoided because the illness was quickly diagnosed and isolated after the clinic visit, and
all eligible clinic patients and employees were previously immune.
However, the health care costs of this exposure were high, costing approximately $140 per exposure. The loss of a clinic room
for 2 hours during the busiest point of the day additionally affected
clinic operations, although these costs were not able to be evaluated. Approximately half of the total costs to the pediatric clinic
resulted from assessing measles immunity among employees; this
cost could have been eliminated if the clinic had documentation of
measles immunity status, including vaccination, for staff. For new
employees without documented immunity, vaccination or titers
could be obtained before employment, such that the results will
be immediately available in the case of a measles exposure. CDC
recommends that all persons working in medical facilities should
be vaccinated for measles because of the potential for these workers
to contract measles and transmit the disease to patients.20 However,
there are no requirements for healthcare providers in Washington
State to provide their employers with documented MMR vaccination. Our analysis indicates that it can be financially prudent for
ambulatory pediatric clinics to maintain a database of employee
evidence of immunity status.
Post-exposure measures to prevent exposed infants from
experiencing measles accounted for the majority of the total cost to
the health care system, but in our case, the cost was primarily borne
by private insurers and Washington State’s Vaccine Program. These
costs would have been higher if other exposed patients or their family
members had been incompletely vaccinated and required prophylaxis.
Costs to the pediatric clinic might also be low because in Washington
State, childhood vaccines are provided at no cost to vaccinators and
patients. Clinic costs might also increase substantially if uninsured
infants required ED visits for IVIG or intramuscular immunoglobulin
after a clinic exposure to measles. In our case, the charges for the 5
infants treated in this incident would have exceeded $7000.
Previous studies have described costs incurred by hospitals
and public health departments in response to measles cases. In
2008, a single patient with measles in Arizona infected 13 persons, 4 of whom required hospitalization. Of 7 hospitals visited
by these measles patients, none maintained records of measles
immunity; the estimated cost to just 2 of these hospitals was
$800,000, of which approximately half resulted from payment
for staff furlough because of presumptive exposure, measles disease or lack of evidence of measles immunity.8 The cost to public health departments for responding to even limited numbers of
measles cases has also been reported as substantial. In 2004, the
public health response to 3 measles cases in Iowa cost approximately $140,000,9 and in 2008, 12 cases cost the San Diego and
California public health departments approximately $125,000.21
Public health response activities, including investigation, emergency response and materials for limited outbreaks, have been
estimated at $2700–$22,000 per outbreak, although widespread
outbreaks can cost as much as $985,000.10
Minimizing patient and employee exposures is especially
important in pediatric ambulatory care clinics where measles cases
are likely to be first evaluated and where susceptible infants aged
<12 months are often present. For example, the San Diego example
of 2008 included an exposure in a pediatric clinic where 6 children were exposed to measles, 5 of which were unvaccinated and
4 of whom became ill, including 3 infants <12 months and one
2-year-old.20 Outbreaks of infectious diseases in ambulatory care
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clinics have been previously reported.22 In such outbreaks, persons
at particular risk for contracting a severe case of measles include
unvaccinated persons (including infants aged <12 months), pregnant women and immunocompromised persons.14
Exposure of susceptible patients to vaccine-preventable
diseases in the ambulatory pediatric setting might be an increasing
problem. A 2005 investigation reported that 85% of pediatricians
had encountered a child during the preceding 12 months whose
caretakers had refused at least 1 vaccination,23 and in 2011, surveyed pediatricians reported a 62% increase in vaccination refusals
during the previous 5 years.24 The most commonly refused vaccinations include MMR, varicella and influenza.24 Persons who have
not received MMR vaccine account for the vast majority of measles
cases during outbreaks in the US.7,21
To reduce spread of measles in the health care setting, the
American Academy of Pediatrics recommends triaging patients at
the time of scheduling or arrival to identify patients with symptomatic infections (especially suspected measles or varicella) and
directing symptomatic patients to a separate entrance to avoid
potentially exposing others in the waiting area. American Academy of Pediatrics also recommends prominently displaying signs
at the clinic entrance instructing caretakers to immediately notify
staff if their child has a rash or respiratory symptoms (or exposure to someone with similar symptoms) and providing surgical
masks for any coughing persons.14 Furthermore, employees should
be vaccinated and be alert to recognize respiratory illnesses and
enforce masking and isolation of such patients. Finally, contaminated rooms in which patients with suspected measles were treated
should be cleaned and not used for ≥2 hours after the infectious
person has left. In our case, the majority of exposed persons (71%)
had evidence of measles immunity, and measles containment was
successful, with no secondary cases of measles reported.
This cost analysis had some limitations. Cost questionnaires
were completed retrospectively, and therefore, they are subject to
recall bias. We do not expect the error to be substantial because we
asked the clinic to track time spent responding to the exposure while
the investigation was occurring. The cost of purchasing MMR vaccine in private clinics was estimated using 2013 data published by
CDC18 and might differ from private sector prices. A 2009 report
regarding vaccine purchase price and reimbursements per dose
noted substantial differences among 67 private pediatric and family
medicine practices studied.25 We calculated charges for ED visits
that were based on minimum charges for each component of the services provided from the billing department of the local hospital that
treated our patients. Actual charges might have been considerably
higher if patients had received more than the minimal billable services. We also estimated costs of ED visits using CMS reimbursement rates, which are likely lower than what private insurance companies pay. One study reported that in 2008 in Washington State,
physician services were reimbursed by private insurance companies at 113% of that amount reimbursed by Medicare.26 Therefore,
our analysis potentially underestimates costs and time incurred by
ambulatory pediatric clinics responding to measles exposures within
their clinics. Our analysis highlights the need for documentation of
employee vaccination status and vaccination of eligible patients in
accordance with the recommended vaccination schedule.
Imported measles infections remain a threat to U.S. populations and are often first recognized and evaluated in outpatient
clinics. Costs to prevent outbreaks related to these clinic exposures
are substantial. Vaccination of all eligible persons according to
the recommended vaccination schedule remains the most important method for preventing outbreaks and containing costs. Other
methods for mitigating costs include preemptively documenting
employee vaccination status and promptly instituting infection control measures when a case of measles is suspected.
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The Pediatric Infectious Disease Journal • Volume 34, Number 6, June 2015
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Current Abstracts
Edited by: Robert J. Leggiadro, MD
Microbiota, Antibiotics, and Obesity
Jess T. N Engl J Med. 2015; 371: 2526–8.
Obesity is a major health issue worldwide, but the background for this condition is more complex than commonly assumed. Dietary and genetic factors have but partial roles in the development of obesity. The focus in recent
years has turned to the trillions of microbes residing in the human intestine
and their possible effect on energy harvest and metabolic signaling. Studies
by Cox et al (Cell. 2014;158:705 and Nature. 2012;488:621) in this area
form the basis of this review.
Early life is a critical period both for the establishment of the intestinal microbiota and for metabolic development. Cox et al found that mice
are particularly vulnerable to exposure to low-dose penicillin during a critical time around the time of birth. Male mice whose mothers were treated
with penicillin before the birth of the pups and throughout the weaning process had a markedly altered body composition in adulthood, with increased
total mass and fat mass, increased ectopic fat deposition, increased hepatic
expression of genes involved in adipogenesis, decreased bone mineral content and increased bone area. By contrast, the body composition of adult
male mice who had received penicillin after weaning and female mice who
had received penicillin at either phase of development (just before birth or
after weaning) was more similar to that of controls.
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Cox et al also studied whether treatment with prenatally administered penicillin added to the effect of a high-fat diet in the development of
obesity. Low-dose penicillin and high-fat diet were found to have independent selective effects on the microbiota and body mass of male mice. Exposure to penicillin also resulted in substantially more fat mass in female mice
fed a high-fat diet, when compared with penicillin-exposed female mice fed
a low-fat diet. Penicillin and high-fat diet in combination, but not separately,
increased fasting insulin levels.
Whether penicillin-moderated gut microbiota would have similar
effects on body composition and metabolism if transferred to germ-free
mice was also examined by Cox et al. Cecal microbiota were transferred
from 18-week-old controls and penicillin-treated mice to 3-week-old germfree mice. The young mice that received penicillin-altered microbiota
gained total mass and fat mass at a significantly faster rate than did the mice
that received microbiota from controls.
comment: The studies by Cox et al provide evidence for the existence of
a critical window in early life, when the intestinal microbiota can influence
the development of persisting metabolic traits. Currently, however, there is
no direct evidence for a causal relation in humans. The translation of findings from mouse to humans is challenging.
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